ORIGINALARTICLE
Cretaceous West Gondwana vicarianceshaped giant water scavenger beetlebiogeographyEmmanuel F A Toussaint1dagger Devin Bloom2 and
Andrew E Z Short1
1Department of Ecology and Evolutionary
Biology and Division of Entomology
Biodiversity Institute University of Kansas
Lawrence KS 66045 USA 2Department of
Biological Sciences and Environmental amp
Sustainability Studies Program Western
Michigan University Kalamazoo MI 49008
USA
Correspondence Emmanuel F A Toussaint
Department of Ecology and Evolutionary
Biology and Division of Entomology
Biodiversity Institute University of Kansas
Lawrence KS 66045 USA
E-mail emmanueltouss1gmailcom
daggerPresent address Florida Museum of Natural
History University of Florida Gainesville
Florida 32611 USA
ABSTRACT
Aim We tested the hypothesis that ancient vicariance in giant water scavenger
beetles shaped their current distribution
Location Worldwide except Antarctica
Methods We inferred a molecular phylogenetic hypothesis for the tribe
Hydrophilini using probabilistic methods based on broad geographical and tax-
onomic sampling We used fossil-based molecular dating and likelihood
model-based ancestral range estimation to reconstruct the biogeography of this
clade
Results Our results suggest that the tribe originated in the Cretaceous about
120 Ma with a most likely ancestral range in the Gondwanan fragment com-
prising continental Africa and South America We infer an ancient vicariance
following this early origin consistent with the split of these two large land-
masses in the mid-Cretaceous The rest of the biogeographical history of the
group is shaped by dispersal events throughout the Cenozoic
Main conclusions The biogeographical history of hydrophiline water beetles
is consistent with the hypothesis of West Gondwana vicariance although an
origin in either Africa or South America is a likely alternative Although the
early cladogenesis of this clade might have been shaped by the opening of the
Atlantic Ocean subsequent biogeographical evolution is mainly driven by dis-
persal events
Keywords
Africa beetle evolution Cretaceous vicariance founder-event speciation
Hydrophilidae Hydrophilini South America West Gondwana biogeography
INTRODUCTION
The origin and biogeographical evolution of clades on Earth
is a paramount question in evolutionary biology (Lomolino
et al 2010) Several major mechanisms are commonly
invoked to explain the present-day distribution of biodiver-
sity including but not limited to dispersal vicariance and
regional extinction However it is not trivial to discriminate
among the roles played by these factors in shaping evolution-
ary histories Because of the development of increasingly
sophisticated methods to infer divergence times based on
molecular datasets and the fossil record (eg Drummond
et al 2012) and estimate ancestral ranges using model-
based approaches (reviewed in Ronquist amp Sanmartın 2011
Matzke 2013a) it is now possible to weigh the likelihood of
vicariance versus dispersal (andor regional extinction)
hypotheses in empirical studies It has been shown using
dated molecular phylogenies that disjunct distributions can
be accounted for by an ancient vicariance on the now sepa-
rated continental fragments of Gondwana Examples of such
patterns have been proposed for geckoes (Gamble et al
2008) stoneflies (McCulloch et al 2016) stag beetles (Kim
amp Farrell 2015) water beetles (Toussaint et al 2016 2017)
euedaphic ground beetles (Andujar et al 2016) and several
plant clades (eg Beaulieu et al 2013 Thomas et al 2014
Mennes et al 2015 Milner et al 2015 Berger et al 2016
Luebert et al 2017) Nevertheless a majority of clades
exhibiting potential Gondwanan vicariant patterns remain to
be explored using molecular dated approaches These might
be crucial to understand the relative contributions of
ordf 2017 John Wiley amp Sons Ltd httpwileyonlinelibrarycomjournaljbi 1doi101111jbi12977
Journal of Biogeography (J Biogeogr) (2017)
vicariance and dispersal in governing biodiversity assembly
through space and time in the Southern Hemisphere
The tribe Hydrophilini includes some of the most com-
mon and recognizable members of the water beetle family
Hydrophilidae Commonly referred to as the giant water
scavenger beetles the lineage includes some of the largest
aquatic beetles in the world with some exceeding five cen-
timetres in length Members are easily distinguished by a
sharply delimited lsquosternal keelrsquo that is formed by the fusion
and elongation of the meso- and metaventrites The mono-
phyly of the tribe has been strongly supported by cladistic
analyses based both on morphological (Short 2010) and
molecular (Short amp Fikacek 2013) data Taxa within the
Hydrophilini occupy a relatively narrow range of aquatic
habitats preferring open standing waters or the sluggish
margins and side pools of streams and rivers There are cur-
rently seven genera recognized within the tribe all of which
are easily diagnosed by suites of distinct morphological
synapomorphies (Short 2010) However the interrelation-
ships among these genera remain poorly understood
Giant water scavenger beetles are found in all the worldrsquos
biogeographical regions except Antarctica However this
diversity is not evenly distributed the majority of the grouprsquos
200 species are found in tropical regions and South America
alone is home to more than half of the known species (Short
amp Fikacek 2011) The tribe is one of the most fossil-rich
among the Hydrophilidae and its crown age was recently
estimated to be older than 120 million years ago (Ma)
(Bloom et al 2014 Toussaint et al 2016) Consequently
the diversification and biogeographical dynamics of this
lineage have been unfolding since before the breakup of
Gondwana
Using DNA sequence data from four loci and a broad tax-
onomic and geographic sampling we present the most
detailed phylogenetic and biogeographical analyses of the
tribe Hydrophilini to date to (1) infer the evolutionary rela-
tionships within the lineage (2) refine the age of the tribe
and its major clades and (3) reconstruct the biogeographical
history of the tribe to investigate the biogeographical origins
of hydrophiline diversity We specifically aim at testing the
contribution of vicariance versus dispersal in shaping the
biogeography of Hydrophilini
MATERIALS AND METHODS
Taxon sampling
In total 69 species out of approximately 200 described
(Short amp Fikacek 2011 unpublished data) from six of the
seven currently recognized genera were included (the sev-
enth the monotypic Protistolophus is only known from the
holotype collected in Venezuela) (see Appendix S1 in Sup-
porting Information for more details) Within the six genera
taxa were broadly sampled both taxonomically including 10
of the 12 included subgenera and geographically sampling
species from each genus across all biogeographical regions in
which they occur except for Australian representatives of
Hydrobiomorpha Most missing species belong to the genera
Hydrobiomorpha and Tropisternus and within these missing
taxa a large fraction is concentrated in South America Nev-
ertheless we have a good representation of Neotropical taxa
for these genera in our taxonomic sampling and therefore
are unlikely to lack major lineages Additionally missing
Neotropical species are supported as falling within already-
sampled Neotropical clades in Hydrobiomorpha both Old
and New World clades have unique synapomorphies of the
parameres of the male genitalia and have previously been
resolved as reciprocally monophyletic clades (Short 2010)
In Hydrophilus the missing Neotropical species are primarily
members of the subgenus Dibolocelus a lineage endemic to
South America except for one Nearctic species that we have
already included The well-defined genus Tropisternus does
not occur in the Old World and so any missing Neotropical
taxa would group with existing New World lineages There-
fore based on morphological evidence (Short 2010) we are
confident that most of the taxonomic and geographic diver-
sity of the tribe is represented in our sampling therefore
limiting possible biases in biogeographical analyses We
selected several outgroups including multiple representatives
of the sister tribe Hydrobiusini two more distant outgroups
from the tribes Amphiopini and Berosini and a representa-
tive of the closely related family Epimetopidae The selection
of outgroups was based on the most recent phylogenetic
studies of the family Hydrophilidae (Short amp Fikacek 2013
Toussaint et al 2016)
Molecular methods
From the dataset of Short amp Fikacek (2013) we used the
sequences of Hydrochara obtusata Sternolophus marginicollis
Tropisternus affinis T collaris and T lateralis as well as our
selection of outgroups All other Hydrophilini species used
in this study (64 in total) were sequenced de novo from
freshly collected tissues (see Table S1 for more information)
Specimens were preserved in 96 ethanol and kept frozen at
20 degC or below In a few cases pinned museum specimens
were used Total genomic DNA was extracted from legs with
a DNeasy kit (Qiagen Alameda CA USA)
Four gene fragments were amplified a 1764-bp fragment
of 18S rDNA a 696-bp fragment of arginine kinase (ARK) a
1025-bp fragment of 28S rDNA and a 750-bp fragment of
cytochrome oxidase 1 (CO1) Primers polymerase chain
reaction ingredients and thermocycler conditions were iden-
tical to those described in Short amp Fikacek (2013)
Trace files were edited and assembled in Geneious R
805 (Biomatters httpwwwgeneiouscom) All gene frag-
ments were aligned and refined using Muscle (Edgar
2004) as implemented in Geneious with default settings
Final alignments were adjusted by eye The final concate-
nated alignment consisted of 4235 sites Newly generated
sequences are deposited in GenBank under accession num-
bers KY554217-KY554442
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
2
E F A Toussaint et al
Phylogenetic analyses
We inferred gene fragment tree topologies in a maximum
likelihood (ML) framework using Iq-Tree 15 (Nguyen
et al 2015) as implemented on the W-Iq-Tree web server
(httpiqtreecibivunivieacat Trifinopoulos et al 2016)
The different gene fragment alignments were left unparti-
tioned and the models of substitution were estimated using
the Auto function and selected using the Akaike information
criterion corrected (AICc) After confirming there was no
significant incongruence (Bootstrap value BS lt 70) among
gene fragment topologies (see Appendix S2) we combined
these into a concatenate matrix for analysis
We used Bayesian inference (BI) to reconstruct phyloge-
netic relationships in Hydrophilini using the concatenated
matrix The partitions and corresponding models of substitu-
tion were selected under PartitionFinder 111 (Lanfear
et al 2012) using the lsquogreedyrsquo algorithm the lsquomrbayesrsquo set of
models and the AICc Phylogenetic analyses were performed
using MrBayes 326 (Ronquist et al 2012) as implemented
on CIPRES (Miller et al 2010) Two simultaneous and inde-
pendent runs consisting of eight MCMC (one cold and seven
incrementally heated) running 30 million generations were
used with a tree sampling every 5000 generations to calcu-
late posterior probabilities (PP) We assessed convergence of
the runs by investigating the average standard deviation of
split frequencies and effective sample size (ESS) of all param-
eters in Tracer 15 (httpBEASTbioedacukTracer) A
value of ESS gt 200 was acknowledged as a good indicator of
convergence After discarding 25 of the trees as burn-in
the remaining trees in the posterior sample were pooled to
generate a 50 majority-rule consensus tree
W-Iq-Tree was also used to analyse this concatenated data-
set using 1000 ultrafast bootstrap replicates to assess nodal
support (Minh et al 2013) The dataset was partitioned using
the scheme of the BI analysis but the Auto function was used
to explore the fit of substitution models based on the AICc
Divergence time estimation
We inferred divergence time estimates using beast 182
(Drummond et al 2012) To avoid poor Markov chain
Monte Carlo (MCMC) chain mixing and convergence issues
the MrBayes topology was manually fixed by editing thexml
file generated in Beauti 182 Preliminary beast runs with-
out a fixed input topology resulted in trees highly similar to
the MrBayes majority-rule consensus tree although some
parameters consistently had low ESS values (data not
shown) The three distant outgroups Epimetopus Berosus and
Amphiops were pruned to avoid generating artefactual ages
because of a lack of constraint and moderate phylogenetic
resolution The molecular clock hypothesis was tested in
mega 6 (Tamura et al 2013) Since it was significantly
rejected (P-value lt 001) we used a Bayesian relaxed clock
approach We partitioned the data by gene fragments to infer
substitution rates for each of these and to facilitate
convergence of the runs The substitution and clock models
were unlinked in Beauti 182 (Drummond et al 2012)
The best-fit substitution model for each gene fragment was
searched in PartitionFinder 111 (Lanfear et al 2012)
using the lsquobeastrsquo set of models the lsquogreedyrsquo algorithm and the
AICc to compare the fit of the different models An uncorre-
lated lognormal relaxed clock was assigned to each gene frag-
ment partition and the Tree Model was set to a Yule or a
birth-death process The runs consisted of 50 million genera-
tions sampled every 5000 generations Convergence of the
runs was investigated using ESS a burn-in of 10 applied
after checking the log-likelihood curves and the different
runs merged using LogCombiner 182 (Drummond et al
2012) Comparison of fit between the Yule and birth-death
models was assessed based on the marginal likelihoods esti-
mated (MLE) using stepping-stone sampling in beast 182
(Drummond et al 2012) The marginal likelihoods were
estimated using a chain of one million generations and 100
steps with a = 03 We used Bayes factors to select the best
tree model using the 2log(BF) = 2x(logMLE1logMLE2)
index assuming a value gt 10 as strong evidence for a model
over another (Kass amp Raftery 1995) The MCC tree median
ages and their 95 highest posterior density (HPD) were
generated afterwards under TreeAnnotator 182 (Drum-
mond et al 2012)
We used four fossils to calibrate the phylogeny (1) Hydro-
biomorpha eopalpalisdagger from the Messel pit in Germany dated
from the mid-Eocene (Mertz amp Renne 2005 Fikacek et al
2010) was used to constrain the age of the genus Hydro-
biomorpha with an exponential prior distribution (Beauti
settings mean = 3875 offset = 4602) 95 of the distribu-
tion was constrained to encompass an interval comprised
between 47 and 189 Ma The latter age was selected based on
the median age estimate calculated for the subfamily
Hydrophilinae (Bloom et al 2014) (2) Hydrochara spdaggerfrom the same geological formation (Fikacek et al 2010)
was used to constrain the age of the genus Hydrochara
(Beauti settings mean = 3875 offset = 4602) (3) Hydro-
bius titandagger described from the Florissant Formation in Color-
ado (USA 339ndash372 Ma) This fossil belongs to the extant
genus Sperchopsis (Bloom et al 2014) and was used to con-
strain the age of this genus (Beauti settings mean = 4234
offset = 3283) (4) Baissalarva hydrobioidesdagger from the Baissa
deposits in the Buryat Republic (Fikacek et al 2014) was
used to constrain the age of the extant tribe Hydrobiusini
(Beauti settings mean = 1475 offset = 13460) As a result
of uncertainty in the intra-generic placement of these fossils
we used calibrations on stems rather than crowns
Ancestral range estimation
We inferred the biogeographical history of Hydrophilini
scavenger beetles across their entire range of distribution
with lsquoBioGeoBEARSrsquo (Matzke 2013a) as implemented in R
330 (R Core Team 2016) This program allows estimating
historical biogeography patterns under different models
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
3
Biogeography of Hydrophilini giant water scavenger beetles
combining vicariance and dispersal and implements a
parameter describing founder-event jump dispersal (j) This
free parameter allows a cladogenetic event where one daugh-
ter lineage inherits the ancestral range while another colo-
nizes a different one via founder-event speciation (Matzke
2013a) This parameter that has been shown in some biogeo-
graphical settings (eg archipelagos) to result in higher like-
lihood compared to models ignoring this parameter (Matzke
2013b) We conducted the analyses under the Dispersal
Extinction Cladogenesis (DEC Ree et al 2005 Ree amp Smith
2008) and DEC+j models using the beast maximum clade
credibility (MCC) tree with outgroups pruned (only Hydro-
philini representatives were kept) The following regions were
used in the analyses A Africa U Australian region (Aus-
tralia and Melanesia) N Nearctic S South America O Ori-
ental P Palaearctic We coded India as part of the Oriental
region although it was not part of this region until c 55 Ma
The distribution of each taxon was recovered from the litera-
ture (Hansen 1999 Short amp Fikacek 2011) andor from our
field notes To account for the extremely dynamic palaeogeo-
graphical events that occurred during the past 130 million
years (Myr) (Seton et al 2012) we designed four time slices
with differential dispersal rate scalers (s) between areas The
scalers were used to downweight the baseline dispersal rate
(d) between areas with respect to geographical barriers and
distance (Ree amp Sanmartın 2009) We followed the ensuing
rules dispersal between adjacent areas (dadj) is not penalized
(dadj = 10d) dispersal between areas separated by a small
water barrier (dswb) is downweighted by a scaler value of
075 (dswb = 075d) dispersal between areas separated by
another area (dar) is downweighted by a scaler value of 050
(dar = 050d) and dispersal between areas separated by a
large water barrier (dlwb) is downweighted by a scaler value
of 025 (dlwb = 025d) The dispersal rate matrices for the
four time slices between all possible area combinations were
calculated following these rules and considering multiple bar-
riers and landmass discontinuities throughout the timeframe
of the grouprsquos evolution (Seton et al 2012) We selected the
shortest path between two areas to impose the dispersal rate
scalers [eg dispersal between Africa (A) and the Australian
region (U) in the first time slice (130ndash80 Ma) was scaled by
025 because at that time those two regions were separated
by Antarctica (s = 050) but also by a small water barrier
(s = 025)] In the case of areas separated by several barriers
andor landmass discontinuities we chose in a conservative
manner to use a minimum scaler of s = 005 to take into
consideration unlikely long-dispersal events Finally we
allowed different adjacency matrices in the four time slices
(Fig 1) The rationale was to allow different ancestral ranges
(0 or more areas) in each time slice to take into account the
palaeogeographical rearrangements of landmasses throughout
the Cenozoic As a result a unique continuous-time Markov
Chain (CTMC) was used for each time slice For each time
slice the downpass likelihood of non-existing ranges was set
to 0 and non-existing ranges were removed from the rate
matrix (Matzke pers comm)
RESULTS
Phylogenetic analyses
The partitioning scheme and substitution models selected in
PartitionFinder are given in Table 1 All partitions
included in the MrBayes analyses had a GTR+I+Γ model
The results of our phylogenetic analyses are summarized in
Fig 2 We recover Hydrophilini monophyletic with strong
support with Hydrobiusini as its sister taxon (PP = 099
BS = 89) The tribe is divided into two primary clades C2
(PP = 095BS = 89) and C3 (PP = 091BS = 77) respec-
tively comprising Hydrobiomorpha + Hydrophilus and
HydrocharaBrownephilus + (Sternolophus + Tropisternus)
Most hydrophiline genera including Hydrobiomorpha
(clade C4 PP = 1BS = 100) Hydrophilus (clade C5 PP = 1
BS = 100) Sternolophus (clade C7 PP = 1BS = 100) and
Tropisternus (clade C8 PP = 1BS = 100) are all resolved as
monophyletic with strong support The middle-eastern ende-
mic genus Brownephilus is found deeply nested within
Hydrochara which otherwise is strongly supported as mono-
phyletic (clade C6 PP = 1BS = 100)
Divergence time estimates and ancestral range
estimation
The partitioning scheme and substitution models selected in
PartitionFinder are given in Table 2 The beast analyses
converged as indicated by the stationarity of the MCMC and
ESS values above 200 Based on Bayes Factor comparisons
the birth-death model (Ln = 3059321) was preferred over
the Yule model (Ln = 3059321) though both models gave
very similar dating estimates (Table 3) The estimated rates
of gene fragments were also highly similar between the two
models (Table 4) The median ages across the phylogeny of
Hydrophilini based on the birth-death model are presented
in Fig 3 along with the 95 credibility intervals of the most
important nodes lsquoBioGeoBEARSrsquo favoured the DEC+j model
over the DEC model with a significant difference in log-like-
lihood (LnLDEC+j = 9719 against LnLDEC = 12233)
Results from both analyses (the ancestral ranges receiving the
highest relative probability) are mapped on the phylogeny in
Fig 3 (see Appendix S3 for more details on alternative
ranges and uncertainty in reconstructions)
Under the estimated DEC+j model (e = 00000 d = 00028
j = 00841) we infer an origin of the group in the joint area
Africa+South America (AS West Gondwana) about 120 Ma
during the Lower Cretaceous (Fig 3) We infer a subsequent
vicariant event leading to a clade in Africa comprising Hydro-
biomorpha and Hydrophilus and another in South America
comprising the rest of the tribe In Hydrobiomorpha Africa is
colonized via dispersal from South America in the Palaeocene
Eocene In Hydrophilus the Oriental region is colonized from
South America in the Upper Cretaceous The Australian
Nearctic and Palaearctic regions are colonized from South
America respectively between the Upper Cretaceous and
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
4
E F A Toussaint et al
mid-Eocene and in the Eocene We infer an EoceneMiocene
colonization of the Palaearctic region out of Africa in Hydro-
chara with subsequent colonization of the Nearctic region in
the Miocene We infer two Miocene dispersal events out of
Africa in Sternolophus toward the Australian and Oriental
regions In Tropisternus we infer a range expansion in the
Figure 1 Dispersal rate scaling matrices used in the lsquoBioGeoBEARSrsquo analyses Summary of the time slices used in the lsquoBioGeoBEARSrsquo
analyses and arranged from top to bottom in inversed chronological order Each time slice (TS1 to TS4) is presented with a mapderived from Seton et al (2012 copyright permission from Elsevier with order number 4007750560480) and a matrix of dispersal rate
scalers relative to potential geographical barriers and distance Several symbols are used to represent the possible barriers between thechosen areas A Africa U Australian region O Oriental region S South America N Nearctic P Palaearctic
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
5
Biogeography of Hydrophilini giant water scavenger beetles
Eocene toward the Nearctic region and a dispersal event out of
South America toward the Nearctic region in the Oligocene
The rest of present-day distribution of Hydrophilini is the
result of late dispersal events
Although most of the biogeographical pattern inferred is
robust with high ancestral range probabilities across the
chronogram some important nodes have equiprobable esti-
mated ancestral ranges (Fig 3) This is the case for instance
of the nodes corresponding to the root and clades C2 C4 C5
and C6 for which the second most likely ancestral range
received a relatively high likelihood (Fig 3 see Appendix S3)
Under the estimated DEC model (extinction rate = 001
dispersal rate = 001) the ancestral range with the highest
probability still supports a vicariant initial pattern in West
Gondwana although with lower probability Clade C2 is also
inferred as ancestrally Neotropical with subsequent range
expansion toward Africa in Clade C5 in the Upper Cretaceous
This scenario would imply local extinction in Africa followed
by recolonization of this region when both landmasses had
already been drifting apart for 20ndash30 Myr therefore invoking
long-distance dispersal The biogeographical scenario in Clade
C3 is different from the one inferred under the DEC+j model
Africa is the ancestral range but the daughter nodes present a
vicariant pattern respectively in Africa+Palaeacritc and Afri-
ca+South America In Clade C6 the ancestor would have
shifted its range toward the Nearctic region in the Oligocene
which is in line with palaeogeographic configuration at that
time The rest of the biogeographical history in C6 would
imply several vicariant events between Nearctic and Palaearctic
in the Oligocene and Miocene In clade C7 the most notable
change in comparison to the DEC+j model is the transition
from Africa to a wide range in Africa+Oriental region before a
dispersal event toward Australia in the Oligocene-Miocene In
clade C8 the DEC model recovers vicariant events instead of
dispersal events to explain the distribution of Nearctic Tropis-
ternus species
DISCUSSION
Systematics of Hydrophilini
Our recovered topology (Fig 2) largely agrees with prior
hypotheses of Hydrophilini relationships based on adult
morphology (Short 2010) with two notable exceptions the
monophyly of Hydrochara and the placement of the root
Short (2010) had resolved Hydrochara as a weakly supported
paraphyletic grade while we resolve the genus as mono-
phyletic with strong support and with the inclusion of Brow-
nephilus which contains two enigmatic species from the
Middle East This is not a surprising outcome as Hydrochara
has always been considered a natural group and shares
aedeagal morphology with Brownephilus Additional exami-
nation of the morphology of these two genera and a formal
synonymy of Brownephilus with Hydrochara is forthcoming
(A E Z Short unpublished data)
Though the unrooted networks are congruent the place-
ment of the root differs from Short (2010) After accounting
for the absence of Protistolophus in our analysis the compara-
ble root would insert between the Sternolophus and
the reminder of the Hydrophilini while we inferred it along
the branch between (Hydrobiomorpha+Hydrophilus) and
[Hydrochara+(Sternolophus+Tropisternus)] We believe our
inferred root placement is more congruent with the observed
morphological diversity and distributions of the genera Addi-
tionally even if the other root placement had been recovered
it would not alter a West Gondwana origin of the Hydrophilini
as Protistolophus is a Neotropical endemic and the ancestral
rage of Sternolophus is resolved as Afrotropical in our analysis
Biogeography of giant scavenger water beetles
Our results suggest with moderate support an ancestral origin
of the Hydrophilini in a vast region encompassing both Africa
and South America (ie West Gondwana) in the Lower Creta-
ceous about 120 Ma (Fig 3) At that time these regions were
largely connected and only began to drift apart in the mid-
Cretaceous from 120 to 100 Ma (Seton et al 2012) Follow-
ing this initial vicariance the biogeographical evolution of the
group was mainly driven by dispersal (but see the DEC model
in Fig 3) The dispersal events inferred in clades C4 and C5
respectively from South America toward Africa or Australasia
require a trans-oceanic dispersal explanation or continental
dispersal through Antarctica followed by extinction in the lat-
ter case Trans-oceanic dispersal events have been suggested
on other water beetle clades for instance in Platynectini div-
ing beetles (Coleoptera Dytiscidae) from the Oriental region
Table 1 Partitioning scheme and substitution models for the
W-Iq-Tree analyses
Partition name Composition W-IQ-TREE AICc model
P1 CO1 pos2 TIM2+I+GP2 CO1 pos1 TPM3+IP3 CO1 pos3 TIM2+I+GP4 ARK pos1 TPM3u+I+GP5 ARK pos2 K3P+I+GP6 ARK pos3 TPM2+I+GP7 18S TNe+I+GP8 28S GTR+I+G
Figure 2 Molecular phylogeny of the tribe Hydrophilini The topology derived from the MrBayes analysis is presented with nodal
support of the BI and ML analyses as indicated in the inserted caption The black vertical bar delimits outgroups used in this study andthe grey ones delimit the different genera of the tribe Hydrophilini Hydrochara and Brownephilus being found in a single clade the
paraphyly of the former is highlighted with a dashed vertical bar On the left part of the figure is presented a habitus of Hydrophilus
rufomarginatus from Africa
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
6
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
7
Biogeography of Hydrophilini giant water scavenger beetles
toward South America (Toussaint et al 2017) In clade C5
the dispersal from South America toward the Oriental region
(Fig 3) has to be explained by long-distance dispersal in the
Upper Cretaceous possibly toward India that at this time was
part of East Gondwana (Gibbons et al 2013) The lineages
would have persisted on the Indian plate until its docking
with Eurasia 30 Myr later (Seton et al 2012) Despite the
intense volcanism recorded during the drifting of India
examples of clades that survived such dramatic conditions
have been suggested (eg Toussaint et al 2016) The African
continent was later recolonized via range expansion in the
genus Hydrophilus (Fig 3) The colonization of the Palaearctic
region out of South America in C5 is puzzling and could
either result from a long-distance dispersal event or from dis-
persal via the Nearctic region followed by regional extinction
In clade C6 the Palaearctic region was colonized from Africa
when both landmasses were very close (Fig 1) The genus
Sternolophus also presents some intriguing biogeographical
patterns such as a dispersal event from Africa toward Aus-
tralasia in the OligoceneMiocene possibly using the Kergue-
len plateau as a stepping-stone as hypothesized in allodapine
bees (Hymenoptera Apidae) (Schwarz et al 2006)
Our results moderately support the West Gondwanan
vicariant scenario (relative probability P = 18) with two
slightly less likely origins Afrotropical (P = 15) or wide-
spread (Africa+South America+Oriental P = 15) Consid-
ering the incomplete sampling in Hydrophilus and the
equiprobable Afrotropical origin (P = 29 Fig 3) of the
clade supported as being Oriental (P = 30) in the DEC+janalyses we believe that the widespread origin scenario is
less plausible than the two other alternatives (West Gond-
wana and Africa) In the Afrotropical origin scenario the
tribe would have dispersed across the Atlantic Ocean toward
South America This scenario is less straightforward than the
West Gondwana vicariant one but does not seem completely
implausible considering that such dispersal occurred at least
another time with the ancestor of Tropisternus (Fig 3)
Though the DEC model received significantly less support
than the DEC+J model in lsquoBioGeoBEARSrsquo it is relevant to
Table 2 Partitioning scheme and substitution models for the
beast analyses
Partition name PF AICc model
ARK GTR+I+GCO1 GTR+I+G18S TrN+I+G28S GTR+I+G
PF PartitionFinder AICc Akaike information criterion corrected
Table 3 Median divergence time estimates of major nodes
within Hydrophilini as recovered in the beast analyses
Node
Yule model
(95 HPD)
Birth-death model
(95 HPD)
Root 13845 (13460ndash15083) 13846 (13460ndash15125)Hydrobiusini 8493 (6518ndash10765) 8552 (6508ndash10891)C1 (Hydrophilini) 12385 (10308ndash14349) 12253 (10067ndash14149)C2 11781 (9670ndash13649) 11630 (9600ndash13629)C3 11471 (9377ndash13529) 11396 (9183ndash13350)C4 (Hydrobiomorpha) 6598 (4721ndash8474) 6547 (4758ndash8526)C5 (Hydrophilus) 9512 (7676ndash11305) 9397 (7604ndash11247)C6 (Hydrochara) 4264 (2980ndash5793) 4256 (2973ndash5809)C7 (Sternolophus) 3770 (2712ndash5006) 3728 (2710ndash4989)C8 (Tropisternus) 5778 (4348ndash7329) 5717 (4348ndash7300)
Median ages in millions of years (Myr) HPD highest posterior
density
Table 4 Rates of the different gene fragments in Hydrophilini as estimated from the beast analyses using Bayesian lognormal relaxedclocks
Gene
Yule model Birth-death model
Mean rate ( SD) ucldmean ( SD) Mean rate ( SD) ucldmean ( SD)
CO1 001041 000136 001123 000172 001045 000134 001135 000174
ARK 000060 000007 000061 000008 000060 000007 000061 000008
18S 000006 000001 000007 000001 000006 000001 000007 000001
28S 000052 000006 000060 000011 000052 000006 000060 000010
Mean rate number of substitutions per site divided by the tree length ucldmean mean of branch rates SD standard deviation
Figure 3 Divergence times and palaeobiogeography of the tribe Hydrophilini Chronogram derived from the MCC tree beast analysis
presenting the median ages estimated as well as the 95 credibility intervals (horizontal grey bars) Range distribution of each species isgiven on the right of the chronogram following the colour-coded caption inserted at the bottom of the figure The most likely ancestral
range as estimated under the DEC+j model in lsquoBioGeoBEARSrsquo is presented at each node as a coloured square Nodes for which the
likelihood of the ancestral state is superior to 50 are highlighted with an asterisk For major nodes with lower probability the threemost likely states are presented in a box For more derived nodes with low probability only the second most likely state is given with a
letter corresponding to the inserted caption The results of the DEC model are also presented with coloured circles for each node wherethe ancestral estimated range differs from the one estimated under the DEC+j model For more details on the relative probabilities of
both models refer to Appendix S3 The timeframe of West Gondwana (Africa and South America) breakup is indicated by a large greyrectangle and a representation of the two landmasses c 100 Ma according to the model of Seton et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
8
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
9
Biogeography of Hydrophilini giant water scavenger beetles
compare results from the two methods here The founder-
event jump dispersal parameter j has been proven to be par-
ticularly relevant in island systems (Matzke 2014) where it
often significantly improves the likelihood of the model
However it is not entirely clear if or how this parameter is
relevant in continental island-like settings and more impor-
tantly in non-island-like continental settings In Hydrophi-
lini the j parameter is the main factor explaining the
biogeographical history of the group whereas the role of
extinction and range expansion is much reduced (see
Results) Considering the inferred negligible value of the
extinction parameter e in DEC+j it seems difficult to invoke
range expansion followed by extinction in hydrophilines In
contrast in the DEC model extinction and range expansion
play a crucial role as illustrated by the complex biogeo-
graphical scenario inferred (Fig 3 see Appendix S3) Indeed
most range expansion and vicariant events inferred by the
DEC model are difficult to reconciliate with the arrangement
of landmasses at the time without invoking regional
extinction
The fossil record indicates that at least some regional extinc-
tion has occurred in Hydrophilini (Fikacek et al 2010) Four
genera of Hydrophilini have Eocene representatives that have
been found in the Palaearctic region and two have Eocene rep-
resentatives from the Nearctic region Although our biogeo-
graphical reconstructions are consistent with such
distributions in Hydrochara (Palaearctic) Hydrophilus (Nearc-
tic and Palaearctic) and Tropisternus (Nearctic) the lack of
present-day Palaearctic Hydrobiomorpha suggests regional
extinction Thus although the DEC+j model receives a much
better likelihood than the DEC model it might not entirely
capture the complexity of the evolutionary history in this
group The DEC model on the other hand recovers extinction
and range expansion as important forces driving the biogeo-
graphical evolution of hydrophiline water beetles It also
implies biologically intricate biogeographical processes such as
repeated long-distance dispersal and regional extinction which
might be obscured by a potential role of Antarctica in shaping
the biogeography of the group Despite the stronger statistical
support for the DEC+j model over the DEC model it is not
clear which model is the most appropriate in the case of
Hydrophilini biogeographical history Unfortunately it is not
presently possible to place the described fossils in the present
phylogenetic framework because there is not enough morpho-
logical support for the inclusion of these taxa beyond generic
assignments Therefore it will be important to revise the
inferred patterns in the light of denser taxon sampling and bet-
ter knowledge of the fossil record as these can partly obscure
macroevolutionary patterns (eg Meseguer et al 2015 Tous-
saint amp Condamine 2016)
Comparison with other West Gondwana vicariance
patterns
Our ancestral range estimation recovers with moderate sup-
port a West Gondwana vicariant pattern with a joint ancestral
distribution in these two regions A recent study on Sericini
chafers (Coleoptera Scarabaeidae) recovered a similar pattern
with the best biogeographical model estimating a vicariant
split consistent with the West Gondwana vicariance hypothe-
sis (WGVH) (Eberle et al 2017 Fig 4) Likewise Luebert
et al (2017) recovered a potential case of vicariance support-
ing the WGVH in Boraginales (Asterids) with the upper
bound of their age estimate slightly overlapping with the tim-
ing of West Gondwana break-up (Fig 4) Flowering plants of
the families Combretaceae (Rosids Myrtales) and Elatinaceae
CentroplacaceaeMalpighiaceae (Rosids Malpighiales) have
also been recently suggested as a potential example of West
Gondwana vicariance (Berger et al 2016 Cai et al 2016)
Some clades with exclusive sister relationships between
Afrotropical and Neotropical lineages have been suggested as
good candidates for the WGVH For example the divergence
of the freshwater fish sister genera Arapaima and Heterosis
(Teleostei Osteoglossiformes) respectively found in South
America and Africa was dated from the Cretaceous (Fig 4)
Although the dating analyses were somewhat contradictory
these osteoglossiform fishes are amongst the best candidates
for the WGVH (Lavoue 2016) Aciliine diving beetles
(Coleoptera Dytiscidae) have also been suggested as a candi-
date for WGVH (Fig 4) although the results of dating anal-
yses were inconsistent when based on either crown or stem
fossil placement (Bukontaite et al 2014) A more compelling
example is found in the gecko family Sphaerodactylidae in
which Gamble et al (2008) recovered as split between Mor-
occo and Neotropical geckoes in the Upper Cretaceous con-
sistent with the WGVH In caecilians the family
Dermophiidae endemic to South America has been resolved
as sister to Siphonopidae distributed on each side of the
Atlantic Ocean with Neotropical siphonopids being the most
derived clade in the family The dating of the split between
the two families has been somewhat controversial with esti-
mates largely spanning the Lower Cretaceous (Kamei et al
2012) and younger ones postdating the West Gondwana
break-up (Pyron 2014)
In contrast other studies focusing on clades with a well-
supported sister-group relationship between Africa and South
America have rejected the WGVH For instance Givnish
et al (2004) suggested a very recent Miocene divergence
between the AfricanSouth American disjunct lineages in
Bromeliaceae and Rapateaceae suggesting long-distance dis-
persal Likewise the divergence between the African wild
almond genus Brabejum and its sister genus Panopsis from
South America was dated from the Eocene (Barker et al
2007) therefore rejecting the hypothesis of a West Gond-
wanan signature Other examples of molecular divergence
time estimates that are irreconcilable with the WGVH are
also found in cichlid fishes (Matschiner et al 2017 but see
Lopez-Fernandez et al 2013) amphisbaenian worm lizards
(Longrich et al 2015) Leguminosae (Meng et al 2014)
and Sapotaceae (Bartish et al 2011)
Although we relied on a rather limited fraction of the total
diversity of hydrophiline water beetles we included most of
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
10
E F A Toussaint et al
Figure 4 Examples of clades supporting the West Gondwana vicariance hypothesis Overview of clades for which the West Gondwanavicariance hypothesis (WGVH) was suggested based on molecular dating andor model-based biogeographical estimationreconstruction
The divergence times for the focal nodes representing the split between Africa and South America are given for each clade as credibilityintervals Names with an asterisk indicate that in the selected study an alternative analysis did not support the WGVH For more details
on these alternative analyses please refer to the original publications The timeframe of West Gondwana (Africa and South America)breakup is indicated by a large grey rectangle and a representation of the two landmasses c 100 Ma according to the model of Seton
et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
11
Biogeography of Hydrophilini giant water scavenger beetles
the taxonomic and geographical diversity for each genus
Given that the missing taxa can be morphologically assigned
to sampled clades and more specifically that missing
Neotropical taxa are morphologically supported as members
of sampled Neotropical clades the possibility that our bio-
geographical estimation is biased by incomplete taxon sam-
pling is very unlikely The lack of an exclusive sister
relationship and the moderate relative probability for a sce-
nario supporting the WGVH suggest that a conservative view
of hydrophiline biogeographical history is prudent Future
empirical studies with denser taxon sampling will help to
confirm or revise this evolutionary pattern This study adds
to the scarce literature supporting the WGVH and is thus
important to our understanding of the relationship between
Gondwanan tectonic events and biogeographical evolution of
clades in the Cretaceous There is no doubt that the increas-
ing number of empirical studies using molecular dating and
model-based approaches will shed new light on the heated
debate between ancient vicariance and dispersalism
ACKNOWLEDGEMENTS
We would like to acknowledge the editors Mike Dawson and
Isabel Sanmartın as well as three anonymous reviewers for
constructive comments on earlier drafts of this paper We
thank the many colleagues that contributed tissues for this
study Kelly Miller Ignacio Ribera Michael Balke Robert
Sites Yusuke Minoshima Johannes Bergsten and Michael
Caterino Martin Fikacek provided material as well as critical
analysis of the fossil calibrations This study was funded in
part by a University of Kansas General Research Fund grant
to AEZS
REFERENCES
Andujar C Faille A Perez-Gonzalez S Zaballos JP
Vogler AP amp Ribera I (2016) Gondwanian relicts and
oceanic dispersal in a cosmopolitan radiation of euedaphic
ground beetles Molecular Phylogenetics and Evolution 99
235ndash246Barker NP Weston PH Rutschmann F amp Sauquet H
(2007) Molecular dating of the lsquoGondwananrsquo plant family
Proteaceae is only partially congruent with the timing of
the break-up of Gondwana Journal of Biogeography 34
2012ndash2027Bartish IV Antonelli A Richardson JE amp Swenson U
(2011) Vicariance or long-distance dispersal historical bio-
geography of the pantropical subfamily Chrysophylloideae
(Sapotaceae) Journal of Biogeography 38 177ndash190Beaulieu JM Tank DC amp Donoghue MJ (2013) A
Southern Hemisphere origin for campanulid angiosperms
with traces of the break-up of Gondwana BMC Evolution-
ary Biology 13 1
Berger BA Kriebel R Spalink D amp Sytsma KJ (2016)
Divergence times historical biogeography and shifts in
speciation rates of Myrtales Molecular Phylogenetics and
Evolution 95 116ndash136Bloom DD Fikacek M amp Short AEZ (2014) Clade age
and diversification rate variation explain disparity in spe-
cies richness among water scavenger beetle (Hydrophili-
dae) lineages PLoS ONE 9 e98430
Bukontaite R Miller KB amp Bergsten J (2014) The utility
of CAD in recovering Gondwanan vicariance events and
the evolutionary history of Aciliini (Coleoptera Dytisci-
dae) BMC Evolutionary Biology 14 5
Cai L Xi Z Peterson K Rushworth C Beaulieu J amp
Davis CC (2016) Phylogeny of Elatinaceae and the tropi-
cal Gondwanan origin of the Centroplacaceae (Malpighi-
aceae Elatinaceae) clade PLoS ONE 11 e0161881
Drummond AJ Suchard MA Xie D amp Rambaut A
(2012) Bayesian phylogenetics with BEAUti and the
BEAST 17 Molecular Biology and Evolution 29 1969ndash1973
Eberle J Fabrizi S Lago P amp Ahrens D (2017) A histori-
cal biogeography of megadiverse Sericinimdashanother story
ldquoout of Africardquo Cladistics in press doi 101111cla12162
Edgar RC (2004) MUSCLE multiple sequence alignment
with high accuracy and high throughput Nucleic Acids
Research 32 1792ndash1797Fikacek M Wedmann S amp Schmied H (2010) Diversifica-
tion of the greater hydrophilines clade of giant water scav-
enger beetles dated back to the Middle
Eocene (Coleoptera Hydrophilidae Hydrophilina) Inver-
tebrate Systematics 24 9ndash22Fikacek M Prokin A Yan E Yue Y Wang B Ren D
amp Beattie R (2014) Modern hydrophilid clades present
and widespread in the Late Jurassic and Early Cretaceous
(Coleoptera Hydrophiloidea Hydrophilidae) Zoological
Journal of the Linnean Society 170 710ndash734Gamble T Bauer AM Greenbaum E amp Jackman TR
(2008) Evidence for Gondwanan vicariance in an ancient
clade of gecko lizards Journal of Biogeography 35 88ndash104Gibbons AD Whittaker JM amp Meurouller RD (2013) The
breakup of East Gondwana assimilating constraints from
Cretaceous ocean basins around India into a best-fit tec-
tonic model Journal of Geophysical Research Solid Earth
118 808ndash822Givnish TJ Millam KC Evans TM Hall JC Pires
JC Berry PE amp Sytsma KJ (2004) Ancient vicariance
or recent long-distance dispersal Inferences about phy-
logeny and South American-African disjunctions in Rap-
ateaceae and Bromeliaceae based on ndhF sequence data
International Journal of Plant Sciences 165 S35ndashS54Hansen M (1999) World catalogue of insects Volume 2
Hydrophiloidea (s str) (Coleoptera) Apollo Books Sten-
strup Denmark
Kamei RG San Mauro D Gower DJ Van Bocxlaer I
Sherratt E Thomas A Babu S Bossuyt F Wilkinson
M amp Biju SD (2012) Discovery of a new family of
amphibians from northeast India with ancient links to
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
12
E F A Toussaint et al
Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
vicariance and dispersal in governing biodiversity assembly
through space and time in the Southern Hemisphere
The tribe Hydrophilini includes some of the most com-
mon and recognizable members of the water beetle family
Hydrophilidae Commonly referred to as the giant water
scavenger beetles the lineage includes some of the largest
aquatic beetles in the world with some exceeding five cen-
timetres in length Members are easily distinguished by a
sharply delimited lsquosternal keelrsquo that is formed by the fusion
and elongation of the meso- and metaventrites The mono-
phyly of the tribe has been strongly supported by cladistic
analyses based both on morphological (Short 2010) and
molecular (Short amp Fikacek 2013) data Taxa within the
Hydrophilini occupy a relatively narrow range of aquatic
habitats preferring open standing waters or the sluggish
margins and side pools of streams and rivers There are cur-
rently seven genera recognized within the tribe all of which
are easily diagnosed by suites of distinct morphological
synapomorphies (Short 2010) However the interrelation-
ships among these genera remain poorly understood
Giant water scavenger beetles are found in all the worldrsquos
biogeographical regions except Antarctica However this
diversity is not evenly distributed the majority of the grouprsquos
200 species are found in tropical regions and South America
alone is home to more than half of the known species (Short
amp Fikacek 2011) The tribe is one of the most fossil-rich
among the Hydrophilidae and its crown age was recently
estimated to be older than 120 million years ago (Ma)
(Bloom et al 2014 Toussaint et al 2016) Consequently
the diversification and biogeographical dynamics of this
lineage have been unfolding since before the breakup of
Gondwana
Using DNA sequence data from four loci and a broad tax-
onomic and geographic sampling we present the most
detailed phylogenetic and biogeographical analyses of the
tribe Hydrophilini to date to (1) infer the evolutionary rela-
tionships within the lineage (2) refine the age of the tribe
and its major clades and (3) reconstruct the biogeographical
history of the tribe to investigate the biogeographical origins
of hydrophiline diversity We specifically aim at testing the
contribution of vicariance versus dispersal in shaping the
biogeography of Hydrophilini
MATERIALS AND METHODS
Taxon sampling
In total 69 species out of approximately 200 described
(Short amp Fikacek 2011 unpublished data) from six of the
seven currently recognized genera were included (the sev-
enth the monotypic Protistolophus is only known from the
holotype collected in Venezuela) (see Appendix S1 in Sup-
porting Information for more details) Within the six genera
taxa were broadly sampled both taxonomically including 10
of the 12 included subgenera and geographically sampling
species from each genus across all biogeographical regions in
which they occur except for Australian representatives of
Hydrobiomorpha Most missing species belong to the genera
Hydrobiomorpha and Tropisternus and within these missing
taxa a large fraction is concentrated in South America Nev-
ertheless we have a good representation of Neotropical taxa
for these genera in our taxonomic sampling and therefore
are unlikely to lack major lineages Additionally missing
Neotropical species are supported as falling within already-
sampled Neotropical clades in Hydrobiomorpha both Old
and New World clades have unique synapomorphies of the
parameres of the male genitalia and have previously been
resolved as reciprocally monophyletic clades (Short 2010)
In Hydrophilus the missing Neotropical species are primarily
members of the subgenus Dibolocelus a lineage endemic to
South America except for one Nearctic species that we have
already included The well-defined genus Tropisternus does
not occur in the Old World and so any missing Neotropical
taxa would group with existing New World lineages There-
fore based on morphological evidence (Short 2010) we are
confident that most of the taxonomic and geographic diver-
sity of the tribe is represented in our sampling therefore
limiting possible biases in biogeographical analyses We
selected several outgroups including multiple representatives
of the sister tribe Hydrobiusini two more distant outgroups
from the tribes Amphiopini and Berosini and a representa-
tive of the closely related family Epimetopidae The selection
of outgroups was based on the most recent phylogenetic
studies of the family Hydrophilidae (Short amp Fikacek 2013
Toussaint et al 2016)
Molecular methods
From the dataset of Short amp Fikacek (2013) we used the
sequences of Hydrochara obtusata Sternolophus marginicollis
Tropisternus affinis T collaris and T lateralis as well as our
selection of outgroups All other Hydrophilini species used
in this study (64 in total) were sequenced de novo from
freshly collected tissues (see Table S1 for more information)
Specimens were preserved in 96 ethanol and kept frozen at
20 degC or below In a few cases pinned museum specimens
were used Total genomic DNA was extracted from legs with
a DNeasy kit (Qiagen Alameda CA USA)
Four gene fragments were amplified a 1764-bp fragment
of 18S rDNA a 696-bp fragment of arginine kinase (ARK) a
1025-bp fragment of 28S rDNA and a 750-bp fragment of
cytochrome oxidase 1 (CO1) Primers polymerase chain
reaction ingredients and thermocycler conditions were iden-
tical to those described in Short amp Fikacek (2013)
Trace files were edited and assembled in Geneious R
805 (Biomatters httpwwwgeneiouscom) All gene frag-
ments were aligned and refined using Muscle (Edgar
2004) as implemented in Geneious with default settings
Final alignments were adjusted by eye The final concate-
nated alignment consisted of 4235 sites Newly generated
sequences are deposited in GenBank under accession num-
bers KY554217-KY554442
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
2
E F A Toussaint et al
Phylogenetic analyses
We inferred gene fragment tree topologies in a maximum
likelihood (ML) framework using Iq-Tree 15 (Nguyen
et al 2015) as implemented on the W-Iq-Tree web server
(httpiqtreecibivunivieacat Trifinopoulos et al 2016)
The different gene fragment alignments were left unparti-
tioned and the models of substitution were estimated using
the Auto function and selected using the Akaike information
criterion corrected (AICc) After confirming there was no
significant incongruence (Bootstrap value BS lt 70) among
gene fragment topologies (see Appendix S2) we combined
these into a concatenate matrix for analysis
We used Bayesian inference (BI) to reconstruct phyloge-
netic relationships in Hydrophilini using the concatenated
matrix The partitions and corresponding models of substitu-
tion were selected under PartitionFinder 111 (Lanfear
et al 2012) using the lsquogreedyrsquo algorithm the lsquomrbayesrsquo set of
models and the AICc Phylogenetic analyses were performed
using MrBayes 326 (Ronquist et al 2012) as implemented
on CIPRES (Miller et al 2010) Two simultaneous and inde-
pendent runs consisting of eight MCMC (one cold and seven
incrementally heated) running 30 million generations were
used with a tree sampling every 5000 generations to calcu-
late posterior probabilities (PP) We assessed convergence of
the runs by investigating the average standard deviation of
split frequencies and effective sample size (ESS) of all param-
eters in Tracer 15 (httpBEASTbioedacukTracer) A
value of ESS gt 200 was acknowledged as a good indicator of
convergence After discarding 25 of the trees as burn-in
the remaining trees in the posterior sample were pooled to
generate a 50 majority-rule consensus tree
W-Iq-Tree was also used to analyse this concatenated data-
set using 1000 ultrafast bootstrap replicates to assess nodal
support (Minh et al 2013) The dataset was partitioned using
the scheme of the BI analysis but the Auto function was used
to explore the fit of substitution models based on the AICc
Divergence time estimation
We inferred divergence time estimates using beast 182
(Drummond et al 2012) To avoid poor Markov chain
Monte Carlo (MCMC) chain mixing and convergence issues
the MrBayes topology was manually fixed by editing thexml
file generated in Beauti 182 Preliminary beast runs with-
out a fixed input topology resulted in trees highly similar to
the MrBayes majority-rule consensus tree although some
parameters consistently had low ESS values (data not
shown) The three distant outgroups Epimetopus Berosus and
Amphiops were pruned to avoid generating artefactual ages
because of a lack of constraint and moderate phylogenetic
resolution The molecular clock hypothesis was tested in
mega 6 (Tamura et al 2013) Since it was significantly
rejected (P-value lt 001) we used a Bayesian relaxed clock
approach We partitioned the data by gene fragments to infer
substitution rates for each of these and to facilitate
convergence of the runs The substitution and clock models
were unlinked in Beauti 182 (Drummond et al 2012)
The best-fit substitution model for each gene fragment was
searched in PartitionFinder 111 (Lanfear et al 2012)
using the lsquobeastrsquo set of models the lsquogreedyrsquo algorithm and the
AICc to compare the fit of the different models An uncorre-
lated lognormal relaxed clock was assigned to each gene frag-
ment partition and the Tree Model was set to a Yule or a
birth-death process The runs consisted of 50 million genera-
tions sampled every 5000 generations Convergence of the
runs was investigated using ESS a burn-in of 10 applied
after checking the log-likelihood curves and the different
runs merged using LogCombiner 182 (Drummond et al
2012) Comparison of fit between the Yule and birth-death
models was assessed based on the marginal likelihoods esti-
mated (MLE) using stepping-stone sampling in beast 182
(Drummond et al 2012) The marginal likelihoods were
estimated using a chain of one million generations and 100
steps with a = 03 We used Bayes factors to select the best
tree model using the 2log(BF) = 2x(logMLE1logMLE2)
index assuming a value gt 10 as strong evidence for a model
over another (Kass amp Raftery 1995) The MCC tree median
ages and their 95 highest posterior density (HPD) were
generated afterwards under TreeAnnotator 182 (Drum-
mond et al 2012)
We used four fossils to calibrate the phylogeny (1) Hydro-
biomorpha eopalpalisdagger from the Messel pit in Germany dated
from the mid-Eocene (Mertz amp Renne 2005 Fikacek et al
2010) was used to constrain the age of the genus Hydro-
biomorpha with an exponential prior distribution (Beauti
settings mean = 3875 offset = 4602) 95 of the distribu-
tion was constrained to encompass an interval comprised
between 47 and 189 Ma The latter age was selected based on
the median age estimate calculated for the subfamily
Hydrophilinae (Bloom et al 2014) (2) Hydrochara spdaggerfrom the same geological formation (Fikacek et al 2010)
was used to constrain the age of the genus Hydrochara
(Beauti settings mean = 3875 offset = 4602) (3) Hydro-
bius titandagger described from the Florissant Formation in Color-
ado (USA 339ndash372 Ma) This fossil belongs to the extant
genus Sperchopsis (Bloom et al 2014) and was used to con-
strain the age of this genus (Beauti settings mean = 4234
offset = 3283) (4) Baissalarva hydrobioidesdagger from the Baissa
deposits in the Buryat Republic (Fikacek et al 2014) was
used to constrain the age of the extant tribe Hydrobiusini
(Beauti settings mean = 1475 offset = 13460) As a result
of uncertainty in the intra-generic placement of these fossils
we used calibrations on stems rather than crowns
Ancestral range estimation
We inferred the biogeographical history of Hydrophilini
scavenger beetles across their entire range of distribution
with lsquoBioGeoBEARSrsquo (Matzke 2013a) as implemented in R
330 (R Core Team 2016) This program allows estimating
historical biogeography patterns under different models
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
3
Biogeography of Hydrophilini giant water scavenger beetles
combining vicariance and dispersal and implements a
parameter describing founder-event jump dispersal (j) This
free parameter allows a cladogenetic event where one daugh-
ter lineage inherits the ancestral range while another colo-
nizes a different one via founder-event speciation (Matzke
2013a) This parameter that has been shown in some biogeo-
graphical settings (eg archipelagos) to result in higher like-
lihood compared to models ignoring this parameter (Matzke
2013b) We conducted the analyses under the Dispersal
Extinction Cladogenesis (DEC Ree et al 2005 Ree amp Smith
2008) and DEC+j models using the beast maximum clade
credibility (MCC) tree with outgroups pruned (only Hydro-
philini representatives were kept) The following regions were
used in the analyses A Africa U Australian region (Aus-
tralia and Melanesia) N Nearctic S South America O Ori-
ental P Palaearctic We coded India as part of the Oriental
region although it was not part of this region until c 55 Ma
The distribution of each taxon was recovered from the litera-
ture (Hansen 1999 Short amp Fikacek 2011) andor from our
field notes To account for the extremely dynamic palaeogeo-
graphical events that occurred during the past 130 million
years (Myr) (Seton et al 2012) we designed four time slices
with differential dispersal rate scalers (s) between areas The
scalers were used to downweight the baseline dispersal rate
(d) between areas with respect to geographical barriers and
distance (Ree amp Sanmartın 2009) We followed the ensuing
rules dispersal between adjacent areas (dadj) is not penalized
(dadj = 10d) dispersal between areas separated by a small
water barrier (dswb) is downweighted by a scaler value of
075 (dswb = 075d) dispersal between areas separated by
another area (dar) is downweighted by a scaler value of 050
(dar = 050d) and dispersal between areas separated by a
large water barrier (dlwb) is downweighted by a scaler value
of 025 (dlwb = 025d) The dispersal rate matrices for the
four time slices between all possible area combinations were
calculated following these rules and considering multiple bar-
riers and landmass discontinuities throughout the timeframe
of the grouprsquos evolution (Seton et al 2012) We selected the
shortest path between two areas to impose the dispersal rate
scalers [eg dispersal between Africa (A) and the Australian
region (U) in the first time slice (130ndash80 Ma) was scaled by
025 because at that time those two regions were separated
by Antarctica (s = 050) but also by a small water barrier
(s = 025)] In the case of areas separated by several barriers
andor landmass discontinuities we chose in a conservative
manner to use a minimum scaler of s = 005 to take into
consideration unlikely long-dispersal events Finally we
allowed different adjacency matrices in the four time slices
(Fig 1) The rationale was to allow different ancestral ranges
(0 or more areas) in each time slice to take into account the
palaeogeographical rearrangements of landmasses throughout
the Cenozoic As a result a unique continuous-time Markov
Chain (CTMC) was used for each time slice For each time
slice the downpass likelihood of non-existing ranges was set
to 0 and non-existing ranges were removed from the rate
matrix (Matzke pers comm)
RESULTS
Phylogenetic analyses
The partitioning scheme and substitution models selected in
PartitionFinder are given in Table 1 All partitions
included in the MrBayes analyses had a GTR+I+Γ model
The results of our phylogenetic analyses are summarized in
Fig 2 We recover Hydrophilini monophyletic with strong
support with Hydrobiusini as its sister taxon (PP = 099
BS = 89) The tribe is divided into two primary clades C2
(PP = 095BS = 89) and C3 (PP = 091BS = 77) respec-
tively comprising Hydrobiomorpha + Hydrophilus and
HydrocharaBrownephilus + (Sternolophus + Tropisternus)
Most hydrophiline genera including Hydrobiomorpha
(clade C4 PP = 1BS = 100) Hydrophilus (clade C5 PP = 1
BS = 100) Sternolophus (clade C7 PP = 1BS = 100) and
Tropisternus (clade C8 PP = 1BS = 100) are all resolved as
monophyletic with strong support The middle-eastern ende-
mic genus Brownephilus is found deeply nested within
Hydrochara which otherwise is strongly supported as mono-
phyletic (clade C6 PP = 1BS = 100)
Divergence time estimates and ancestral range
estimation
The partitioning scheme and substitution models selected in
PartitionFinder are given in Table 2 The beast analyses
converged as indicated by the stationarity of the MCMC and
ESS values above 200 Based on Bayes Factor comparisons
the birth-death model (Ln = 3059321) was preferred over
the Yule model (Ln = 3059321) though both models gave
very similar dating estimates (Table 3) The estimated rates
of gene fragments were also highly similar between the two
models (Table 4) The median ages across the phylogeny of
Hydrophilini based on the birth-death model are presented
in Fig 3 along with the 95 credibility intervals of the most
important nodes lsquoBioGeoBEARSrsquo favoured the DEC+j model
over the DEC model with a significant difference in log-like-
lihood (LnLDEC+j = 9719 against LnLDEC = 12233)
Results from both analyses (the ancestral ranges receiving the
highest relative probability) are mapped on the phylogeny in
Fig 3 (see Appendix S3 for more details on alternative
ranges and uncertainty in reconstructions)
Under the estimated DEC+j model (e = 00000 d = 00028
j = 00841) we infer an origin of the group in the joint area
Africa+South America (AS West Gondwana) about 120 Ma
during the Lower Cretaceous (Fig 3) We infer a subsequent
vicariant event leading to a clade in Africa comprising Hydro-
biomorpha and Hydrophilus and another in South America
comprising the rest of the tribe In Hydrobiomorpha Africa is
colonized via dispersal from South America in the Palaeocene
Eocene In Hydrophilus the Oriental region is colonized from
South America in the Upper Cretaceous The Australian
Nearctic and Palaearctic regions are colonized from South
America respectively between the Upper Cretaceous and
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
4
E F A Toussaint et al
mid-Eocene and in the Eocene We infer an EoceneMiocene
colonization of the Palaearctic region out of Africa in Hydro-
chara with subsequent colonization of the Nearctic region in
the Miocene We infer two Miocene dispersal events out of
Africa in Sternolophus toward the Australian and Oriental
regions In Tropisternus we infer a range expansion in the
Figure 1 Dispersal rate scaling matrices used in the lsquoBioGeoBEARSrsquo analyses Summary of the time slices used in the lsquoBioGeoBEARSrsquo
analyses and arranged from top to bottom in inversed chronological order Each time slice (TS1 to TS4) is presented with a mapderived from Seton et al (2012 copyright permission from Elsevier with order number 4007750560480) and a matrix of dispersal rate
scalers relative to potential geographical barriers and distance Several symbols are used to represent the possible barriers between thechosen areas A Africa U Australian region O Oriental region S South America N Nearctic P Palaearctic
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
5
Biogeography of Hydrophilini giant water scavenger beetles
Eocene toward the Nearctic region and a dispersal event out of
South America toward the Nearctic region in the Oligocene
The rest of present-day distribution of Hydrophilini is the
result of late dispersal events
Although most of the biogeographical pattern inferred is
robust with high ancestral range probabilities across the
chronogram some important nodes have equiprobable esti-
mated ancestral ranges (Fig 3) This is the case for instance
of the nodes corresponding to the root and clades C2 C4 C5
and C6 for which the second most likely ancestral range
received a relatively high likelihood (Fig 3 see Appendix S3)
Under the estimated DEC model (extinction rate = 001
dispersal rate = 001) the ancestral range with the highest
probability still supports a vicariant initial pattern in West
Gondwana although with lower probability Clade C2 is also
inferred as ancestrally Neotropical with subsequent range
expansion toward Africa in Clade C5 in the Upper Cretaceous
This scenario would imply local extinction in Africa followed
by recolonization of this region when both landmasses had
already been drifting apart for 20ndash30 Myr therefore invoking
long-distance dispersal The biogeographical scenario in Clade
C3 is different from the one inferred under the DEC+j model
Africa is the ancestral range but the daughter nodes present a
vicariant pattern respectively in Africa+Palaeacritc and Afri-
ca+South America In Clade C6 the ancestor would have
shifted its range toward the Nearctic region in the Oligocene
which is in line with palaeogeographic configuration at that
time The rest of the biogeographical history in C6 would
imply several vicariant events between Nearctic and Palaearctic
in the Oligocene and Miocene In clade C7 the most notable
change in comparison to the DEC+j model is the transition
from Africa to a wide range in Africa+Oriental region before a
dispersal event toward Australia in the Oligocene-Miocene In
clade C8 the DEC model recovers vicariant events instead of
dispersal events to explain the distribution of Nearctic Tropis-
ternus species
DISCUSSION
Systematics of Hydrophilini
Our recovered topology (Fig 2) largely agrees with prior
hypotheses of Hydrophilini relationships based on adult
morphology (Short 2010) with two notable exceptions the
monophyly of Hydrochara and the placement of the root
Short (2010) had resolved Hydrochara as a weakly supported
paraphyletic grade while we resolve the genus as mono-
phyletic with strong support and with the inclusion of Brow-
nephilus which contains two enigmatic species from the
Middle East This is not a surprising outcome as Hydrochara
has always been considered a natural group and shares
aedeagal morphology with Brownephilus Additional exami-
nation of the morphology of these two genera and a formal
synonymy of Brownephilus with Hydrochara is forthcoming
(A E Z Short unpublished data)
Though the unrooted networks are congruent the place-
ment of the root differs from Short (2010) After accounting
for the absence of Protistolophus in our analysis the compara-
ble root would insert between the Sternolophus and
the reminder of the Hydrophilini while we inferred it along
the branch between (Hydrobiomorpha+Hydrophilus) and
[Hydrochara+(Sternolophus+Tropisternus)] We believe our
inferred root placement is more congruent with the observed
morphological diversity and distributions of the genera Addi-
tionally even if the other root placement had been recovered
it would not alter a West Gondwana origin of the Hydrophilini
as Protistolophus is a Neotropical endemic and the ancestral
rage of Sternolophus is resolved as Afrotropical in our analysis
Biogeography of giant scavenger water beetles
Our results suggest with moderate support an ancestral origin
of the Hydrophilini in a vast region encompassing both Africa
and South America (ie West Gondwana) in the Lower Creta-
ceous about 120 Ma (Fig 3) At that time these regions were
largely connected and only began to drift apart in the mid-
Cretaceous from 120 to 100 Ma (Seton et al 2012) Follow-
ing this initial vicariance the biogeographical evolution of the
group was mainly driven by dispersal (but see the DEC model
in Fig 3) The dispersal events inferred in clades C4 and C5
respectively from South America toward Africa or Australasia
require a trans-oceanic dispersal explanation or continental
dispersal through Antarctica followed by extinction in the lat-
ter case Trans-oceanic dispersal events have been suggested
on other water beetle clades for instance in Platynectini div-
ing beetles (Coleoptera Dytiscidae) from the Oriental region
Table 1 Partitioning scheme and substitution models for the
W-Iq-Tree analyses
Partition name Composition W-IQ-TREE AICc model
P1 CO1 pos2 TIM2+I+GP2 CO1 pos1 TPM3+IP3 CO1 pos3 TIM2+I+GP4 ARK pos1 TPM3u+I+GP5 ARK pos2 K3P+I+GP6 ARK pos3 TPM2+I+GP7 18S TNe+I+GP8 28S GTR+I+G
Figure 2 Molecular phylogeny of the tribe Hydrophilini The topology derived from the MrBayes analysis is presented with nodal
support of the BI and ML analyses as indicated in the inserted caption The black vertical bar delimits outgroups used in this study andthe grey ones delimit the different genera of the tribe Hydrophilini Hydrochara and Brownephilus being found in a single clade the
paraphyly of the former is highlighted with a dashed vertical bar On the left part of the figure is presented a habitus of Hydrophilus
rufomarginatus from Africa
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
6
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
7
Biogeography of Hydrophilini giant water scavenger beetles
toward South America (Toussaint et al 2017) In clade C5
the dispersal from South America toward the Oriental region
(Fig 3) has to be explained by long-distance dispersal in the
Upper Cretaceous possibly toward India that at this time was
part of East Gondwana (Gibbons et al 2013) The lineages
would have persisted on the Indian plate until its docking
with Eurasia 30 Myr later (Seton et al 2012) Despite the
intense volcanism recorded during the drifting of India
examples of clades that survived such dramatic conditions
have been suggested (eg Toussaint et al 2016) The African
continent was later recolonized via range expansion in the
genus Hydrophilus (Fig 3) The colonization of the Palaearctic
region out of South America in C5 is puzzling and could
either result from a long-distance dispersal event or from dis-
persal via the Nearctic region followed by regional extinction
In clade C6 the Palaearctic region was colonized from Africa
when both landmasses were very close (Fig 1) The genus
Sternolophus also presents some intriguing biogeographical
patterns such as a dispersal event from Africa toward Aus-
tralasia in the OligoceneMiocene possibly using the Kergue-
len plateau as a stepping-stone as hypothesized in allodapine
bees (Hymenoptera Apidae) (Schwarz et al 2006)
Our results moderately support the West Gondwanan
vicariant scenario (relative probability P = 18) with two
slightly less likely origins Afrotropical (P = 15) or wide-
spread (Africa+South America+Oriental P = 15) Consid-
ering the incomplete sampling in Hydrophilus and the
equiprobable Afrotropical origin (P = 29 Fig 3) of the
clade supported as being Oriental (P = 30) in the DEC+janalyses we believe that the widespread origin scenario is
less plausible than the two other alternatives (West Gond-
wana and Africa) In the Afrotropical origin scenario the
tribe would have dispersed across the Atlantic Ocean toward
South America This scenario is less straightforward than the
West Gondwana vicariant one but does not seem completely
implausible considering that such dispersal occurred at least
another time with the ancestor of Tropisternus (Fig 3)
Though the DEC model received significantly less support
than the DEC+J model in lsquoBioGeoBEARSrsquo it is relevant to
Table 2 Partitioning scheme and substitution models for the
beast analyses
Partition name PF AICc model
ARK GTR+I+GCO1 GTR+I+G18S TrN+I+G28S GTR+I+G
PF PartitionFinder AICc Akaike information criterion corrected
Table 3 Median divergence time estimates of major nodes
within Hydrophilini as recovered in the beast analyses
Node
Yule model
(95 HPD)
Birth-death model
(95 HPD)
Root 13845 (13460ndash15083) 13846 (13460ndash15125)Hydrobiusini 8493 (6518ndash10765) 8552 (6508ndash10891)C1 (Hydrophilini) 12385 (10308ndash14349) 12253 (10067ndash14149)C2 11781 (9670ndash13649) 11630 (9600ndash13629)C3 11471 (9377ndash13529) 11396 (9183ndash13350)C4 (Hydrobiomorpha) 6598 (4721ndash8474) 6547 (4758ndash8526)C5 (Hydrophilus) 9512 (7676ndash11305) 9397 (7604ndash11247)C6 (Hydrochara) 4264 (2980ndash5793) 4256 (2973ndash5809)C7 (Sternolophus) 3770 (2712ndash5006) 3728 (2710ndash4989)C8 (Tropisternus) 5778 (4348ndash7329) 5717 (4348ndash7300)
Median ages in millions of years (Myr) HPD highest posterior
density
Table 4 Rates of the different gene fragments in Hydrophilini as estimated from the beast analyses using Bayesian lognormal relaxedclocks
Gene
Yule model Birth-death model
Mean rate ( SD) ucldmean ( SD) Mean rate ( SD) ucldmean ( SD)
CO1 001041 000136 001123 000172 001045 000134 001135 000174
ARK 000060 000007 000061 000008 000060 000007 000061 000008
18S 000006 000001 000007 000001 000006 000001 000007 000001
28S 000052 000006 000060 000011 000052 000006 000060 000010
Mean rate number of substitutions per site divided by the tree length ucldmean mean of branch rates SD standard deviation
Figure 3 Divergence times and palaeobiogeography of the tribe Hydrophilini Chronogram derived from the MCC tree beast analysis
presenting the median ages estimated as well as the 95 credibility intervals (horizontal grey bars) Range distribution of each species isgiven on the right of the chronogram following the colour-coded caption inserted at the bottom of the figure The most likely ancestral
range as estimated under the DEC+j model in lsquoBioGeoBEARSrsquo is presented at each node as a coloured square Nodes for which the
likelihood of the ancestral state is superior to 50 are highlighted with an asterisk For major nodes with lower probability the threemost likely states are presented in a box For more derived nodes with low probability only the second most likely state is given with a
letter corresponding to the inserted caption The results of the DEC model are also presented with coloured circles for each node wherethe ancestral estimated range differs from the one estimated under the DEC+j model For more details on the relative probabilities of
both models refer to Appendix S3 The timeframe of West Gondwana (Africa and South America) breakup is indicated by a large greyrectangle and a representation of the two landmasses c 100 Ma according to the model of Seton et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
8
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
9
Biogeography of Hydrophilini giant water scavenger beetles
compare results from the two methods here The founder-
event jump dispersal parameter j has been proven to be par-
ticularly relevant in island systems (Matzke 2014) where it
often significantly improves the likelihood of the model
However it is not entirely clear if or how this parameter is
relevant in continental island-like settings and more impor-
tantly in non-island-like continental settings In Hydrophi-
lini the j parameter is the main factor explaining the
biogeographical history of the group whereas the role of
extinction and range expansion is much reduced (see
Results) Considering the inferred negligible value of the
extinction parameter e in DEC+j it seems difficult to invoke
range expansion followed by extinction in hydrophilines In
contrast in the DEC model extinction and range expansion
play a crucial role as illustrated by the complex biogeo-
graphical scenario inferred (Fig 3 see Appendix S3) Indeed
most range expansion and vicariant events inferred by the
DEC model are difficult to reconciliate with the arrangement
of landmasses at the time without invoking regional
extinction
The fossil record indicates that at least some regional extinc-
tion has occurred in Hydrophilini (Fikacek et al 2010) Four
genera of Hydrophilini have Eocene representatives that have
been found in the Palaearctic region and two have Eocene rep-
resentatives from the Nearctic region Although our biogeo-
graphical reconstructions are consistent with such
distributions in Hydrochara (Palaearctic) Hydrophilus (Nearc-
tic and Palaearctic) and Tropisternus (Nearctic) the lack of
present-day Palaearctic Hydrobiomorpha suggests regional
extinction Thus although the DEC+j model receives a much
better likelihood than the DEC model it might not entirely
capture the complexity of the evolutionary history in this
group The DEC model on the other hand recovers extinction
and range expansion as important forces driving the biogeo-
graphical evolution of hydrophiline water beetles It also
implies biologically intricate biogeographical processes such as
repeated long-distance dispersal and regional extinction which
might be obscured by a potential role of Antarctica in shaping
the biogeography of the group Despite the stronger statistical
support for the DEC+j model over the DEC model it is not
clear which model is the most appropriate in the case of
Hydrophilini biogeographical history Unfortunately it is not
presently possible to place the described fossils in the present
phylogenetic framework because there is not enough morpho-
logical support for the inclusion of these taxa beyond generic
assignments Therefore it will be important to revise the
inferred patterns in the light of denser taxon sampling and bet-
ter knowledge of the fossil record as these can partly obscure
macroevolutionary patterns (eg Meseguer et al 2015 Tous-
saint amp Condamine 2016)
Comparison with other West Gondwana vicariance
patterns
Our ancestral range estimation recovers with moderate sup-
port a West Gondwana vicariant pattern with a joint ancestral
distribution in these two regions A recent study on Sericini
chafers (Coleoptera Scarabaeidae) recovered a similar pattern
with the best biogeographical model estimating a vicariant
split consistent with the West Gondwana vicariance hypothe-
sis (WGVH) (Eberle et al 2017 Fig 4) Likewise Luebert
et al (2017) recovered a potential case of vicariance support-
ing the WGVH in Boraginales (Asterids) with the upper
bound of their age estimate slightly overlapping with the tim-
ing of West Gondwana break-up (Fig 4) Flowering plants of
the families Combretaceae (Rosids Myrtales) and Elatinaceae
CentroplacaceaeMalpighiaceae (Rosids Malpighiales) have
also been recently suggested as a potential example of West
Gondwana vicariance (Berger et al 2016 Cai et al 2016)
Some clades with exclusive sister relationships between
Afrotropical and Neotropical lineages have been suggested as
good candidates for the WGVH For example the divergence
of the freshwater fish sister genera Arapaima and Heterosis
(Teleostei Osteoglossiformes) respectively found in South
America and Africa was dated from the Cretaceous (Fig 4)
Although the dating analyses were somewhat contradictory
these osteoglossiform fishes are amongst the best candidates
for the WGVH (Lavoue 2016) Aciliine diving beetles
(Coleoptera Dytiscidae) have also been suggested as a candi-
date for WGVH (Fig 4) although the results of dating anal-
yses were inconsistent when based on either crown or stem
fossil placement (Bukontaite et al 2014) A more compelling
example is found in the gecko family Sphaerodactylidae in
which Gamble et al (2008) recovered as split between Mor-
occo and Neotropical geckoes in the Upper Cretaceous con-
sistent with the WGVH In caecilians the family
Dermophiidae endemic to South America has been resolved
as sister to Siphonopidae distributed on each side of the
Atlantic Ocean with Neotropical siphonopids being the most
derived clade in the family The dating of the split between
the two families has been somewhat controversial with esti-
mates largely spanning the Lower Cretaceous (Kamei et al
2012) and younger ones postdating the West Gondwana
break-up (Pyron 2014)
In contrast other studies focusing on clades with a well-
supported sister-group relationship between Africa and South
America have rejected the WGVH For instance Givnish
et al (2004) suggested a very recent Miocene divergence
between the AfricanSouth American disjunct lineages in
Bromeliaceae and Rapateaceae suggesting long-distance dis-
persal Likewise the divergence between the African wild
almond genus Brabejum and its sister genus Panopsis from
South America was dated from the Eocene (Barker et al
2007) therefore rejecting the hypothesis of a West Gond-
wanan signature Other examples of molecular divergence
time estimates that are irreconcilable with the WGVH are
also found in cichlid fishes (Matschiner et al 2017 but see
Lopez-Fernandez et al 2013) amphisbaenian worm lizards
(Longrich et al 2015) Leguminosae (Meng et al 2014)
and Sapotaceae (Bartish et al 2011)
Although we relied on a rather limited fraction of the total
diversity of hydrophiline water beetles we included most of
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
10
E F A Toussaint et al
Figure 4 Examples of clades supporting the West Gondwana vicariance hypothesis Overview of clades for which the West Gondwanavicariance hypothesis (WGVH) was suggested based on molecular dating andor model-based biogeographical estimationreconstruction
The divergence times for the focal nodes representing the split between Africa and South America are given for each clade as credibilityintervals Names with an asterisk indicate that in the selected study an alternative analysis did not support the WGVH For more details
on these alternative analyses please refer to the original publications The timeframe of West Gondwana (Africa and South America)breakup is indicated by a large grey rectangle and a representation of the two landmasses c 100 Ma according to the model of Seton
et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
11
Biogeography of Hydrophilini giant water scavenger beetles
the taxonomic and geographical diversity for each genus
Given that the missing taxa can be morphologically assigned
to sampled clades and more specifically that missing
Neotropical taxa are morphologically supported as members
of sampled Neotropical clades the possibility that our bio-
geographical estimation is biased by incomplete taxon sam-
pling is very unlikely The lack of an exclusive sister
relationship and the moderate relative probability for a sce-
nario supporting the WGVH suggest that a conservative view
of hydrophiline biogeographical history is prudent Future
empirical studies with denser taxon sampling will help to
confirm or revise this evolutionary pattern This study adds
to the scarce literature supporting the WGVH and is thus
important to our understanding of the relationship between
Gondwanan tectonic events and biogeographical evolution of
clades in the Cretaceous There is no doubt that the increas-
ing number of empirical studies using molecular dating and
model-based approaches will shed new light on the heated
debate between ancient vicariance and dispersalism
ACKNOWLEDGEMENTS
We would like to acknowledge the editors Mike Dawson and
Isabel Sanmartın as well as three anonymous reviewers for
constructive comments on earlier drafts of this paper We
thank the many colleagues that contributed tissues for this
study Kelly Miller Ignacio Ribera Michael Balke Robert
Sites Yusuke Minoshima Johannes Bergsten and Michael
Caterino Martin Fikacek provided material as well as critical
analysis of the fossil calibrations This study was funded in
part by a University of Kansas General Research Fund grant
to AEZS
REFERENCES
Andujar C Faille A Perez-Gonzalez S Zaballos JP
Vogler AP amp Ribera I (2016) Gondwanian relicts and
oceanic dispersal in a cosmopolitan radiation of euedaphic
ground beetles Molecular Phylogenetics and Evolution 99
235ndash246Barker NP Weston PH Rutschmann F amp Sauquet H
(2007) Molecular dating of the lsquoGondwananrsquo plant family
Proteaceae is only partially congruent with the timing of
the break-up of Gondwana Journal of Biogeography 34
2012ndash2027Bartish IV Antonelli A Richardson JE amp Swenson U
(2011) Vicariance or long-distance dispersal historical bio-
geography of the pantropical subfamily Chrysophylloideae
(Sapotaceae) Journal of Biogeography 38 177ndash190Beaulieu JM Tank DC amp Donoghue MJ (2013) A
Southern Hemisphere origin for campanulid angiosperms
with traces of the break-up of Gondwana BMC Evolution-
ary Biology 13 1
Berger BA Kriebel R Spalink D amp Sytsma KJ (2016)
Divergence times historical biogeography and shifts in
speciation rates of Myrtales Molecular Phylogenetics and
Evolution 95 116ndash136Bloom DD Fikacek M amp Short AEZ (2014) Clade age
and diversification rate variation explain disparity in spe-
cies richness among water scavenger beetle (Hydrophili-
dae) lineages PLoS ONE 9 e98430
Bukontaite R Miller KB amp Bergsten J (2014) The utility
of CAD in recovering Gondwanan vicariance events and
the evolutionary history of Aciliini (Coleoptera Dytisci-
dae) BMC Evolutionary Biology 14 5
Cai L Xi Z Peterson K Rushworth C Beaulieu J amp
Davis CC (2016) Phylogeny of Elatinaceae and the tropi-
cal Gondwanan origin of the Centroplacaceae (Malpighi-
aceae Elatinaceae) clade PLoS ONE 11 e0161881
Drummond AJ Suchard MA Xie D amp Rambaut A
(2012) Bayesian phylogenetics with BEAUti and the
BEAST 17 Molecular Biology and Evolution 29 1969ndash1973
Eberle J Fabrizi S Lago P amp Ahrens D (2017) A histori-
cal biogeography of megadiverse Sericinimdashanother story
ldquoout of Africardquo Cladistics in press doi 101111cla12162
Edgar RC (2004) MUSCLE multiple sequence alignment
with high accuracy and high throughput Nucleic Acids
Research 32 1792ndash1797Fikacek M Wedmann S amp Schmied H (2010) Diversifica-
tion of the greater hydrophilines clade of giant water scav-
enger beetles dated back to the Middle
Eocene (Coleoptera Hydrophilidae Hydrophilina) Inver-
tebrate Systematics 24 9ndash22Fikacek M Prokin A Yan E Yue Y Wang B Ren D
amp Beattie R (2014) Modern hydrophilid clades present
and widespread in the Late Jurassic and Early Cretaceous
(Coleoptera Hydrophiloidea Hydrophilidae) Zoological
Journal of the Linnean Society 170 710ndash734Gamble T Bauer AM Greenbaum E amp Jackman TR
(2008) Evidence for Gondwanan vicariance in an ancient
clade of gecko lizards Journal of Biogeography 35 88ndash104Gibbons AD Whittaker JM amp Meurouller RD (2013) The
breakup of East Gondwana assimilating constraints from
Cretaceous ocean basins around India into a best-fit tec-
tonic model Journal of Geophysical Research Solid Earth
118 808ndash822Givnish TJ Millam KC Evans TM Hall JC Pires
JC Berry PE amp Sytsma KJ (2004) Ancient vicariance
or recent long-distance dispersal Inferences about phy-
logeny and South American-African disjunctions in Rap-
ateaceae and Bromeliaceae based on ndhF sequence data
International Journal of Plant Sciences 165 S35ndashS54Hansen M (1999) World catalogue of insects Volume 2
Hydrophiloidea (s str) (Coleoptera) Apollo Books Sten-
strup Denmark
Kamei RG San Mauro D Gower DJ Van Bocxlaer I
Sherratt E Thomas A Babu S Bossuyt F Wilkinson
M amp Biju SD (2012) Discovery of a new family of
amphibians from northeast India with ancient links to
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
12
E F A Toussaint et al
Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
Phylogenetic analyses
We inferred gene fragment tree topologies in a maximum
likelihood (ML) framework using Iq-Tree 15 (Nguyen
et al 2015) as implemented on the W-Iq-Tree web server
(httpiqtreecibivunivieacat Trifinopoulos et al 2016)
The different gene fragment alignments were left unparti-
tioned and the models of substitution were estimated using
the Auto function and selected using the Akaike information
criterion corrected (AICc) After confirming there was no
significant incongruence (Bootstrap value BS lt 70) among
gene fragment topologies (see Appendix S2) we combined
these into a concatenate matrix for analysis
We used Bayesian inference (BI) to reconstruct phyloge-
netic relationships in Hydrophilini using the concatenated
matrix The partitions and corresponding models of substitu-
tion were selected under PartitionFinder 111 (Lanfear
et al 2012) using the lsquogreedyrsquo algorithm the lsquomrbayesrsquo set of
models and the AICc Phylogenetic analyses were performed
using MrBayes 326 (Ronquist et al 2012) as implemented
on CIPRES (Miller et al 2010) Two simultaneous and inde-
pendent runs consisting of eight MCMC (one cold and seven
incrementally heated) running 30 million generations were
used with a tree sampling every 5000 generations to calcu-
late posterior probabilities (PP) We assessed convergence of
the runs by investigating the average standard deviation of
split frequencies and effective sample size (ESS) of all param-
eters in Tracer 15 (httpBEASTbioedacukTracer) A
value of ESS gt 200 was acknowledged as a good indicator of
convergence After discarding 25 of the trees as burn-in
the remaining trees in the posterior sample were pooled to
generate a 50 majority-rule consensus tree
W-Iq-Tree was also used to analyse this concatenated data-
set using 1000 ultrafast bootstrap replicates to assess nodal
support (Minh et al 2013) The dataset was partitioned using
the scheme of the BI analysis but the Auto function was used
to explore the fit of substitution models based on the AICc
Divergence time estimation
We inferred divergence time estimates using beast 182
(Drummond et al 2012) To avoid poor Markov chain
Monte Carlo (MCMC) chain mixing and convergence issues
the MrBayes topology was manually fixed by editing thexml
file generated in Beauti 182 Preliminary beast runs with-
out a fixed input topology resulted in trees highly similar to
the MrBayes majority-rule consensus tree although some
parameters consistently had low ESS values (data not
shown) The three distant outgroups Epimetopus Berosus and
Amphiops were pruned to avoid generating artefactual ages
because of a lack of constraint and moderate phylogenetic
resolution The molecular clock hypothesis was tested in
mega 6 (Tamura et al 2013) Since it was significantly
rejected (P-value lt 001) we used a Bayesian relaxed clock
approach We partitioned the data by gene fragments to infer
substitution rates for each of these and to facilitate
convergence of the runs The substitution and clock models
were unlinked in Beauti 182 (Drummond et al 2012)
The best-fit substitution model for each gene fragment was
searched in PartitionFinder 111 (Lanfear et al 2012)
using the lsquobeastrsquo set of models the lsquogreedyrsquo algorithm and the
AICc to compare the fit of the different models An uncorre-
lated lognormal relaxed clock was assigned to each gene frag-
ment partition and the Tree Model was set to a Yule or a
birth-death process The runs consisted of 50 million genera-
tions sampled every 5000 generations Convergence of the
runs was investigated using ESS a burn-in of 10 applied
after checking the log-likelihood curves and the different
runs merged using LogCombiner 182 (Drummond et al
2012) Comparison of fit between the Yule and birth-death
models was assessed based on the marginal likelihoods esti-
mated (MLE) using stepping-stone sampling in beast 182
(Drummond et al 2012) The marginal likelihoods were
estimated using a chain of one million generations and 100
steps with a = 03 We used Bayes factors to select the best
tree model using the 2log(BF) = 2x(logMLE1logMLE2)
index assuming a value gt 10 as strong evidence for a model
over another (Kass amp Raftery 1995) The MCC tree median
ages and their 95 highest posterior density (HPD) were
generated afterwards under TreeAnnotator 182 (Drum-
mond et al 2012)
We used four fossils to calibrate the phylogeny (1) Hydro-
biomorpha eopalpalisdagger from the Messel pit in Germany dated
from the mid-Eocene (Mertz amp Renne 2005 Fikacek et al
2010) was used to constrain the age of the genus Hydro-
biomorpha with an exponential prior distribution (Beauti
settings mean = 3875 offset = 4602) 95 of the distribu-
tion was constrained to encompass an interval comprised
between 47 and 189 Ma The latter age was selected based on
the median age estimate calculated for the subfamily
Hydrophilinae (Bloom et al 2014) (2) Hydrochara spdaggerfrom the same geological formation (Fikacek et al 2010)
was used to constrain the age of the genus Hydrochara
(Beauti settings mean = 3875 offset = 4602) (3) Hydro-
bius titandagger described from the Florissant Formation in Color-
ado (USA 339ndash372 Ma) This fossil belongs to the extant
genus Sperchopsis (Bloom et al 2014) and was used to con-
strain the age of this genus (Beauti settings mean = 4234
offset = 3283) (4) Baissalarva hydrobioidesdagger from the Baissa
deposits in the Buryat Republic (Fikacek et al 2014) was
used to constrain the age of the extant tribe Hydrobiusini
(Beauti settings mean = 1475 offset = 13460) As a result
of uncertainty in the intra-generic placement of these fossils
we used calibrations on stems rather than crowns
Ancestral range estimation
We inferred the biogeographical history of Hydrophilini
scavenger beetles across their entire range of distribution
with lsquoBioGeoBEARSrsquo (Matzke 2013a) as implemented in R
330 (R Core Team 2016) This program allows estimating
historical biogeography patterns under different models
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
3
Biogeography of Hydrophilini giant water scavenger beetles
combining vicariance and dispersal and implements a
parameter describing founder-event jump dispersal (j) This
free parameter allows a cladogenetic event where one daugh-
ter lineage inherits the ancestral range while another colo-
nizes a different one via founder-event speciation (Matzke
2013a) This parameter that has been shown in some biogeo-
graphical settings (eg archipelagos) to result in higher like-
lihood compared to models ignoring this parameter (Matzke
2013b) We conducted the analyses under the Dispersal
Extinction Cladogenesis (DEC Ree et al 2005 Ree amp Smith
2008) and DEC+j models using the beast maximum clade
credibility (MCC) tree with outgroups pruned (only Hydro-
philini representatives were kept) The following regions were
used in the analyses A Africa U Australian region (Aus-
tralia and Melanesia) N Nearctic S South America O Ori-
ental P Palaearctic We coded India as part of the Oriental
region although it was not part of this region until c 55 Ma
The distribution of each taxon was recovered from the litera-
ture (Hansen 1999 Short amp Fikacek 2011) andor from our
field notes To account for the extremely dynamic palaeogeo-
graphical events that occurred during the past 130 million
years (Myr) (Seton et al 2012) we designed four time slices
with differential dispersal rate scalers (s) between areas The
scalers were used to downweight the baseline dispersal rate
(d) between areas with respect to geographical barriers and
distance (Ree amp Sanmartın 2009) We followed the ensuing
rules dispersal between adjacent areas (dadj) is not penalized
(dadj = 10d) dispersal between areas separated by a small
water barrier (dswb) is downweighted by a scaler value of
075 (dswb = 075d) dispersal between areas separated by
another area (dar) is downweighted by a scaler value of 050
(dar = 050d) and dispersal between areas separated by a
large water barrier (dlwb) is downweighted by a scaler value
of 025 (dlwb = 025d) The dispersal rate matrices for the
four time slices between all possible area combinations were
calculated following these rules and considering multiple bar-
riers and landmass discontinuities throughout the timeframe
of the grouprsquos evolution (Seton et al 2012) We selected the
shortest path between two areas to impose the dispersal rate
scalers [eg dispersal between Africa (A) and the Australian
region (U) in the first time slice (130ndash80 Ma) was scaled by
025 because at that time those two regions were separated
by Antarctica (s = 050) but also by a small water barrier
(s = 025)] In the case of areas separated by several barriers
andor landmass discontinuities we chose in a conservative
manner to use a minimum scaler of s = 005 to take into
consideration unlikely long-dispersal events Finally we
allowed different adjacency matrices in the four time slices
(Fig 1) The rationale was to allow different ancestral ranges
(0 or more areas) in each time slice to take into account the
palaeogeographical rearrangements of landmasses throughout
the Cenozoic As a result a unique continuous-time Markov
Chain (CTMC) was used for each time slice For each time
slice the downpass likelihood of non-existing ranges was set
to 0 and non-existing ranges were removed from the rate
matrix (Matzke pers comm)
RESULTS
Phylogenetic analyses
The partitioning scheme and substitution models selected in
PartitionFinder are given in Table 1 All partitions
included in the MrBayes analyses had a GTR+I+Γ model
The results of our phylogenetic analyses are summarized in
Fig 2 We recover Hydrophilini monophyletic with strong
support with Hydrobiusini as its sister taxon (PP = 099
BS = 89) The tribe is divided into two primary clades C2
(PP = 095BS = 89) and C3 (PP = 091BS = 77) respec-
tively comprising Hydrobiomorpha + Hydrophilus and
HydrocharaBrownephilus + (Sternolophus + Tropisternus)
Most hydrophiline genera including Hydrobiomorpha
(clade C4 PP = 1BS = 100) Hydrophilus (clade C5 PP = 1
BS = 100) Sternolophus (clade C7 PP = 1BS = 100) and
Tropisternus (clade C8 PP = 1BS = 100) are all resolved as
monophyletic with strong support The middle-eastern ende-
mic genus Brownephilus is found deeply nested within
Hydrochara which otherwise is strongly supported as mono-
phyletic (clade C6 PP = 1BS = 100)
Divergence time estimates and ancestral range
estimation
The partitioning scheme and substitution models selected in
PartitionFinder are given in Table 2 The beast analyses
converged as indicated by the stationarity of the MCMC and
ESS values above 200 Based on Bayes Factor comparisons
the birth-death model (Ln = 3059321) was preferred over
the Yule model (Ln = 3059321) though both models gave
very similar dating estimates (Table 3) The estimated rates
of gene fragments were also highly similar between the two
models (Table 4) The median ages across the phylogeny of
Hydrophilini based on the birth-death model are presented
in Fig 3 along with the 95 credibility intervals of the most
important nodes lsquoBioGeoBEARSrsquo favoured the DEC+j model
over the DEC model with a significant difference in log-like-
lihood (LnLDEC+j = 9719 against LnLDEC = 12233)
Results from both analyses (the ancestral ranges receiving the
highest relative probability) are mapped on the phylogeny in
Fig 3 (see Appendix S3 for more details on alternative
ranges and uncertainty in reconstructions)
Under the estimated DEC+j model (e = 00000 d = 00028
j = 00841) we infer an origin of the group in the joint area
Africa+South America (AS West Gondwana) about 120 Ma
during the Lower Cretaceous (Fig 3) We infer a subsequent
vicariant event leading to a clade in Africa comprising Hydro-
biomorpha and Hydrophilus and another in South America
comprising the rest of the tribe In Hydrobiomorpha Africa is
colonized via dispersal from South America in the Palaeocene
Eocene In Hydrophilus the Oriental region is colonized from
South America in the Upper Cretaceous The Australian
Nearctic and Palaearctic regions are colonized from South
America respectively between the Upper Cretaceous and
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
4
E F A Toussaint et al
mid-Eocene and in the Eocene We infer an EoceneMiocene
colonization of the Palaearctic region out of Africa in Hydro-
chara with subsequent colonization of the Nearctic region in
the Miocene We infer two Miocene dispersal events out of
Africa in Sternolophus toward the Australian and Oriental
regions In Tropisternus we infer a range expansion in the
Figure 1 Dispersal rate scaling matrices used in the lsquoBioGeoBEARSrsquo analyses Summary of the time slices used in the lsquoBioGeoBEARSrsquo
analyses and arranged from top to bottom in inversed chronological order Each time slice (TS1 to TS4) is presented with a mapderived from Seton et al (2012 copyright permission from Elsevier with order number 4007750560480) and a matrix of dispersal rate
scalers relative to potential geographical barriers and distance Several symbols are used to represent the possible barriers between thechosen areas A Africa U Australian region O Oriental region S South America N Nearctic P Palaearctic
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
5
Biogeography of Hydrophilini giant water scavenger beetles
Eocene toward the Nearctic region and a dispersal event out of
South America toward the Nearctic region in the Oligocene
The rest of present-day distribution of Hydrophilini is the
result of late dispersal events
Although most of the biogeographical pattern inferred is
robust with high ancestral range probabilities across the
chronogram some important nodes have equiprobable esti-
mated ancestral ranges (Fig 3) This is the case for instance
of the nodes corresponding to the root and clades C2 C4 C5
and C6 for which the second most likely ancestral range
received a relatively high likelihood (Fig 3 see Appendix S3)
Under the estimated DEC model (extinction rate = 001
dispersal rate = 001) the ancestral range with the highest
probability still supports a vicariant initial pattern in West
Gondwana although with lower probability Clade C2 is also
inferred as ancestrally Neotropical with subsequent range
expansion toward Africa in Clade C5 in the Upper Cretaceous
This scenario would imply local extinction in Africa followed
by recolonization of this region when both landmasses had
already been drifting apart for 20ndash30 Myr therefore invoking
long-distance dispersal The biogeographical scenario in Clade
C3 is different from the one inferred under the DEC+j model
Africa is the ancestral range but the daughter nodes present a
vicariant pattern respectively in Africa+Palaeacritc and Afri-
ca+South America In Clade C6 the ancestor would have
shifted its range toward the Nearctic region in the Oligocene
which is in line with palaeogeographic configuration at that
time The rest of the biogeographical history in C6 would
imply several vicariant events between Nearctic and Palaearctic
in the Oligocene and Miocene In clade C7 the most notable
change in comparison to the DEC+j model is the transition
from Africa to a wide range in Africa+Oriental region before a
dispersal event toward Australia in the Oligocene-Miocene In
clade C8 the DEC model recovers vicariant events instead of
dispersal events to explain the distribution of Nearctic Tropis-
ternus species
DISCUSSION
Systematics of Hydrophilini
Our recovered topology (Fig 2) largely agrees with prior
hypotheses of Hydrophilini relationships based on adult
morphology (Short 2010) with two notable exceptions the
monophyly of Hydrochara and the placement of the root
Short (2010) had resolved Hydrochara as a weakly supported
paraphyletic grade while we resolve the genus as mono-
phyletic with strong support and with the inclusion of Brow-
nephilus which contains two enigmatic species from the
Middle East This is not a surprising outcome as Hydrochara
has always been considered a natural group and shares
aedeagal morphology with Brownephilus Additional exami-
nation of the morphology of these two genera and a formal
synonymy of Brownephilus with Hydrochara is forthcoming
(A E Z Short unpublished data)
Though the unrooted networks are congruent the place-
ment of the root differs from Short (2010) After accounting
for the absence of Protistolophus in our analysis the compara-
ble root would insert between the Sternolophus and
the reminder of the Hydrophilini while we inferred it along
the branch between (Hydrobiomorpha+Hydrophilus) and
[Hydrochara+(Sternolophus+Tropisternus)] We believe our
inferred root placement is more congruent with the observed
morphological diversity and distributions of the genera Addi-
tionally even if the other root placement had been recovered
it would not alter a West Gondwana origin of the Hydrophilini
as Protistolophus is a Neotropical endemic and the ancestral
rage of Sternolophus is resolved as Afrotropical in our analysis
Biogeography of giant scavenger water beetles
Our results suggest with moderate support an ancestral origin
of the Hydrophilini in a vast region encompassing both Africa
and South America (ie West Gondwana) in the Lower Creta-
ceous about 120 Ma (Fig 3) At that time these regions were
largely connected and only began to drift apart in the mid-
Cretaceous from 120 to 100 Ma (Seton et al 2012) Follow-
ing this initial vicariance the biogeographical evolution of the
group was mainly driven by dispersal (but see the DEC model
in Fig 3) The dispersal events inferred in clades C4 and C5
respectively from South America toward Africa or Australasia
require a trans-oceanic dispersal explanation or continental
dispersal through Antarctica followed by extinction in the lat-
ter case Trans-oceanic dispersal events have been suggested
on other water beetle clades for instance in Platynectini div-
ing beetles (Coleoptera Dytiscidae) from the Oriental region
Table 1 Partitioning scheme and substitution models for the
W-Iq-Tree analyses
Partition name Composition W-IQ-TREE AICc model
P1 CO1 pos2 TIM2+I+GP2 CO1 pos1 TPM3+IP3 CO1 pos3 TIM2+I+GP4 ARK pos1 TPM3u+I+GP5 ARK pos2 K3P+I+GP6 ARK pos3 TPM2+I+GP7 18S TNe+I+GP8 28S GTR+I+G
Figure 2 Molecular phylogeny of the tribe Hydrophilini The topology derived from the MrBayes analysis is presented with nodal
support of the BI and ML analyses as indicated in the inserted caption The black vertical bar delimits outgroups used in this study andthe grey ones delimit the different genera of the tribe Hydrophilini Hydrochara and Brownephilus being found in a single clade the
paraphyly of the former is highlighted with a dashed vertical bar On the left part of the figure is presented a habitus of Hydrophilus
rufomarginatus from Africa
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
6
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
7
Biogeography of Hydrophilini giant water scavenger beetles
toward South America (Toussaint et al 2017) In clade C5
the dispersal from South America toward the Oriental region
(Fig 3) has to be explained by long-distance dispersal in the
Upper Cretaceous possibly toward India that at this time was
part of East Gondwana (Gibbons et al 2013) The lineages
would have persisted on the Indian plate until its docking
with Eurasia 30 Myr later (Seton et al 2012) Despite the
intense volcanism recorded during the drifting of India
examples of clades that survived such dramatic conditions
have been suggested (eg Toussaint et al 2016) The African
continent was later recolonized via range expansion in the
genus Hydrophilus (Fig 3) The colonization of the Palaearctic
region out of South America in C5 is puzzling and could
either result from a long-distance dispersal event or from dis-
persal via the Nearctic region followed by regional extinction
In clade C6 the Palaearctic region was colonized from Africa
when both landmasses were very close (Fig 1) The genus
Sternolophus also presents some intriguing biogeographical
patterns such as a dispersal event from Africa toward Aus-
tralasia in the OligoceneMiocene possibly using the Kergue-
len plateau as a stepping-stone as hypothesized in allodapine
bees (Hymenoptera Apidae) (Schwarz et al 2006)
Our results moderately support the West Gondwanan
vicariant scenario (relative probability P = 18) with two
slightly less likely origins Afrotropical (P = 15) or wide-
spread (Africa+South America+Oriental P = 15) Consid-
ering the incomplete sampling in Hydrophilus and the
equiprobable Afrotropical origin (P = 29 Fig 3) of the
clade supported as being Oriental (P = 30) in the DEC+janalyses we believe that the widespread origin scenario is
less plausible than the two other alternatives (West Gond-
wana and Africa) In the Afrotropical origin scenario the
tribe would have dispersed across the Atlantic Ocean toward
South America This scenario is less straightforward than the
West Gondwana vicariant one but does not seem completely
implausible considering that such dispersal occurred at least
another time with the ancestor of Tropisternus (Fig 3)
Though the DEC model received significantly less support
than the DEC+J model in lsquoBioGeoBEARSrsquo it is relevant to
Table 2 Partitioning scheme and substitution models for the
beast analyses
Partition name PF AICc model
ARK GTR+I+GCO1 GTR+I+G18S TrN+I+G28S GTR+I+G
PF PartitionFinder AICc Akaike information criterion corrected
Table 3 Median divergence time estimates of major nodes
within Hydrophilini as recovered in the beast analyses
Node
Yule model
(95 HPD)
Birth-death model
(95 HPD)
Root 13845 (13460ndash15083) 13846 (13460ndash15125)Hydrobiusini 8493 (6518ndash10765) 8552 (6508ndash10891)C1 (Hydrophilini) 12385 (10308ndash14349) 12253 (10067ndash14149)C2 11781 (9670ndash13649) 11630 (9600ndash13629)C3 11471 (9377ndash13529) 11396 (9183ndash13350)C4 (Hydrobiomorpha) 6598 (4721ndash8474) 6547 (4758ndash8526)C5 (Hydrophilus) 9512 (7676ndash11305) 9397 (7604ndash11247)C6 (Hydrochara) 4264 (2980ndash5793) 4256 (2973ndash5809)C7 (Sternolophus) 3770 (2712ndash5006) 3728 (2710ndash4989)C8 (Tropisternus) 5778 (4348ndash7329) 5717 (4348ndash7300)
Median ages in millions of years (Myr) HPD highest posterior
density
Table 4 Rates of the different gene fragments in Hydrophilini as estimated from the beast analyses using Bayesian lognormal relaxedclocks
Gene
Yule model Birth-death model
Mean rate ( SD) ucldmean ( SD) Mean rate ( SD) ucldmean ( SD)
CO1 001041 000136 001123 000172 001045 000134 001135 000174
ARK 000060 000007 000061 000008 000060 000007 000061 000008
18S 000006 000001 000007 000001 000006 000001 000007 000001
28S 000052 000006 000060 000011 000052 000006 000060 000010
Mean rate number of substitutions per site divided by the tree length ucldmean mean of branch rates SD standard deviation
Figure 3 Divergence times and palaeobiogeography of the tribe Hydrophilini Chronogram derived from the MCC tree beast analysis
presenting the median ages estimated as well as the 95 credibility intervals (horizontal grey bars) Range distribution of each species isgiven on the right of the chronogram following the colour-coded caption inserted at the bottom of the figure The most likely ancestral
range as estimated under the DEC+j model in lsquoBioGeoBEARSrsquo is presented at each node as a coloured square Nodes for which the
likelihood of the ancestral state is superior to 50 are highlighted with an asterisk For major nodes with lower probability the threemost likely states are presented in a box For more derived nodes with low probability only the second most likely state is given with a
letter corresponding to the inserted caption The results of the DEC model are also presented with coloured circles for each node wherethe ancestral estimated range differs from the one estimated under the DEC+j model For more details on the relative probabilities of
both models refer to Appendix S3 The timeframe of West Gondwana (Africa and South America) breakup is indicated by a large greyrectangle and a representation of the two landmasses c 100 Ma according to the model of Seton et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
8
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
9
Biogeography of Hydrophilini giant water scavenger beetles
compare results from the two methods here The founder-
event jump dispersal parameter j has been proven to be par-
ticularly relevant in island systems (Matzke 2014) where it
often significantly improves the likelihood of the model
However it is not entirely clear if or how this parameter is
relevant in continental island-like settings and more impor-
tantly in non-island-like continental settings In Hydrophi-
lini the j parameter is the main factor explaining the
biogeographical history of the group whereas the role of
extinction and range expansion is much reduced (see
Results) Considering the inferred negligible value of the
extinction parameter e in DEC+j it seems difficult to invoke
range expansion followed by extinction in hydrophilines In
contrast in the DEC model extinction and range expansion
play a crucial role as illustrated by the complex biogeo-
graphical scenario inferred (Fig 3 see Appendix S3) Indeed
most range expansion and vicariant events inferred by the
DEC model are difficult to reconciliate with the arrangement
of landmasses at the time without invoking regional
extinction
The fossil record indicates that at least some regional extinc-
tion has occurred in Hydrophilini (Fikacek et al 2010) Four
genera of Hydrophilini have Eocene representatives that have
been found in the Palaearctic region and two have Eocene rep-
resentatives from the Nearctic region Although our biogeo-
graphical reconstructions are consistent with such
distributions in Hydrochara (Palaearctic) Hydrophilus (Nearc-
tic and Palaearctic) and Tropisternus (Nearctic) the lack of
present-day Palaearctic Hydrobiomorpha suggests regional
extinction Thus although the DEC+j model receives a much
better likelihood than the DEC model it might not entirely
capture the complexity of the evolutionary history in this
group The DEC model on the other hand recovers extinction
and range expansion as important forces driving the biogeo-
graphical evolution of hydrophiline water beetles It also
implies biologically intricate biogeographical processes such as
repeated long-distance dispersal and regional extinction which
might be obscured by a potential role of Antarctica in shaping
the biogeography of the group Despite the stronger statistical
support for the DEC+j model over the DEC model it is not
clear which model is the most appropriate in the case of
Hydrophilini biogeographical history Unfortunately it is not
presently possible to place the described fossils in the present
phylogenetic framework because there is not enough morpho-
logical support for the inclusion of these taxa beyond generic
assignments Therefore it will be important to revise the
inferred patterns in the light of denser taxon sampling and bet-
ter knowledge of the fossil record as these can partly obscure
macroevolutionary patterns (eg Meseguer et al 2015 Tous-
saint amp Condamine 2016)
Comparison with other West Gondwana vicariance
patterns
Our ancestral range estimation recovers with moderate sup-
port a West Gondwana vicariant pattern with a joint ancestral
distribution in these two regions A recent study on Sericini
chafers (Coleoptera Scarabaeidae) recovered a similar pattern
with the best biogeographical model estimating a vicariant
split consistent with the West Gondwana vicariance hypothe-
sis (WGVH) (Eberle et al 2017 Fig 4) Likewise Luebert
et al (2017) recovered a potential case of vicariance support-
ing the WGVH in Boraginales (Asterids) with the upper
bound of their age estimate slightly overlapping with the tim-
ing of West Gondwana break-up (Fig 4) Flowering plants of
the families Combretaceae (Rosids Myrtales) and Elatinaceae
CentroplacaceaeMalpighiaceae (Rosids Malpighiales) have
also been recently suggested as a potential example of West
Gondwana vicariance (Berger et al 2016 Cai et al 2016)
Some clades with exclusive sister relationships between
Afrotropical and Neotropical lineages have been suggested as
good candidates for the WGVH For example the divergence
of the freshwater fish sister genera Arapaima and Heterosis
(Teleostei Osteoglossiformes) respectively found in South
America and Africa was dated from the Cretaceous (Fig 4)
Although the dating analyses were somewhat contradictory
these osteoglossiform fishes are amongst the best candidates
for the WGVH (Lavoue 2016) Aciliine diving beetles
(Coleoptera Dytiscidae) have also been suggested as a candi-
date for WGVH (Fig 4) although the results of dating anal-
yses were inconsistent when based on either crown or stem
fossil placement (Bukontaite et al 2014) A more compelling
example is found in the gecko family Sphaerodactylidae in
which Gamble et al (2008) recovered as split between Mor-
occo and Neotropical geckoes in the Upper Cretaceous con-
sistent with the WGVH In caecilians the family
Dermophiidae endemic to South America has been resolved
as sister to Siphonopidae distributed on each side of the
Atlantic Ocean with Neotropical siphonopids being the most
derived clade in the family The dating of the split between
the two families has been somewhat controversial with esti-
mates largely spanning the Lower Cretaceous (Kamei et al
2012) and younger ones postdating the West Gondwana
break-up (Pyron 2014)
In contrast other studies focusing on clades with a well-
supported sister-group relationship between Africa and South
America have rejected the WGVH For instance Givnish
et al (2004) suggested a very recent Miocene divergence
between the AfricanSouth American disjunct lineages in
Bromeliaceae and Rapateaceae suggesting long-distance dis-
persal Likewise the divergence between the African wild
almond genus Brabejum and its sister genus Panopsis from
South America was dated from the Eocene (Barker et al
2007) therefore rejecting the hypothesis of a West Gond-
wanan signature Other examples of molecular divergence
time estimates that are irreconcilable with the WGVH are
also found in cichlid fishes (Matschiner et al 2017 but see
Lopez-Fernandez et al 2013) amphisbaenian worm lizards
(Longrich et al 2015) Leguminosae (Meng et al 2014)
and Sapotaceae (Bartish et al 2011)
Although we relied on a rather limited fraction of the total
diversity of hydrophiline water beetles we included most of
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
10
E F A Toussaint et al
Figure 4 Examples of clades supporting the West Gondwana vicariance hypothesis Overview of clades for which the West Gondwanavicariance hypothesis (WGVH) was suggested based on molecular dating andor model-based biogeographical estimationreconstruction
The divergence times for the focal nodes representing the split between Africa and South America are given for each clade as credibilityintervals Names with an asterisk indicate that in the selected study an alternative analysis did not support the WGVH For more details
on these alternative analyses please refer to the original publications The timeframe of West Gondwana (Africa and South America)breakup is indicated by a large grey rectangle and a representation of the two landmasses c 100 Ma according to the model of Seton
et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
11
Biogeography of Hydrophilini giant water scavenger beetles
the taxonomic and geographical diversity for each genus
Given that the missing taxa can be morphologically assigned
to sampled clades and more specifically that missing
Neotropical taxa are morphologically supported as members
of sampled Neotropical clades the possibility that our bio-
geographical estimation is biased by incomplete taxon sam-
pling is very unlikely The lack of an exclusive sister
relationship and the moderate relative probability for a sce-
nario supporting the WGVH suggest that a conservative view
of hydrophiline biogeographical history is prudent Future
empirical studies with denser taxon sampling will help to
confirm or revise this evolutionary pattern This study adds
to the scarce literature supporting the WGVH and is thus
important to our understanding of the relationship between
Gondwanan tectonic events and biogeographical evolution of
clades in the Cretaceous There is no doubt that the increas-
ing number of empirical studies using molecular dating and
model-based approaches will shed new light on the heated
debate between ancient vicariance and dispersalism
ACKNOWLEDGEMENTS
We would like to acknowledge the editors Mike Dawson and
Isabel Sanmartın as well as three anonymous reviewers for
constructive comments on earlier drafts of this paper We
thank the many colleagues that contributed tissues for this
study Kelly Miller Ignacio Ribera Michael Balke Robert
Sites Yusuke Minoshima Johannes Bergsten and Michael
Caterino Martin Fikacek provided material as well as critical
analysis of the fossil calibrations This study was funded in
part by a University of Kansas General Research Fund grant
to AEZS
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235ndash246Barker NP Weston PH Rutschmann F amp Sauquet H
(2007) Molecular dating of the lsquoGondwananrsquo plant family
Proteaceae is only partially congruent with the timing of
the break-up of Gondwana Journal of Biogeography 34
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Southern Hemisphere origin for campanulid angiosperms
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Berger BA Kriebel R Spalink D amp Sytsma KJ (2016)
Divergence times historical biogeography and shifts in
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Evolution 95 116ndash136Bloom DD Fikacek M amp Short AEZ (2014) Clade age
and diversification rate variation explain disparity in spe-
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Bukontaite R Miller KB amp Bergsten J (2014) The utility
of CAD in recovering Gondwanan vicariance events and
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Cai L Xi Z Peterson K Rushworth C Beaulieu J amp
Davis CC (2016) Phylogeny of Elatinaceae and the tropi-
cal Gondwanan origin of the Centroplacaceae (Malpighi-
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Drummond AJ Suchard MA Xie D amp Rambaut A
(2012) Bayesian phylogenetics with BEAUti and the
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Eberle J Fabrizi S Lago P amp Ahrens D (2017) A histori-
cal biogeography of megadiverse Sericinimdashanother story
ldquoout of Africardquo Cladistics in press doi 101111cla12162
Edgar RC (2004) MUSCLE multiple sequence alignment
with high accuracy and high throughput Nucleic Acids
Research 32 1792ndash1797Fikacek M Wedmann S amp Schmied H (2010) Diversifica-
tion of the greater hydrophilines clade of giant water scav-
enger beetles dated back to the Middle
Eocene (Coleoptera Hydrophilidae Hydrophilina) Inver-
tebrate Systematics 24 9ndash22Fikacek M Prokin A Yan E Yue Y Wang B Ren D
amp Beattie R (2014) Modern hydrophilid clades present
and widespread in the Late Jurassic and Early Cretaceous
(Coleoptera Hydrophiloidea Hydrophilidae) Zoological
Journal of the Linnean Society 170 710ndash734Gamble T Bauer AM Greenbaum E amp Jackman TR
(2008) Evidence for Gondwanan vicariance in an ancient
clade of gecko lizards Journal of Biogeography 35 88ndash104Gibbons AD Whittaker JM amp Meurouller RD (2013) The
breakup of East Gondwana assimilating constraints from
Cretaceous ocean basins around India into a best-fit tec-
tonic model Journal of Geophysical Research Solid Earth
118 808ndash822Givnish TJ Millam KC Evans TM Hall JC Pires
JC Berry PE amp Sytsma KJ (2004) Ancient vicariance
or recent long-distance dispersal Inferences about phy-
logeny and South American-African disjunctions in Rap-
ateaceae and Bromeliaceae based on ndhF sequence data
International Journal of Plant Sciences 165 S35ndashS54Hansen M (1999) World catalogue of insects Volume 2
Hydrophiloidea (s str) (Coleoptera) Apollo Books Sten-
strup Denmark
Kamei RG San Mauro D Gower DJ Van Bocxlaer I
Sherratt E Thomas A Babu S Bossuyt F Wilkinson
M amp Biju SD (2012) Discovery of a new family of
amphibians from northeast India with ancient links to
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Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
combining vicariance and dispersal and implements a
parameter describing founder-event jump dispersal (j) This
free parameter allows a cladogenetic event where one daugh-
ter lineage inherits the ancestral range while another colo-
nizes a different one via founder-event speciation (Matzke
2013a) This parameter that has been shown in some biogeo-
graphical settings (eg archipelagos) to result in higher like-
lihood compared to models ignoring this parameter (Matzke
2013b) We conducted the analyses under the Dispersal
Extinction Cladogenesis (DEC Ree et al 2005 Ree amp Smith
2008) and DEC+j models using the beast maximum clade
credibility (MCC) tree with outgroups pruned (only Hydro-
philini representatives were kept) The following regions were
used in the analyses A Africa U Australian region (Aus-
tralia and Melanesia) N Nearctic S South America O Ori-
ental P Palaearctic We coded India as part of the Oriental
region although it was not part of this region until c 55 Ma
The distribution of each taxon was recovered from the litera-
ture (Hansen 1999 Short amp Fikacek 2011) andor from our
field notes To account for the extremely dynamic palaeogeo-
graphical events that occurred during the past 130 million
years (Myr) (Seton et al 2012) we designed four time slices
with differential dispersal rate scalers (s) between areas The
scalers were used to downweight the baseline dispersal rate
(d) between areas with respect to geographical barriers and
distance (Ree amp Sanmartın 2009) We followed the ensuing
rules dispersal between adjacent areas (dadj) is not penalized
(dadj = 10d) dispersal between areas separated by a small
water barrier (dswb) is downweighted by a scaler value of
075 (dswb = 075d) dispersal between areas separated by
another area (dar) is downweighted by a scaler value of 050
(dar = 050d) and dispersal between areas separated by a
large water barrier (dlwb) is downweighted by a scaler value
of 025 (dlwb = 025d) The dispersal rate matrices for the
four time slices between all possible area combinations were
calculated following these rules and considering multiple bar-
riers and landmass discontinuities throughout the timeframe
of the grouprsquos evolution (Seton et al 2012) We selected the
shortest path between two areas to impose the dispersal rate
scalers [eg dispersal between Africa (A) and the Australian
region (U) in the first time slice (130ndash80 Ma) was scaled by
025 because at that time those two regions were separated
by Antarctica (s = 050) but also by a small water barrier
(s = 025)] In the case of areas separated by several barriers
andor landmass discontinuities we chose in a conservative
manner to use a minimum scaler of s = 005 to take into
consideration unlikely long-dispersal events Finally we
allowed different adjacency matrices in the four time slices
(Fig 1) The rationale was to allow different ancestral ranges
(0 or more areas) in each time slice to take into account the
palaeogeographical rearrangements of landmasses throughout
the Cenozoic As a result a unique continuous-time Markov
Chain (CTMC) was used for each time slice For each time
slice the downpass likelihood of non-existing ranges was set
to 0 and non-existing ranges were removed from the rate
matrix (Matzke pers comm)
RESULTS
Phylogenetic analyses
The partitioning scheme and substitution models selected in
PartitionFinder are given in Table 1 All partitions
included in the MrBayes analyses had a GTR+I+Γ model
The results of our phylogenetic analyses are summarized in
Fig 2 We recover Hydrophilini monophyletic with strong
support with Hydrobiusini as its sister taxon (PP = 099
BS = 89) The tribe is divided into two primary clades C2
(PP = 095BS = 89) and C3 (PP = 091BS = 77) respec-
tively comprising Hydrobiomorpha + Hydrophilus and
HydrocharaBrownephilus + (Sternolophus + Tropisternus)
Most hydrophiline genera including Hydrobiomorpha
(clade C4 PP = 1BS = 100) Hydrophilus (clade C5 PP = 1
BS = 100) Sternolophus (clade C7 PP = 1BS = 100) and
Tropisternus (clade C8 PP = 1BS = 100) are all resolved as
monophyletic with strong support The middle-eastern ende-
mic genus Brownephilus is found deeply nested within
Hydrochara which otherwise is strongly supported as mono-
phyletic (clade C6 PP = 1BS = 100)
Divergence time estimates and ancestral range
estimation
The partitioning scheme and substitution models selected in
PartitionFinder are given in Table 2 The beast analyses
converged as indicated by the stationarity of the MCMC and
ESS values above 200 Based on Bayes Factor comparisons
the birth-death model (Ln = 3059321) was preferred over
the Yule model (Ln = 3059321) though both models gave
very similar dating estimates (Table 3) The estimated rates
of gene fragments were also highly similar between the two
models (Table 4) The median ages across the phylogeny of
Hydrophilini based on the birth-death model are presented
in Fig 3 along with the 95 credibility intervals of the most
important nodes lsquoBioGeoBEARSrsquo favoured the DEC+j model
over the DEC model with a significant difference in log-like-
lihood (LnLDEC+j = 9719 against LnLDEC = 12233)
Results from both analyses (the ancestral ranges receiving the
highest relative probability) are mapped on the phylogeny in
Fig 3 (see Appendix S3 for more details on alternative
ranges and uncertainty in reconstructions)
Under the estimated DEC+j model (e = 00000 d = 00028
j = 00841) we infer an origin of the group in the joint area
Africa+South America (AS West Gondwana) about 120 Ma
during the Lower Cretaceous (Fig 3) We infer a subsequent
vicariant event leading to a clade in Africa comprising Hydro-
biomorpha and Hydrophilus and another in South America
comprising the rest of the tribe In Hydrobiomorpha Africa is
colonized via dispersal from South America in the Palaeocene
Eocene In Hydrophilus the Oriental region is colonized from
South America in the Upper Cretaceous The Australian
Nearctic and Palaearctic regions are colonized from South
America respectively between the Upper Cretaceous and
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
4
E F A Toussaint et al
mid-Eocene and in the Eocene We infer an EoceneMiocene
colonization of the Palaearctic region out of Africa in Hydro-
chara with subsequent colonization of the Nearctic region in
the Miocene We infer two Miocene dispersal events out of
Africa in Sternolophus toward the Australian and Oriental
regions In Tropisternus we infer a range expansion in the
Figure 1 Dispersal rate scaling matrices used in the lsquoBioGeoBEARSrsquo analyses Summary of the time slices used in the lsquoBioGeoBEARSrsquo
analyses and arranged from top to bottom in inversed chronological order Each time slice (TS1 to TS4) is presented with a mapderived from Seton et al (2012 copyright permission from Elsevier with order number 4007750560480) and a matrix of dispersal rate
scalers relative to potential geographical barriers and distance Several symbols are used to represent the possible barriers between thechosen areas A Africa U Australian region O Oriental region S South America N Nearctic P Palaearctic
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
5
Biogeography of Hydrophilini giant water scavenger beetles
Eocene toward the Nearctic region and a dispersal event out of
South America toward the Nearctic region in the Oligocene
The rest of present-day distribution of Hydrophilini is the
result of late dispersal events
Although most of the biogeographical pattern inferred is
robust with high ancestral range probabilities across the
chronogram some important nodes have equiprobable esti-
mated ancestral ranges (Fig 3) This is the case for instance
of the nodes corresponding to the root and clades C2 C4 C5
and C6 for which the second most likely ancestral range
received a relatively high likelihood (Fig 3 see Appendix S3)
Under the estimated DEC model (extinction rate = 001
dispersal rate = 001) the ancestral range with the highest
probability still supports a vicariant initial pattern in West
Gondwana although with lower probability Clade C2 is also
inferred as ancestrally Neotropical with subsequent range
expansion toward Africa in Clade C5 in the Upper Cretaceous
This scenario would imply local extinction in Africa followed
by recolonization of this region when both landmasses had
already been drifting apart for 20ndash30 Myr therefore invoking
long-distance dispersal The biogeographical scenario in Clade
C3 is different from the one inferred under the DEC+j model
Africa is the ancestral range but the daughter nodes present a
vicariant pattern respectively in Africa+Palaeacritc and Afri-
ca+South America In Clade C6 the ancestor would have
shifted its range toward the Nearctic region in the Oligocene
which is in line with palaeogeographic configuration at that
time The rest of the biogeographical history in C6 would
imply several vicariant events between Nearctic and Palaearctic
in the Oligocene and Miocene In clade C7 the most notable
change in comparison to the DEC+j model is the transition
from Africa to a wide range in Africa+Oriental region before a
dispersal event toward Australia in the Oligocene-Miocene In
clade C8 the DEC model recovers vicariant events instead of
dispersal events to explain the distribution of Nearctic Tropis-
ternus species
DISCUSSION
Systematics of Hydrophilini
Our recovered topology (Fig 2) largely agrees with prior
hypotheses of Hydrophilini relationships based on adult
morphology (Short 2010) with two notable exceptions the
monophyly of Hydrochara and the placement of the root
Short (2010) had resolved Hydrochara as a weakly supported
paraphyletic grade while we resolve the genus as mono-
phyletic with strong support and with the inclusion of Brow-
nephilus which contains two enigmatic species from the
Middle East This is not a surprising outcome as Hydrochara
has always been considered a natural group and shares
aedeagal morphology with Brownephilus Additional exami-
nation of the morphology of these two genera and a formal
synonymy of Brownephilus with Hydrochara is forthcoming
(A E Z Short unpublished data)
Though the unrooted networks are congruent the place-
ment of the root differs from Short (2010) After accounting
for the absence of Protistolophus in our analysis the compara-
ble root would insert between the Sternolophus and
the reminder of the Hydrophilini while we inferred it along
the branch between (Hydrobiomorpha+Hydrophilus) and
[Hydrochara+(Sternolophus+Tropisternus)] We believe our
inferred root placement is more congruent with the observed
morphological diversity and distributions of the genera Addi-
tionally even if the other root placement had been recovered
it would not alter a West Gondwana origin of the Hydrophilini
as Protistolophus is a Neotropical endemic and the ancestral
rage of Sternolophus is resolved as Afrotropical in our analysis
Biogeography of giant scavenger water beetles
Our results suggest with moderate support an ancestral origin
of the Hydrophilini in a vast region encompassing both Africa
and South America (ie West Gondwana) in the Lower Creta-
ceous about 120 Ma (Fig 3) At that time these regions were
largely connected and only began to drift apart in the mid-
Cretaceous from 120 to 100 Ma (Seton et al 2012) Follow-
ing this initial vicariance the biogeographical evolution of the
group was mainly driven by dispersal (but see the DEC model
in Fig 3) The dispersal events inferred in clades C4 and C5
respectively from South America toward Africa or Australasia
require a trans-oceanic dispersal explanation or continental
dispersal through Antarctica followed by extinction in the lat-
ter case Trans-oceanic dispersal events have been suggested
on other water beetle clades for instance in Platynectini div-
ing beetles (Coleoptera Dytiscidae) from the Oriental region
Table 1 Partitioning scheme and substitution models for the
W-Iq-Tree analyses
Partition name Composition W-IQ-TREE AICc model
P1 CO1 pos2 TIM2+I+GP2 CO1 pos1 TPM3+IP3 CO1 pos3 TIM2+I+GP4 ARK pos1 TPM3u+I+GP5 ARK pos2 K3P+I+GP6 ARK pos3 TPM2+I+GP7 18S TNe+I+GP8 28S GTR+I+G
Figure 2 Molecular phylogeny of the tribe Hydrophilini The topology derived from the MrBayes analysis is presented with nodal
support of the BI and ML analyses as indicated in the inserted caption The black vertical bar delimits outgroups used in this study andthe grey ones delimit the different genera of the tribe Hydrophilini Hydrochara and Brownephilus being found in a single clade the
paraphyly of the former is highlighted with a dashed vertical bar On the left part of the figure is presented a habitus of Hydrophilus
rufomarginatus from Africa
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
6
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
7
Biogeography of Hydrophilini giant water scavenger beetles
toward South America (Toussaint et al 2017) In clade C5
the dispersal from South America toward the Oriental region
(Fig 3) has to be explained by long-distance dispersal in the
Upper Cretaceous possibly toward India that at this time was
part of East Gondwana (Gibbons et al 2013) The lineages
would have persisted on the Indian plate until its docking
with Eurasia 30 Myr later (Seton et al 2012) Despite the
intense volcanism recorded during the drifting of India
examples of clades that survived such dramatic conditions
have been suggested (eg Toussaint et al 2016) The African
continent was later recolonized via range expansion in the
genus Hydrophilus (Fig 3) The colonization of the Palaearctic
region out of South America in C5 is puzzling and could
either result from a long-distance dispersal event or from dis-
persal via the Nearctic region followed by regional extinction
In clade C6 the Palaearctic region was colonized from Africa
when both landmasses were very close (Fig 1) The genus
Sternolophus also presents some intriguing biogeographical
patterns such as a dispersal event from Africa toward Aus-
tralasia in the OligoceneMiocene possibly using the Kergue-
len plateau as a stepping-stone as hypothesized in allodapine
bees (Hymenoptera Apidae) (Schwarz et al 2006)
Our results moderately support the West Gondwanan
vicariant scenario (relative probability P = 18) with two
slightly less likely origins Afrotropical (P = 15) or wide-
spread (Africa+South America+Oriental P = 15) Consid-
ering the incomplete sampling in Hydrophilus and the
equiprobable Afrotropical origin (P = 29 Fig 3) of the
clade supported as being Oriental (P = 30) in the DEC+janalyses we believe that the widespread origin scenario is
less plausible than the two other alternatives (West Gond-
wana and Africa) In the Afrotropical origin scenario the
tribe would have dispersed across the Atlantic Ocean toward
South America This scenario is less straightforward than the
West Gondwana vicariant one but does not seem completely
implausible considering that such dispersal occurred at least
another time with the ancestor of Tropisternus (Fig 3)
Though the DEC model received significantly less support
than the DEC+J model in lsquoBioGeoBEARSrsquo it is relevant to
Table 2 Partitioning scheme and substitution models for the
beast analyses
Partition name PF AICc model
ARK GTR+I+GCO1 GTR+I+G18S TrN+I+G28S GTR+I+G
PF PartitionFinder AICc Akaike information criterion corrected
Table 3 Median divergence time estimates of major nodes
within Hydrophilini as recovered in the beast analyses
Node
Yule model
(95 HPD)
Birth-death model
(95 HPD)
Root 13845 (13460ndash15083) 13846 (13460ndash15125)Hydrobiusini 8493 (6518ndash10765) 8552 (6508ndash10891)C1 (Hydrophilini) 12385 (10308ndash14349) 12253 (10067ndash14149)C2 11781 (9670ndash13649) 11630 (9600ndash13629)C3 11471 (9377ndash13529) 11396 (9183ndash13350)C4 (Hydrobiomorpha) 6598 (4721ndash8474) 6547 (4758ndash8526)C5 (Hydrophilus) 9512 (7676ndash11305) 9397 (7604ndash11247)C6 (Hydrochara) 4264 (2980ndash5793) 4256 (2973ndash5809)C7 (Sternolophus) 3770 (2712ndash5006) 3728 (2710ndash4989)C8 (Tropisternus) 5778 (4348ndash7329) 5717 (4348ndash7300)
Median ages in millions of years (Myr) HPD highest posterior
density
Table 4 Rates of the different gene fragments in Hydrophilini as estimated from the beast analyses using Bayesian lognormal relaxedclocks
Gene
Yule model Birth-death model
Mean rate ( SD) ucldmean ( SD) Mean rate ( SD) ucldmean ( SD)
CO1 001041 000136 001123 000172 001045 000134 001135 000174
ARK 000060 000007 000061 000008 000060 000007 000061 000008
18S 000006 000001 000007 000001 000006 000001 000007 000001
28S 000052 000006 000060 000011 000052 000006 000060 000010
Mean rate number of substitutions per site divided by the tree length ucldmean mean of branch rates SD standard deviation
Figure 3 Divergence times and palaeobiogeography of the tribe Hydrophilini Chronogram derived from the MCC tree beast analysis
presenting the median ages estimated as well as the 95 credibility intervals (horizontal grey bars) Range distribution of each species isgiven on the right of the chronogram following the colour-coded caption inserted at the bottom of the figure The most likely ancestral
range as estimated under the DEC+j model in lsquoBioGeoBEARSrsquo is presented at each node as a coloured square Nodes for which the
likelihood of the ancestral state is superior to 50 are highlighted with an asterisk For major nodes with lower probability the threemost likely states are presented in a box For more derived nodes with low probability only the second most likely state is given with a
letter corresponding to the inserted caption The results of the DEC model are also presented with coloured circles for each node wherethe ancestral estimated range differs from the one estimated under the DEC+j model For more details on the relative probabilities of
both models refer to Appendix S3 The timeframe of West Gondwana (Africa and South America) breakup is indicated by a large greyrectangle and a representation of the two landmasses c 100 Ma according to the model of Seton et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
8
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
9
Biogeography of Hydrophilini giant water scavenger beetles
compare results from the two methods here The founder-
event jump dispersal parameter j has been proven to be par-
ticularly relevant in island systems (Matzke 2014) where it
often significantly improves the likelihood of the model
However it is not entirely clear if or how this parameter is
relevant in continental island-like settings and more impor-
tantly in non-island-like continental settings In Hydrophi-
lini the j parameter is the main factor explaining the
biogeographical history of the group whereas the role of
extinction and range expansion is much reduced (see
Results) Considering the inferred negligible value of the
extinction parameter e in DEC+j it seems difficult to invoke
range expansion followed by extinction in hydrophilines In
contrast in the DEC model extinction and range expansion
play a crucial role as illustrated by the complex biogeo-
graphical scenario inferred (Fig 3 see Appendix S3) Indeed
most range expansion and vicariant events inferred by the
DEC model are difficult to reconciliate with the arrangement
of landmasses at the time without invoking regional
extinction
The fossil record indicates that at least some regional extinc-
tion has occurred in Hydrophilini (Fikacek et al 2010) Four
genera of Hydrophilini have Eocene representatives that have
been found in the Palaearctic region and two have Eocene rep-
resentatives from the Nearctic region Although our biogeo-
graphical reconstructions are consistent with such
distributions in Hydrochara (Palaearctic) Hydrophilus (Nearc-
tic and Palaearctic) and Tropisternus (Nearctic) the lack of
present-day Palaearctic Hydrobiomorpha suggests regional
extinction Thus although the DEC+j model receives a much
better likelihood than the DEC model it might not entirely
capture the complexity of the evolutionary history in this
group The DEC model on the other hand recovers extinction
and range expansion as important forces driving the biogeo-
graphical evolution of hydrophiline water beetles It also
implies biologically intricate biogeographical processes such as
repeated long-distance dispersal and regional extinction which
might be obscured by a potential role of Antarctica in shaping
the biogeography of the group Despite the stronger statistical
support for the DEC+j model over the DEC model it is not
clear which model is the most appropriate in the case of
Hydrophilini biogeographical history Unfortunately it is not
presently possible to place the described fossils in the present
phylogenetic framework because there is not enough morpho-
logical support for the inclusion of these taxa beyond generic
assignments Therefore it will be important to revise the
inferred patterns in the light of denser taxon sampling and bet-
ter knowledge of the fossil record as these can partly obscure
macroevolutionary patterns (eg Meseguer et al 2015 Tous-
saint amp Condamine 2016)
Comparison with other West Gondwana vicariance
patterns
Our ancestral range estimation recovers with moderate sup-
port a West Gondwana vicariant pattern with a joint ancestral
distribution in these two regions A recent study on Sericini
chafers (Coleoptera Scarabaeidae) recovered a similar pattern
with the best biogeographical model estimating a vicariant
split consistent with the West Gondwana vicariance hypothe-
sis (WGVH) (Eberle et al 2017 Fig 4) Likewise Luebert
et al (2017) recovered a potential case of vicariance support-
ing the WGVH in Boraginales (Asterids) with the upper
bound of their age estimate slightly overlapping with the tim-
ing of West Gondwana break-up (Fig 4) Flowering plants of
the families Combretaceae (Rosids Myrtales) and Elatinaceae
CentroplacaceaeMalpighiaceae (Rosids Malpighiales) have
also been recently suggested as a potential example of West
Gondwana vicariance (Berger et al 2016 Cai et al 2016)
Some clades with exclusive sister relationships between
Afrotropical and Neotropical lineages have been suggested as
good candidates for the WGVH For example the divergence
of the freshwater fish sister genera Arapaima and Heterosis
(Teleostei Osteoglossiformes) respectively found in South
America and Africa was dated from the Cretaceous (Fig 4)
Although the dating analyses were somewhat contradictory
these osteoglossiform fishes are amongst the best candidates
for the WGVH (Lavoue 2016) Aciliine diving beetles
(Coleoptera Dytiscidae) have also been suggested as a candi-
date for WGVH (Fig 4) although the results of dating anal-
yses were inconsistent when based on either crown or stem
fossil placement (Bukontaite et al 2014) A more compelling
example is found in the gecko family Sphaerodactylidae in
which Gamble et al (2008) recovered as split between Mor-
occo and Neotropical geckoes in the Upper Cretaceous con-
sistent with the WGVH In caecilians the family
Dermophiidae endemic to South America has been resolved
as sister to Siphonopidae distributed on each side of the
Atlantic Ocean with Neotropical siphonopids being the most
derived clade in the family The dating of the split between
the two families has been somewhat controversial with esti-
mates largely spanning the Lower Cretaceous (Kamei et al
2012) and younger ones postdating the West Gondwana
break-up (Pyron 2014)
In contrast other studies focusing on clades with a well-
supported sister-group relationship between Africa and South
America have rejected the WGVH For instance Givnish
et al (2004) suggested a very recent Miocene divergence
between the AfricanSouth American disjunct lineages in
Bromeliaceae and Rapateaceae suggesting long-distance dis-
persal Likewise the divergence between the African wild
almond genus Brabejum and its sister genus Panopsis from
South America was dated from the Eocene (Barker et al
2007) therefore rejecting the hypothesis of a West Gond-
wanan signature Other examples of molecular divergence
time estimates that are irreconcilable with the WGVH are
also found in cichlid fishes (Matschiner et al 2017 but see
Lopez-Fernandez et al 2013) amphisbaenian worm lizards
(Longrich et al 2015) Leguminosae (Meng et al 2014)
and Sapotaceae (Bartish et al 2011)
Although we relied on a rather limited fraction of the total
diversity of hydrophiline water beetles we included most of
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
10
E F A Toussaint et al
Figure 4 Examples of clades supporting the West Gondwana vicariance hypothesis Overview of clades for which the West Gondwanavicariance hypothesis (WGVH) was suggested based on molecular dating andor model-based biogeographical estimationreconstruction
The divergence times for the focal nodes representing the split between Africa and South America are given for each clade as credibilityintervals Names with an asterisk indicate that in the selected study an alternative analysis did not support the WGVH For more details
on these alternative analyses please refer to the original publications The timeframe of West Gondwana (Africa and South America)breakup is indicated by a large grey rectangle and a representation of the two landmasses c 100 Ma according to the model of Seton
et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
11
Biogeography of Hydrophilini giant water scavenger beetles
the taxonomic and geographical diversity for each genus
Given that the missing taxa can be morphologically assigned
to sampled clades and more specifically that missing
Neotropical taxa are morphologically supported as members
of sampled Neotropical clades the possibility that our bio-
geographical estimation is biased by incomplete taxon sam-
pling is very unlikely The lack of an exclusive sister
relationship and the moderate relative probability for a sce-
nario supporting the WGVH suggest that a conservative view
of hydrophiline biogeographical history is prudent Future
empirical studies with denser taxon sampling will help to
confirm or revise this evolutionary pattern This study adds
to the scarce literature supporting the WGVH and is thus
important to our understanding of the relationship between
Gondwanan tectonic events and biogeographical evolution of
clades in the Cretaceous There is no doubt that the increas-
ing number of empirical studies using molecular dating and
model-based approaches will shed new light on the heated
debate between ancient vicariance and dispersalism
ACKNOWLEDGEMENTS
We would like to acknowledge the editors Mike Dawson and
Isabel Sanmartın as well as three anonymous reviewers for
constructive comments on earlier drafts of this paper We
thank the many colleagues that contributed tissues for this
study Kelly Miller Ignacio Ribera Michael Balke Robert
Sites Yusuke Minoshima Johannes Bergsten and Michael
Caterino Martin Fikacek provided material as well as critical
analysis of the fossil calibrations This study was funded in
part by a University of Kansas General Research Fund grant
to AEZS
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Andujar C Faille A Perez-Gonzalez S Zaballos JP
Vogler AP amp Ribera I (2016) Gondwanian relicts and
oceanic dispersal in a cosmopolitan radiation of euedaphic
ground beetles Molecular Phylogenetics and Evolution 99
235ndash246Barker NP Weston PH Rutschmann F amp Sauquet H
(2007) Molecular dating of the lsquoGondwananrsquo plant family
Proteaceae is only partially congruent with the timing of
the break-up of Gondwana Journal of Biogeography 34
2012ndash2027Bartish IV Antonelli A Richardson JE amp Swenson U
(2011) Vicariance or long-distance dispersal historical bio-
geography of the pantropical subfamily Chrysophylloideae
(Sapotaceae) Journal of Biogeography 38 177ndash190Beaulieu JM Tank DC amp Donoghue MJ (2013) A
Southern Hemisphere origin for campanulid angiosperms
with traces of the break-up of Gondwana BMC Evolution-
ary Biology 13 1
Berger BA Kriebel R Spalink D amp Sytsma KJ (2016)
Divergence times historical biogeography and shifts in
speciation rates of Myrtales Molecular Phylogenetics and
Evolution 95 116ndash136Bloom DD Fikacek M amp Short AEZ (2014) Clade age
and diversification rate variation explain disparity in spe-
cies richness among water scavenger beetle (Hydrophili-
dae) lineages PLoS ONE 9 e98430
Bukontaite R Miller KB amp Bergsten J (2014) The utility
of CAD in recovering Gondwanan vicariance events and
the evolutionary history of Aciliini (Coleoptera Dytisci-
dae) BMC Evolutionary Biology 14 5
Cai L Xi Z Peterson K Rushworth C Beaulieu J amp
Davis CC (2016) Phylogeny of Elatinaceae and the tropi-
cal Gondwanan origin of the Centroplacaceae (Malpighi-
aceae Elatinaceae) clade PLoS ONE 11 e0161881
Drummond AJ Suchard MA Xie D amp Rambaut A
(2012) Bayesian phylogenetics with BEAUti and the
BEAST 17 Molecular Biology and Evolution 29 1969ndash1973
Eberle J Fabrizi S Lago P amp Ahrens D (2017) A histori-
cal biogeography of megadiverse Sericinimdashanother story
ldquoout of Africardquo Cladistics in press doi 101111cla12162
Edgar RC (2004) MUSCLE multiple sequence alignment
with high accuracy and high throughput Nucleic Acids
Research 32 1792ndash1797Fikacek M Wedmann S amp Schmied H (2010) Diversifica-
tion of the greater hydrophilines clade of giant water scav-
enger beetles dated back to the Middle
Eocene (Coleoptera Hydrophilidae Hydrophilina) Inver-
tebrate Systematics 24 9ndash22Fikacek M Prokin A Yan E Yue Y Wang B Ren D
amp Beattie R (2014) Modern hydrophilid clades present
and widespread in the Late Jurassic and Early Cretaceous
(Coleoptera Hydrophiloidea Hydrophilidae) Zoological
Journal of the Linnean Society 170 710ndash734Gamble T Bauer AM Greenbaum E amp Jackman TR
(2008) Evidence for Gondwanan vicariance in an ancient
clade of gecko lizards Journal of Biogeography 35 88ndash104Gibbons AD Whittaker JM amp Meurouller RD (2013) The
breakup of East Gondwana assimilating constraints from
Cretaceous ocean basins around India into a best-fit tec-
tonic model Journal of Geophysical Research Solid Earth
118 808ndash822Givnish TJ Millam KC Evans TM Hall JC Pires
JC Berry PE amp Sytsma KJ (2004) Ancient vicariance
or recent long-distance dispersal Inferences about phy-
logeny and South American-African disjunctions in Rap-
ateaceae and Bromeliaceae based on ndhF sequence data
International Journal of Plant Sciences 165 S35ndashS54Hansen M (1999) World catalogue of insects Volume 2
Hydrophiloidea (s str) (Coleoptera) Apollo Books Sten-
strup Denmark
Kamei RG San Mauro D Gower DJ Van Bocxlaer I
Sherratt E Thomas A Babu S Bossuyt F Wilkinson
M amp Biju SD (2012) Discovery of a new family of
amphibians from northeast India with ancient links to
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
12
E F A Toussaint et al
Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
mid-Eocene and in the Eocene We infer an EoceneMiocene
colonization of the Palaearctic region out of Africa in Hydro-
chara with subsequent colonization of the Nearctic region in
the Miocene We infer two Miocene dispersal events out of
Africa in Sternolophus toward the Australian and Oriental
regions In Tropisternus we infer a range expansion in the
Figure 1 Dispersal rate scaling matrices used in the lsquoBioGeoBEARSrsquo analyses Summary of the time slices used in the lsquoBioGeoBEARSrsquo
analyses and arranged from top to bottom in inversed chronological order Each time slice (TS1 to TS4) is presented with a mapderived from Seton et al (2012 copyright permission from Elsevier with order number 4007750560480) and a matrix of dispersal rate
scalers relative to potential geographical barriers and distance Several symbols are used to represent the possible barriers between thechosen areas A Africa U Australian region O Oriental region S South America N Nearctic P Palaearctic
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
5
Biogeography of Hydrophilini giant water scavenger beetles
Eocene toward the Nearctic region and a dispersal event out of
South America toward the Nearctic region in the Oligocene
The rest of present-day distribution of Hydrophilini is the
result of late dispersal events
Although most of the biogeographical pattern inferred is
robust with high ancestral range probabilities across the
chronogram some important nodes have equiprobable esti-
mated ancestral ranges (Fig 3) This is the case for instance
of the nodes corresponding to the root and clades C2 C4 C5
and C6 for which the second most likely ancestral range
received a relatively high likelihood (Fig 3 see Appendix S3)
Under the estimated DEC model (extinction rate = 001
dispersal rate = 001) the ancestral range with the highest
probability still supports a vicariant initial pattern in West
Gondwana although with lower probability Clade C2 is also
inferred as ancestrally Neotropical with subsequent range
expansion toward Africa in Clade C5 in the Upper Cretaceous
This scenario would imply local extinction in Africa followed
by recolonization of this region when both landmasses had
already been drifting apart for 20ndash30 Myr therefore invoking
long-distance dispersal The biogeographical scenario in Clade
C3 is different from the one inferred under the DEC+j model
Africa is the ancestral range but the daughter nodes present a
vicariant pattern respectively in Africa+Palaeacritc and Afri-
ca+South America In Clade C6 the ancestor would have
shifted its range toward the Nearctic region in the Oligocene
which is in line with palaeogeographic configuration at that
time The rest of the biogeographical history in C6 would
imply several vicariant events between Nearctic and Palaearctic
in the Oligocene and Miocene In clade C7 the most notable
change in comparison to the DEC+j model is the transition
from Africa to a wide range in Africa+Oriental region before a
dispersal event toward Australia in the Oligocene-Miocene In
clade C8 the DEC model recovers vicariant events instead of
dispersal events to explain the distribution of Nearctic Tropis-
ternus species
DISCUSSION
Systematics of Hydrophilini
Our recovered topology (Fig 2) largely agrees with prior
hypotheses of Hydrophilini relationships based on adult
morphology (Short 2010) with two notable exceptions the
monophyly of Hydrochara and the placement of the root
Short (2010) had resolved Hydrochara as a weakly supported
paraphyletic grade while we resolve the genus as mono-
phyletic with strong support and with the inclusion of Brow-
nephilus which contains two enigmatic species from the
Middle East This is not a surprising outcome as Hydrochara
has always been considered a natural group and shares
aedeagal morphology with Brownephilus Additional exami-
nation of the morphology of these two genera and a formal
synonymy of Brownephilus with Hydrochara is forthcoming
(A E Z Short unpublished data)
Though the unrooted networks are congruent the place-
ment of the root differs from Short (2010) After accounting
for the absence of Protistolophus in our analysis the compara-
ble root would insert between the Sternolophus and
the reminder of the Hydrophilini while we inferred it along
the branch between (Hydrobiomorpha+Hydrophilus) and
[Hydrochara+(Sternolophus+Tropisternus)] We believe our
inferred root placement is more congruent with the observed
morphological diversity and distributions of the genera Addi-
tionally even if the other root placement had been recovered
it would not alter a West Gondwana origin of the Hydrophilini
as Protistolophus is a Neotropical endemic and the ancestral
rage of Sternolophus is resolved as Afrotropical in our analysis
Biogeography of giant scavenger water beetles
Our results suggest with moderate support an ancestral origin
of the Hydrophilini in a vast region encompassing both Africa
and South America (ie West Gondwana) in the Lower Creta-
ceous about 120 Ma (Fig 3) At that time these regions were
largely connected and only began to drift apart in the mid-
Cretaceous from 120 to 100 Ma (Seton et al 2012) Follow-
ing this initial vicariance the biogeographical evolution of the
group was mainly driven by dispersal (but see the DEC model
in Fig 3) The dispersal events inferred in clades C4 and C5
respectively from South America toward Africa or Australasia
require a trans-oceanic dispersal explanation or continental
dispersal through Antarctica followed by extinction in the lat-
ter case Trans-oceanic dispersal events have been suggested
on other water beetle clades for instance in Platynectini div-
ing beetles (Coleoptera Dytiscidae) from the Oriental region
Table 1 Partitioning scheme and substitution models for the
W-Iq-Tree analyses
Partition name Composition W-IQ-TREE AICc model
P1 CO1 pos2 TIM2+I+GP2 CO1 pos1 TPM3+IP3 CO1 pos3 TIM2+I+GP4 ARK pos1 TPM3u+I+GP5 ARK pos2 K3P+I+GP6 ARK pos3 TPM2+I+GP7 18S TNe+I+GP8 28S GTR+I+G
Figure 2 Molecular phylogeny of the tribe Hydrophilini The topology derived from the MrBayes analysis is presented with nodal
support of the BI and ML analyses as indicated in the inserted caption The black vertical bar delimits outgroups used in this study andthe grey ones delimit the different genera of the tribe Hydrophilini Hydrochara and Brownephilus being found in a single clade the
paraphyly of the former is highlighted with a dashed vertical bar On the left part of the figure is presented a habitus of Hydrophilus
rufomarginatus from Africa
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
6
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
7
Biogeography of Hydrophilini giant water scavenger beetles
toward South America (Toussaint et al 2017) In clade C5
the dispersal from South America toward the Oriental region
(Fig 3) has to be explained by long-distance dispersal in the
Upper Cretaceous possibly toward India that at this time was
part of East Gondwana (Gibbons et al 2013) The lineages
would have persisted on the Indian plate until its docking
with Eurasia 30 Myr later (Seton et al 2012) Despite the
intense volcanism recorded during the drifting of India
examples of clades that survived such dramatic conditions
have been suggested (eg Toussaint et al 2016) The African
continent was later recolonized via range expansion in the
genus Hydrophilus (Fig 3) The colonization of the Palaearctic
region out of South America in C5 is puzzling and could
either result from a long-distance dispersal event or from dis-
persal via the Nearctic region followed by regional extinction
In clade C6 the Palaearctic region was colonized from Africa
when both landmasses were very close (Fig 1) The genus
Sternolophus also presents some intriguing biogeographical
patterns such as a dispersal event from Africa toward Aus-
tralasia in the OligoceneMiocene possibly using the Kergue-
len plateau as a stepping-stone as hypothesized in allodapine
bees (Hymenoptera Apidae) (Schwarz et al 2006)
Our results moderately support the West Gondwanan
vicariant scenario (relative probability P = 18) with two
slightly less likely origins Afrotropical (P = 15) or wide-
spread (Africa+South America+Oriental P = 15) Consid-
ering the incomplete sampling in Hydrophilus and the
equiprobable Afrotropical origin (P = 29 Fig 3) of the
clade supported as being Oriental (P = 30) in the DEC+janalyses we believe that the widespread origin scenario is
less plausible than the two other alternatives (West Gond-
wana and Africa) In the Afrotropical origin scenario the
tribe would have dispersed across the Atlantic Ocean toward
South America This scenario is less straightforward than the
West Gondwana vicariant one but does not seem completely
implausible considering that such dispersal occurred at least
another time with the ancestor of Tropisternus (Fig 3)
Though the DEC model received significantly less support
than the DEC+J model in lsquoBioGeoBEARSrsquo it is relevant to
Table 2 Partitioning scheme and substitution models for the
beast analyses
Partition name PF AICc model
ARK GTR+I+GCO1 GTR+I+G18S TrN+I+G28S GTR+I+G
PF PartitionFinder AICc Akaike information criterion corrected
Table 3 Median divergence time estimates of major nodes
within Hydrophilini as recovered in the beast analyses
Node
Yule model
(95 HPD)
Birth-death model
(95 HPD)
Root 13845 (13460ndash15083) 13846 (13460ndash15125)Hydrobiusini 8493 (6518ndash10765) 8552 (6508ndash10891)C1 (Hydrophilini) 12385 (10308ndash14349) 12253 (10067ndash14149)C2 11781 (9670ndash13649) 11630 (9600ndash13629)C3 11471 (9377ndash13529) 11396 (9183ndash13350)C4 (Hydrobiomorpha) 6598 (4721ndash8474) 6547 (4758ndash8526)C5 (Hydrophilus) 9512 (7676ndash11305) 9397 (7604ndash11247)C6 (Hydrochara) 4264 (2980ndash5793) 4256 (2973ndash5809)C7 (Sternolophus) 3770 (2712ndash5006) 3728 (2710ndash4989)C8 (Tropisternus) 5778 (4348ndash7329) 5717 (4348ndash7300)
Median ages in millions of years (Myr) HPD highest posterior
density
Table 4 Rates of the different gene fragments in Hydrophilini as estimated from the beast analyses using Bayesian lognormal relaxedclocks
Gene
Yule model Birth-death model
Mean rate ( SD) ucldmean ( SD) Mean rate ( SD) ucldmean ( SD)
CO1 001041 000136 001123 000172 001045 000134 001135 000174
ARK 000060 000007 000061 000008 000060 000007 000061 000008
18S 000006 000001 000007 000001 000006 000001 000007 000001
28S 000052 000006 000060 000011 000052 000006 000060 000010
Mean rate number of substitutions per site divided by the tree length ucldmean mean of branch rates SD standard deviation
Figure 3 Divergence times and palaeobiogeography of the tribe Hydrophilini Chronogram derived from the MCC tree beast analysis
presenting the median ages estimated as well as the 95 credibility intervals (horizontal grey bars) Range distribution of each species isgiven on the right of the chronogram following the colour-coded caption inserted at the bottom of the figure The most likely ancestral
range as estimated under the DEC+j model in lsquoBioGeoBEARSrsquo is presented at each node as a coloured square Nodes for which the
likelihood of the ancestral state is superior to 50 are highlighted with an asterisk For major nodes with lower probability the threemost likely states are presented in a box For more derived nodes with low probability only the second most likely state is given with a
letter corresponding to the inserted caption The results of the DEC model are also presented with coloured circles for each node wherethe ancestral estimated range differs from the one estimated under the DEC+j model For more details on the relative probabilities of
both models refer to Appendix S3 The timeframe of West Gondwana (Africa and South America) breakup is indicated by a large greyrectangle and a representation of the two landmasses c 100 Ma according to the model of Seton et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
8
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
9
Biogeography of Hydrophilini giant water scavenger beetles
compare results from the two methods here The founder-
event jump dispersal parameter j has been proven to be par-
ticularly relevant in island systems (Matzke 2014) where it
often significantly improves the likelihood of the model
However it is not entirely clear if or how this parameter is
relevant in continental island-like settings and more impor-
tantly in non-island-like continental settings In Hydrophi-
lini the j parameter is the main factor explaining the
biogeographical history of the group whereas the role of
extinction and range expansion is much reduced (see
Results) Considering the inferred negligible value of the
extinction parameter e in DEC+j it seems difficult to invoke
range expansion followed by extinction in hydrophilines In
contrast in the DEC model extinction and range expansion
play a crucial role as illustrated by the complex biogeo-
graphical scenario inferred (Fig 3 see Appendix S3) Indeed
most range expansion and vicariant events inferred by the
DEC model are difficult to reconciliate with the arrangement
of landmasses at the time without invoking regional
extinction
The fossil record indicates that at least some regional extinc-
tion has occurred in Hydrophilini (Fikacek et al 2010) Four
genera of Hydrophilini have Eocene representatives that have
been found in the Palaearctic region and two have Eocene rep-
resentatives from the Nearctic region Although our biogeo-
graphical reconstructions are consistent with such
distributions in Hydrochara (Palaearctic) Hydrophilus (Nearc-
tic and Palaearctic) and Tropisternus (Nearctic) the lack of
present-day Palaearctic Hydrobiomorpha suggests regional
extinction Thus although the DEC+j model receives a much
better likelihood than the DEC model it might not entirely
capture the complexity of the evolutionary history in this
group The DEC model on the other hand recovers extinction
and range expansion as important forces driving the biogeo-
graphical evolution of hydrophiline water beetles It also
implies biologically intricate biogeographical processes such as
repeated long-distance dispersal and regional extinction which
might be obscured by a potential role of Antarctica in shaping
the biogeography of the group Despite the stronger statistical
support for the DEC+j model over the DEC model it is not
clear which model is the most appropriate in the case of
Hydrophilini biogeographical history Unfortunately it is not
presently possible to place the described fossils in the present
phylogenetic framework because there is not enough morpho-
logical support for the inclusion of these taxa beyond generic
assignments Therefore it will be important to revise the
inferred patterns in the light of denser taxon sampling and bet-
ter knowledge of the fossil record as these can partly obscure
macroevolutionary patterns (eg Meseguer et al 2015 Tous-
saint amp Condamine 2016)
Comparison with other West Gondwana vicariance
patterns
Our ancestral range estimation recovers with moderate sup-
port a West Gondwana vicariant pattern with a joint ancestral
distribution in these two regions A recent study on Sericini
chafers (Coleoptera Scarabaeidae) recovered a similar pattern
with the best biogeographical model estimating a vicariant
split consistent with the West Gondwana vicariance hypothe-
sis (WGVH) (Eberle et al 2017 Fig 4) Likewise Luebert
et al (2017) recovered a potential case of vicariance support-
ing the WGVH in Boraginales (Asterids) with the upper
bound of their age estimate slightly overlapping with the tim-
ing of West Gondwana break-up (Fig 4) Flowering plants of
the families Combretaceae (Rosids Myrtales) and Elatinaceae
CentroplacaceaeMalpighiaceae (Rosids Malpighiales) have
also been recently suggested as a potential example of West
Gondwana vicariance (Berger et al 2016 Cai et al 2016)
Some clades with exclusive sister relationships between
Afrotropical and Neotropical lineages have been suggested as
good candidates for the WGVH For example the divergence
of the freshwater fish sister genera Arapaima and Heterosis
(Teleostei Osteoglossiformes) respectively found in South
America and Africa was dated from the Cretaceous (Fig 4)
Although the dating analyses were somewhat contradictory
these osteoglossiform fishes are amongst the best candidates
for the WGVH (Lavoue 2016) Aciliine diving beetles
(Coleoptera Dytiscidae) have also been suggested as a candi-
date for WGVH (Fig 4) although the results of dating anal-
yses were inconsistent when based on either crown or stem
fossil placement (Bukontaite et al 2014) A more compelling
example is found in the gecko family Sphaerodactylidae in
which Gamble et al (2008) recovered as split between Mor-
occo and Neotropical geckoes in the Upper Cretaceous con-
sistent with the WGVH In caecilians the family
Dermophiidae endemic to South America has been resolved
as sister to Siphonopidae distributed on each side of the
Atlantic Ocean with Neotropical siphonopids being the most
derived clade in the family The dating of the split between
the two families has been somewhat controversial with esti-
mates largely spanning the Lower Cretaceous (Kamei et al
2012) and younger ones postdating the West Gondwana
break-up (Pyron 2014)
In contrast other studies focusing on clades with a well-
supported sister-group relationship between Africa and South
America have rejected the WGVH For instance Givnish
et al (2004) suggested a very recent Miocene divergence
between the AfricanSouth American disjunct lineages in
Bromeliaceae and Rapateaceae suggesting long-distance dis-
persal Likewise the divergence between the African wild
almond genus Brabejum and its sister genus Panopsis from
South America was dated from the Eocene (Barker et al
2007) therefore rejecting the hypothesis of a West Gond-
wanan signature Other examples of molecular divergence
time estimates that are irreconcilable with the WGVH are
also found in cichlid fishes (Matschiner et al 2017 but see
Lopez-Fernandez et al 2013) amphisbaenian worm lizards
(Longrich et al 2015) Leguminosae (Meng et al 2014)
and Sapotaceae (Bartish et al 2011)
Although we relied on a rather limited fraction of the total
diversity of hydrophiline water beetles we included most of
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
10
E F A Toussaint et al
Figure 4 Examples of clades supporting the West Gondwana vicariance hypothesis Overview of clades for which the West Gondwanavicariance hypothesis (WGVH) was suggested based on molecular dating andor model-based biogeographical estimationreconstruction
The divergence times for the focal nodes representing the split between Africa and South America are given for each clade as credibilityintervals Names with an asterisk indicate that in the selected study an alternative analysis did not support the WGVH For more details
on these alternative analyses please refer to the original publications The timeframe of West Gondwana (Africa and South America)breakup is indicated by a large grey rectangle and a representation of the two landmasses c 100 Ma according to the model of Seton
et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
11
Biogeography of Hydrophilini giant water scavenger beetles
the taxonomic and geographical diversity for each genus
Given that the missing taxa can be morphologically assigned
to sampled clades and more specifically that missing
Neotropical taxa are morphologically supported as members
of sampled Neotropical clades the possibility that our bio-
geographical estimation is biased by incomplete taxon sam-
pling is very unlikely The lack of an exclusive sister
relationship and the moderate relative probability for a sce-
nario supporting the WGVH suggest that a conservative view
of hydrophiline biogeographical history is prudent Future
empirical studies with denser taxon sampling will help to
confirm or revise this evolutionary pattern This study adds
to the scarce literature supporting the WGVH and is thus
important to our understanding of the relationship between
Gondwanan tectonic events and biogeographical evolution of
clades in the Cretaceous There is no doubt that the increas-
ing number of empirical studies using molecular dating and
model-based approaches will shed new light on the heated
debate between ancient vicariance and dispersalism
ACKNOWLEDGEMENTS
We would like to acknowledge the editors Mike Dawson and
Isabel Sanmartın as well as three anonymous reviewers for
constructive comments on earlier drafts of this paper We
thank the many colleagues that contributed tissues for this
study Kelly Miller Ignacio Ribera Michael Balke Robert
Sites Yusuke Minoshima Johannes Bergsten and Michael
Caterino Martin Fikacek provided material as well as critical
analysis of the fossil calibrations This study was funded in
part by a University of Kansas General Research Fund grant
to AEZS
REFERENCES
Andujar C Faille A Perez-Gonzalez S Zaballos JP
Vogler AP amp Ribera I (2016) Gondwanian relicts and
oceanic dispersal in a cosmopolitan radiation of euedaphic
ground beetles Molecular Phylogenetics and Evolution 99
235ndash246Barker NP Weston PH Rutschmann F amp Sauquet H
(2007) Molecular dating of the lsquoGondwananrsquo plant family
Proteaceae is only partially congruent with the timing of
the break-up of Gondwana Journal of Biogeography 34
2012ndash2027Bartish IV Antonelli A Richardson JE amp Swenson U
(2011) Vicariance or long-distance dispersal historical bio-
geography of the pantropical subfamily Chrysophylloideae
(Sapotaceae) Journal of Biogeography 38 177ndash190Beaulieu JM Tank DC amp Donoghue MJ (2013) A
Southern Hemisphere origin for campanulid angiosperms
with traces of the break-up of Gondwana BMC Evolution-
ary Biology 13 1
Berger BA Kriebel R Spalink D amp Sytsma KJ (2016)
Divergence times historical biogeography and shifts in
speciation rates of Myrtales Molecular Phylogenetics and
Evolution 95 116ndash136Bloom DD Fikacek M amp Short AEZ (2014) Clade age
and diversification rate variation explain disparity in spe-
cies richness among water scavenger beetle (Hydrophili-
dae) lineages PLoS ONE 9 e98430
Bukontaite R Miller KB amp Bergsten J (2014) The utility
of CAD in recovering Gondwanan vicariance events and
the evolutionary history of Aciliini (Coleoptera Dytisci-
dae) BMC Evolutionary Biology 14 5
Cai L Xi Z Peterson K Rushworth C Beaulieu J amp
Davis CC (2016) Phylogeny of Elatinaceae and the tropi-
cal Gondwanan origin of the Centroplacaceae (Malpighi-
aceae Elatinaceae) clade PLoS ONE 11 e0161881
Drummond AJ Suchard MA Xie D amp Rambaut A
(2012) Bayesian phylogenetics with BEAUti and the
BEAST 17 Molecular Biology and Evolution 29 1969ndash1973
Eberle J Fabrizi S Lago P amp Ahrens D (2017) A histori-
cal biogeography of megadiverse Sericinimdashanother story
ldquoout of Africardquo Cladistics in press doi 101111cla12162
Edgar RC (2004) MUSCLE multiple sequence alignment
with high accuracy and high throughput Nucleic Acids
Research 32 1792ndash1797Fikacek M Wedmann S amp Schmied H (2010) Diversifica-
tion of the greater hydrophilines clade of giant water scav-
enger beetles dated back to the Middle
Eocene (Coleoptera Hydrophilidae Hydrophilina) Inver-
tebrate Systematics 24 9ndash22Fikacek M Prokin A Yan E Yue Y Wang B Ren D
amp Beattie R (2014) Modern hydrophilid clades present
and widespread in the Late Jurassic and Early Cretaceous
(Coleoptera Hydrophiloidea Hydrophilidae) Zoological
Journal of the Linnean Society 170 710ndash734Gamble T Bauer AM Greenbaum E amp Jackman TR
(2008) Evidence for Gondwanan vicariance in an ancient
clade of gecko lizards Journal of Biogeography 35 88ndash104Gibbons AD Whittaker JM amp Meurouller RD (2013) The
breakup of East Gondwana assimilating constraints from
Cretaceous ocean basins around India into a best-fit tec-
tonic model Journal of Geophysical Research Solid Earth
118 808ndash822Givnish TJ Millam KC Evans TM Hall JC Pires
JC Berry PE amp Sytsma KJ (2004) Ancient vicariance
or recent long-distance dispersal Inferences about phy-
logeny and South American-African disjunctions in Rap-
ateaceae and Bromeliaceae based on ndhF sequence data
International Journal of Plant Sciences 165 S35ndashS54Hansen M (1999) World catalogue of insects Volume 2
Hydrophiloidea (s str) (Coleoptera) Apollo Books Sten-
strup Denmark
Kamei RG San Mauro D Gower DJ Van Bocxlaer I
Sherratt E Thomas A Babu S Bossuyt F Wilkinson
M amp Biju SD (2012) Discovery of a new family of
amphibians from northeast India with ancient links to
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12
E F A Toussaint et al
Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
Eocene toward the Nearctic region and a dispersal event out of
South America toward the Nearctic region in the Oligocene
The rest of present-day distribution of Hydrophilini is the
result of late dispersal events
Although most of the biogeographical pattern inferred is
robust with high ancestral range probabilities across the
chronogram some important nodes have equiprobable esti-
mated ancestral ranges (Fig 3) This is the case for instance
of the nodes corresponding to the root and clades C2 C4 C5
and C6 for which the second most likely ancestral range
received a relatively high likelihood (Fig 3 see Appendix S3)
Under the estimated DEC model (extinction rate = 001
dispersal rate = 001) the ancestral range with the highest
probability still supports a vicariant initial pattern in West
Gondwana although with lower probability Clade C2 is also
inferred as ancestrally Neotropical with subsequent range
expansion toward Africa in Clade C5 in the Upper Cretaceous
This scenario would imply local extinction in Africa followed
by recolonization of this region when both landmasses had
already been drifting apart for 20ndash30 Myr therefore invoking
long-distance dispersal The biogeographical scenario in Clade
C3 is different from the one inferred under the DEC+j model
Africa is the ancestral range but the daughter nodes present a
vicariant pattern respectively in Africa+Palaeacritc and Afri-
ca+South America In Clade C6 the ancestor would have
shifted its range toward the Nearctic region in the Oligocene
which is in line with palaeogeographic configuration at that
time The rest of the biogeographical history in C6 would
imply several vicariant events between Nearctic and Palaearctic
in the Oligocene and Miocene In clade C7 the most notable
change in comparison to the DEC+j model is the transition
from Africa to a wide range in Africa+Oriental region before a
dispersal event toward Australia in the Oligocene-Miocene In
clade C8 the DEC model recovers vicariant events instead of
dispersal events to explain the distribution of Nearctic Tropis-
ternus species
DISCUSSION
Systematics of Hydrophilini
Our recovered topology (Fig 2) largely agrees with prior
hypotheses of Hydrophilini relationships based on adult
morphology (Short 2010) with two notable exceptions the
monophyly of Hydrochara and the placement of the root
Short (2010) had resolved Hydrochara as a weakly supported
paraphyletic grade while we resolve the genus as mono-
phyletic with strong support and with the inclusion of Brow-
nephilus which contains two enigmatic species from the
Middle East This is not a surprising outcome as Hydrochara
has always been considered a natural group and shares
aedeagal morphology with Brownephilus Additional exami-
nation of the morphology of these two genera and a formal
synonymy of Brownephilus with Hydrochara is forthcoming
(A E Z Short unpublished data)
Though the unrooted networks are congruent the place-
ment of the root differs from Short (2010) After accounting
for the absence of Protistolophus in our analysis the compara-
ble root would insert between the Sternolophus and
the reminder of the Hydrophilini while we inferred it along
the branch between (Hydrobiomorpha+Hydrophilus) and
[Hydrochara+(Sternolophus+Tropisternus)] We believe our
inferred root placement is more congruent with the observed
morphological diversity and distributions of the genera Addi-
tionally even if the other root placement had been recovered
it would not alter a West Gondwana origin of the Hydrophilini
as Protistolophus is a Neotropical endemic and the ancestral
rage of Sternolophus is resolved as Afrotropical in our analysis
Biogeography of giant scavenger water beetles
Our results suggest with moderate support an ancestral origin
of the Hydrophilini in a vast region encompassing both Africa
and South America (ie West Gondwana) in the Lower Creta-
ceous about 120 Ma (Fig 3) At that time these regions were
largely connected and only began to drift apart in the mid-
Cretaceous from 120 to 100 Ma (Seton et al 2012) Follow-
ing this initial vicariance the biogeographical evolution of the
group was mainly driven by dispersal (but see the DEC model
in Fig 3) The dispersal events inferred in clades C4 and C5
respectively from South America toward Africa or Australasia
require a trans-oceanic dispersal explanation or continental
dispersal through Antarctica followed by extinction in the lat-
ter case Trans-oceanic dispersal events have been suggested
on other water beetle clades for instance in Platynectini div-
ing beetles (Coleoptera Dytiscidae) from the Oriental region
Table 1 Partitioning scheme and substitution models for the
W-Iq-Tree analyses
Partition name Composition W-IQ-TREE AICc model
P1 CO1 pos2 TIM2+I+GP2 CO1 pos1 TPM3+IP3 CO1 pos3 TIM2+I+GP4 ARK pos1 TPM3u+I+GP5 ARK pos2 K3P+I+GP6 ARK pos3 TPM2+I+GP7 18S TNe+I+GP8 28S GTR+I+G
Figure 2 Molecular phylogeny of the tribe Hydrophilini The topology derived from the MrBayes analysis is presented with nodal
support of the BI and ML analyses as indicated in the inserted caption The black vertical bar delimits outgroups used in this study andthe grey ones delimit the different genera of the tribe Hydrophilini Hydrochara and Brownephilus being found in a single clade the
paraphyly of the former is highlighted with a dashed vertical bar On the left part of the figure is presented a habitus of Hydrophilus
rufomarginatus from Africa
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
6
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
7
Biogeography of Hydrophilini giant water scavenger beetles
toward South America (Toussaint et al 2017) In clade C5
the dispersal from South America toward the Oriental region
(Fig 3) has to be explained by long-distance dispersal in the
Upper Cretaceous possibly toward India that at this time was
part of East Gondwana (Gibbons et al 2013) The lineages
would have persisted on the Indian plate until its docking
with Eurasia 30 Myr later (Seton et al 2012) Despite the
intense volcanism recorded during the drifting of India
examples of clades that survived such dramatic conditions
have been suggested (eg Toussaint et al 2016) The African
continent was later recolonized via range expansion in the
genus Hydrophilus (Fig 3) The colonization of the Palaearctic
region out of South America in C5 is puzzling and could
either result from a long-distance dispersal event or from dis-
persal via the Nearctic region followed by regional extinction
In clade C6 the Palaearctic region was colonized from Africa
when both landmasses were very close (Fig 1) The genus
Sternolophus also presents some intriguing biogeographical
patterns such as a dispersal event from Africa toward Aus-
tralasia in the OligoceneMiocene possibly using the Kergue-
len plateau as a stepping-stone as hypothesized in allodapine
bees (Hymenoptera Apidae) (Schwarz et al 2006)
Our results moderately support the West Gondwanan
vicariant scenario (relative probability P = 18) with two
slightly less likely origins Afrotropical (P = 15) or wide-
spread (Africa+South America+Oriental P = 15) Consid-
ering the incomplete sampling in Hydrophilus and the
equiprobable Afrotropical origin (P = 29 Fig 3) of the
clade supported as being Oriental (P = 30) in the DEC+janalyses we believe that the widespread origin scenario is
less plausible than the two other alternatives (West Gond-
wana and Africa) In the Afrotropical origin scenario the
tribe would have dispersed across the Atlantic Ocean toward
South America This scenario is less straightforward than the
West Gondwana vicariant one but does not seem completely
implausible considering that such dispersal occurred at least
another time with the ancestor of Tropisternus (Fig 3)
Though the DEC model received significantly less support
than the DEC+J model in lsquoBioGeoBEARSrsquo it is relevant to
Table 2 Partitioning scheme and substitution models for the
beast analyses
Partition name PF AICc model
ARK GTR+I+GCO1 GTR+I+G18S TrN+I+G28S GTR+I+G
PF PartitionFinder AICc Akaike information criterion corrected
Table 3 Median divergence time estimates of major nodes
within Hydrophilini as recovered in the beast analyses
Node
Yule model
(95 HPD)
Birth-death model
(95 HPD)
Root 13845 (13460ndash15083) 13846 (13460ndash15125)Hydrobiusini 8493 (6518ndash10765) 8552 (6508ndash10891)C1 (Hydrophilini) 12385 (10308ndash14349) 12253 (10067ndash14149)C2 11781 (9670ndash13649) 11630 (9600ndash13629)C3 11471 (9377ndash13529) 11396 (9183ndash13350)C4 (Hydrobiomorpha) 6598 (4721ndash8474) 6547 (4758ndash8526)C5 (Hydrophilus) 9512 (7676ndash11305) 9397 (7604ndash11247)C6 (Hydrochara) 4264 (2980ndash5793) 4256 (2973ndash5809)C7 (Sternolophus) 3770 (2712ndash5006) 3728 (2710ndash4989)C8 (Tropisternus) 5778 (4348ndash7329) 5717 (4348ndash7300)
Median ages in millions of years (Myr) HPD highest posterior
density
Table 4 Rates of the different gene fragments in Hydrophilini as estimated from the beast analyses using Bayesian lognormal relaxedclocks
Gene
Yule model Birth-death model
Mean rate ( SD) ucldmean ( SD) Mean rate ( SD) ucldmean ( SD)
CO1 001041 000136 001123 000172 001045 000134 001135 000174
ARK 000060 000007 000061 000008 000060 000007 000061 000008
18S 000006 000001 000007 000001 000006 000001 000007 000001
28S 000052 000006 000060 000011 000052 000006 000060 000010
Mean rate number of substitutions per site divided by the tree length ucldmean mean of branch rates SD standard deviation
Figure 3 Divergence times and palaeobiogeography of the tribe Hydrophilini Chronogram derived from the MCC tree beast analysis
presenting the median ages estimated as well as the 95 credibility intervals (horizontal grey bars) Range distribution of each species isgiven on the right of the chronogram following the colour-coded caption inserted at the bottom of the figure The most likely ancestral
range as estimated under the DEC+j model in lsquoBioGeoBEARSrsquo is presented at each node as a coloured square Nodes for which the
likelihood of the ancestral state is superior to 50 are highlighted with an asterisk For major nodes with lower probability the threemost likely states are presented in a box For more derived nodes with low probability only the second most likely state is given with a
letter corresponding to the inserted caption The results of the DEC model are also presented with coloured circles for each node wherethe ancestral estimated range differs from the one estimated under the DEC+j model For more details on the relative probabilities of
both models refer to Appendix S3 The timeframe of West Gondwana (Africa and South America) breakup is indicated by a large greyrectangle and a representation of the two landmasses c 100 Ma according to the model of Seton et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
8
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
9
Biogeography of Hydrophilini giant water scavenger beetles
compare results from the two methods here The founder-
event jump dispersal parameter j has been proven to be par-
ticularly relevant in island systems (Matzke 2014) where it
often significantly improves the likelihood of the model
However it is not entirely clear if or how this parameter is
relevant in continental island-like settings and more impor-
tantly in non-island-like continental settings In Hydrophi-
lini the j parameter is the main factor explaining the
biogeographical history of the group whereas the role of
extinction and range expansion is much reduced (see
Results) Considering the inferred negligible value of the
extinction parameter e in DEC+j it seems difficult to invoke
range expansion followed by extinction in hydrophilines In
contrast in the DEC model extinction and range expansion
play a crucial role as illustrated by the complex biogeo-
graphical scenario inferred (Fig 3 see Appendix S3) Indeed
most range expansion and vicariant events inferred by the
DEC model are difficult to reconciliate with the arrangement
of landmasses at the time without invoking regional
extinction
The fossil record indicates that at least some regional extinc-
tion has occurred in Hydrophilini (Fikacek et al 2010) Four
genera of Hydrophilini have Eocene representatives that have
been found in the Palaearctic region and two have Eocene rep-
resentatives from the Nearctic region Although our biogeo-
graphical reconstructions are consistent with such
distributions in Hydrochara (Palaearctic) Hydrophilus (Nearc-
tic and Palaearctic) and Tropisternus (Nearctic) the lack of
present-day Palaearctic Hydrobiomorpha suggests regional
extinction Thus although the DEC+j model receives a much
better likelihood than the DEC model it might not entirely
capture the complexity of the evolutionary history in this
group The DEC model on the other hand recovers extinction
and range expansion as important forces driving the biogeo-
graphical evolution of hydrophiline water beetles It also
implies biologically intricate biogeographical processes such as
repeated long-distance dispersal and regional extinction which
might be obscured by a potential role of Antarctica in shaping
the biogeography of the group Despite the stronger statistical
support for the DEC+j model over the DEC model it is not
clear which model is the most appropriate in the case of
Hydrophilini biogeographical history Unfortunately it is not
presently possible to place the described fossils in the present
phylogenetic framework because there is not enough morpho-
logical support for the inclusion of these taxa beyond generic
assignments Therefore it will be important to revise the
inferred patterns in the light of denser taxon sampling and bet-
ter knowledge of the fossil record as these can partly obscure
macroevolutionary patterns (eg Meseguer et al 2015 Tous-
saint amp Condamine 2016)
Comparison with other West Gondwana vicariance
patterns
Our ancestral range estimation recovers with moderate sup-
port a West Gondwana vicariant pattern with a joint ancestral
distribution in these two regions A recent study on Sericini
chafers (Coleoptera Scarabaeidae) recovered a similar pattern
with the best biogeographical model estimating a vicariant
split consistent with the West Gondwana vicariance hypothe-
sis (WGVH) (Eberle et al 2017 Fig 4) Likewise Luebert
et al (2017) recovered a potential case of vicariance support-
ing the WGVH in Boraginales (Asterids) with the upper
bound of their age estimate slightly overlapping with the tim-
ing of West Gondwana break-up (Fig 4) Flowering plants of
the families Combretaceae (Rosids Myrtales) and Elatinaceae
CentroplacaceaeMalpighiaceae (Rosids Malpighiales) have
also been recently suggested as a potential example of West
Gondwana vicariance (Berger et al 2016 Cai et al 2016)
Some clades with exclusive sister relationships between
Afrotropical and Neotropical lineages have been suggested as
good candidates for the WGVH For example the divergence
of the freshwater fish sister genera Arapaima and Heterosis
(Teleostei Osteoglossiformes) respectively found in South
America and Africa was dated from the Cretaceous (Fig 4)
Although the dating analyses were somewhat contradictory
these osteoglossiform fishes are amongst the best candidates
for the WGVH (Lavoue 2016) Aciliine diving beetles
(Coleoptera Dytiscidae) have also been suggested as a candi-
date for WGVH (Fig 4) although the results of dating anal-
yses were inconsistent when based on either crown or stem
fossil placement (Bukontaite et al 2014) A more compelling
example is found in the gecko family Sphaerodactylidae in
which Gamble et al (2008) recovered as split between Mor-
occo and Neotropical geckoes in the Upper Cretaceous con-
sistent with the WGVH In caecilians the family
Dermophiidae endemic to South America has been resolved
as sister to Siphonopidae distributed on each side of the
Atlantic Ocean with Neotropical siphonopids being the most
derived clade in the family The dating of the split between
the two families has been somewhat controversial with esti-
mates largely spanning the Lower Cretaceous (Kamei et al
2012) and younger ones postdating the West Gondwana
break-up (Pyron 2014)
In contrast other studies focusing on clades with a well-
supported sister-group relationship between Africa and South
America have rejected the WGVH For instance Givnish
et al (2004) suggested a very recent Miocene divergence
between the AfricanSouth American disjunct lineages in
Bromeliaceae and Rapateaceae suggesting long-distance dis-
persal Likewise the divergence between the African wild
almond genus Brabejum and its sister genus Panopsis from
South America was dated from the Eocene (Barker et al
2007) therefore rejecting the hypothesis of a West Gond-
wanan signature Other examples of molecular divergence
time estimates that are irreconcilable with the WGVH are
also found in cichlid fishes (Matschiner et al 2017 but see
Lopez-Fernandez et al 2013) amphisbaenian worm lizards
(Longrich et al 2015) Leguminosae (Meng et al 2014)
and Sapotaceae (Bartish et al 2011)
Although we relied on a rather limited fraction of the total
diversity of hydrophiline water beetles we included most of
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
10
E F A Toussaint et al
Figure 4 Examples of clades supporting the West Gondwana vicariance hypothesis Overview of clades for which the West Gondwanavicariance hypothesis (WGVH) was suggested based on molecular dating andor model-based biogeographical estimationreconstruction
The divergence times for the focal nodes representing the split between Africa and South America are given for each clade as credibilityintervals Names with an asterisk indicate that in the selected study an alternative analysis did not support the WGVH For more details
on these alternative analyses please refer to the original publications The timeframe of West Gondwana (Africa and South America)breakup is indicated by a large grey rectangle and a representation of the two landmasses c 100 Ma according to the model of Seton
et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
11
Biogeography of Hydrophilini giant water scavenger beetles
the taxonomic and geographical diversity for each genus
Given that the missing taxa can be morphologically assigned
to sampled clades and more specifically that missing
Neotropical taxa are morphologically supported as members
of sampled Neotropical clades the possibility that our bio-
geographical estimation is biased by incomplete taxon sam-
pling is very unlikely The lack of an exclusive sister
relationship and the moderate relative probability for a sce-
nario supporting the WGVH suggest that a conservative view
of hydrophiline biogeographical history is prudent Future
empirical studies with denser taxon sampling will help to
confirm or revise this evolutionary pattern This study adds
to the scarce literature supporting the WGVH and is thus
important to our understanding of the relationship between
Gondwanan tectonic events and biogeographical evolution of
clades in the Cretaceous There is no doubt that the increas-
ing number of empirical studies using molecular dating and
model-based approaches will shed new light on the heated
debate between ancient vicariance and dispersalism
ACKNOWLEDGEMENTS
We would like to acknowledge the editors Mike Dawson and
Isabel Sanmartın as well as three anonymous reviewers for
constructive comments on earlier drafts of this paper We
thank the many colleagues that contributed tissues for this
study Kelly Miller Ignacio Ribera Michael Balke Robert
Sites Yusuke Minoshima Johannes Bergsten and Michael
Caterino Martin Fikacek provided material as well as critical
analysis of the fossil calibrations This study was funded in
part by a University of Kansas General Research Fund grant
to AEZS
REFERENCES
Andujar C Faille A Perez-Gonzalez S Zaballos JP
Vogler AP amp Ribera I (2016) Gondwanian relicts and
oceanic dispersal in a cosmopolitan radiation of euedaphic
ground beetles Molecular Phylogenetics and Evolution 99
235ndash246Barker NP Weston PH Rutschmann F amp Sauquet H
(2007) Molecular dating of the lsquoGondwananrsquo plant family
Proteaceae is only partially congruent with the timing of
the break-up of Gondwana Journal of Biogeography 34
2012ndash2027Bartish IV Antonelli A Richardson JE amp Swenson U
(2011) Vicariance or long-distance dispersal historical bio-
geography of the pantropical subfamily Chrysophylloideae
(Sapotaceae) Journal of Biogeography 38 177ndash190Beaulieu JM Tank DC amp Donoghue MJ (2013) A
Southern Hemisphere origin for campanulid angiosperms
with traces of the break-up of Gondwana BMC Evolution-
ary Biology 13 1
Berger BA Kriebel R Spalink D amp Sytsma KJ (2016)
Divergence times historical biogeography and shifts in
speciation rates of Myrtales Molecular Phylogenetics and
Evolution 95 116ndash136Bloom DD Fikacek M amp Short AEZ (2014) Clade age
and diversification rate variation explain disparity in spe-
cies richness among water scavenger beetle (Hydrophili-
dae) lineages PLoS ONE 9 e98430
Bukontaite R Miller KB amp Bergsten J (2014) The utility
of CAD in recovering Gondwanan vicariance events and
the evolutionary history of Aciliini (Coleoptera Dytisci-
dae) BMC Evolutionary Biology 14 5
Cai L Xi Z Peterson K Rushworth C Beaulieu J amp
Davis CC (2016) Phylogeny of Elatinaceae and the tropi-
cal Gondwanan origin of the Centroplacaceae (Malpighi-
aceae Elatinaceae) clade PLoS ONE 11 e0161881
Drummond AJ Suchard MA Xie D amp Rambaut A
(2012) Bayesian phylogenetics with BEAUti and the
BEAST 17 Molecular Biology and Evolution 29 1969ndash1973
Eberle J Fabrizi S Lago P amp Ahrens D (2017) A histori-
cal biogeography of megadiverse Sericinimdashanother story
ldquoout of Africardquo Cladistics in press doi 101111cla12162
Edgar RC (2004) MUSCLE multiple sequence alignment
with high accuracy and high throughput Nucleic Acids
Research 32 1792ndash1797Fikacek M Wedmann S amp Schmied H (2010) Diversifica-
tion of the greater hydrophilines clade of giant water scav-
enger beetles dated back to the Middle
Eocene (Coleoptera Hydrophilidae Hydrophilina) Inver-
tebrate Systematics 24 9ndash22Fikacek M Prokin A Yan E Yue Y Wang B Ren D
amp Beattie R (2014) Modern hydrophilid clades present
and widespread in the Late Jurassic and Early Cretaceous
(Coleoptera Hydrophiloidea Hydrophilidae) Zoological
Journal of the Linnean Society 170 710ndash734Gamble T Bauer AM Greenbaum E amp Jackman TR
(2008) Evidence for Gondwanan vicariance in an ancient
clade of gecko lizards Journal of Biogeography 35 88ndash104Gibbons AD Whittaker JM amp Meurouller RD (2013) The
breakup of East Gondwana assimilating constraints from
Cretaceous ocean basins around India into a best-fit tec-
tonic model Journal of Geophysical Research Solid Earth
118 808ndash822Givnish TJ Millam KC Evans TM Hall JC Pires
JC Berry PE amp Sytsma KJ (2004) Ancient vicariance
or recent long-distance dispersal Inferences about phy-
logeny and South American-African disjunctions in Rap-
ateaceae and Bromeliaceae based on ndhF sequence data
International Journal of Plant Sciences 165 S35ndashS54Hansen M (1999) World catalogue of insects Volume 2
Hydrophiloidea (s str) (Coleoptera) Apollo Books Sten-
strup Denmark
Kamei RG San Mauro D Gower DJ Van Bocxlaer I
Sherratt E Thomas A Babu S Bossuyt F Wilkinson
M amp Biju SD (2012) Discovery of a new family of
amphibians from northeast India with ancient links to
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
12
E F A Toussaint et al
Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
7
Biogeography of Hydrophilini giant water scavenger beetles
toward South America (Toussaint et al 2017) In clade C5
the dispersal from South America toward the Oriental region
(Fig 3) has to be explained by long-distance dispersal in the
Upper Cretaceous possibly toward India that at this time was
part of East Gondwana (Gibbons et al 2013) The lineages
would have persisted on the Indian plate until its docking
with Eurasia 30 Myr later (Seton et al 2012) Despite the
intense volcanism recorded during the drifting of India
examples of clades that survived such dramatic conditions
have been suggested (eg Toussaint et al 2016) The African
continent was later recolonized via range expansion in the
genus Hydrophilus (Fig 3) The colonization of the Palaearctic
region out of South America in C5 is puzzling and could
either result from a long-distance dispersal event or from dis-
persal via the Nearctic region followed by regional extinction
In clade C6 the Palaearctic region was colonized from Africa
when both landmasses were very close (Fig 1) The genus
Sternolophus also presents some intriguing biogeographical
patterns such as a dispersal event from Africa toward Aus-
tralasia in the OligoceneMiocene possibly using the Kergue-
len plateau as a stepping-stone as hypothesized in allodapine
bees (Hymenoptera Apidae) (Schwarz et al 2006)
Our results moderately support the West Gondwanan
vicariant scenario (relative probability P = 18) with two
slightly less likely origins Afrotropical (P = 15) or wide-
spread (Africa+South America+Oriental P = 15) Consid-
ering the incomplete sampling in Hydrophilus and the
equiprobable Afrotropical origin (P = 29 Fig 3) of the
clade supported as being Oriental (P = 30) in the DEC+janalyses we believe that the widespread origin scenario is
less plausible than the two other alternatives (West Gond-
wana and Africa) In the Afrotropical origin scenario the
tribe would have dispersed across the Atlantic Ocean toward
South America This scenario is less straightforward than the
West Gondwana vicariant one but does not seem completely
implausible considering that such dispersal occurred at least
another time with the ancestor of Tropisternus (Fig 3)
Though the DEC model received significantly less support
than the DEC+J model in lsquoBioGeoBEARSrsquo it is relevant to
Table 2 Partitioning scheme and substitution models for the
beast analyses
Partition name PF AICc model
ARK GTR+I+GCO1 GTR+I+G18S TrN+I+G28S GTR+I+G
PF PartitionFinder AICc Akaike information criterion corrected
Table 3 Median divergence time estimates of major nodes
within Hydrophilini as recovered in the beast analyses
Node
Yule model
(95 HPD)
Birth-death model
(95 HPD)
Root 13845 (13460ndash15083) 13846 (13460ndash15125)Hydrobiusini 8493 (6518ndash10765) 8552 (6508ndash10891)C1 (Hydrophilini) 12385 (10308ndash14349) 12253 (10067ndash14149)C2 11781 (9670ndash13649) 11630 (9600ndash13629)C3 11471 (9377ndash13529) 11396 (9183ndash13350)C4 (Hydrobiomorpha) 6598 (4721ndash8474) 6547 (4758ndash8526)C5 (Hydrophilus) 9512 (7676ndash11305) 9397 (7604ndash11247)C6 (Hydrochara) 4264 (2980ndash5793) 4256 (2973ndash5809)C7 (Sternolophus) 3770 (2712ndash5006) 3728 (2710ndash4989)C8 (Tropisternus) 5778 (4348ndash7329) 5717 (4348ndash7300)
Median ages in millions of years (Myr) HPD highest posterior
density
Table 4 Rates of the different gene fragments in Hydrophilini as estimated from the beast analyses using Bayesian lognormal relaxedclocks
Gene
Yule model Birth-death model
Mean rate ( SD) ucldmean ( SD) Mean rate ( SD) ucldmean ( SD)
CO1 001041 000136 001123 000172 001045 000134 001135 000174
ARK 000060 000007 000061 000008 000060 000007 000061 000008
18S 000006 000001 000007 000001 000006 000001 000007 000001
28S 000052 000006 000060 000011 000052 000006 000060 000010
Mean rate number of substitutions per site divided by the tree length ucldmean mean of branch rates SD standard deviation
Figure 3 Divergence times and palaeobiogeography of the tribe Hydrophilini Chronogram derived from the MCC tree beast analysis
presenting the median ages estimated as well as the 95 credibility intervals (horizontal grey bars) Range distribution of each species isgiven on the right of the chronogram following the colour-coded caption inserted at the bottom of the figure The most likely ancestral
range as estimated under the DEC+j model in lsquoBioGeoBEARSrsquo is presented at each node as a coloured square Nodes for which the
likelihood of the ancestral state is superior to 50 are highlighted with an asterisk For major nodes with lower probability the threemost likely states are presented in a box For more derived nodes with low probability only the second most likely state is given with a
letter corresponding to the inserted caption The results of the DEC model are also presented with coloured circles for each node wherethe ancestral estimated range differs from the one estimated under the DEC+j model For more details on the relative probabilities of
both models refer to Appendix S3 The timeframe of West Gondwana (Africa and South America) breakup is indicated by a large greyrectangle and a representation of the two landmasses c 100 Ma according to the model of Seton et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
8
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
9
Biogeography of Hydrophilini giant water scavenger beetles
compare results from the two methods here The founder-
event jump dispersal parameter j has been proven to be par-
ticularly relevant in island systems (Matzke 2014) where it
often significantly improves the likelihood of the model
However it is not entirely clear if or how this parameter is
relevant in continental island-like settings and more impor-
tantly in non-island-like continental settings In Hydrophi-
lini the j parameter is the main factor explaining the
biogeographical history of the group whereas the role of
extinction and range expansion is much reduced (see
Results) Considering the inferred negligible value of the
extinction parameter e in DEC+j it seems difficult to invoke
range expansion followed by extinction in hydrophilines In
contrast in the DEC model extinction and range expansion
play a crucial role as illustrated by the complex biogeo-
graphical scenario inferred (Fig 3 see Appendix S3) Indeed
most range expansion and vicariant events inferred by the
DEC model are difficult to reconciliate with the arrangement
of landmasses at the time without invoking regional
extinction
The fossil record indicates that at least some regional extinc-
tion has occurred in Hydrophilini (Fikacek et al 2010) Four
genera of Hydrophilini have Eocene representatives that have
been found in the Palaearctic region and two have Eocene rep-
resentatives from the Nearctic region Although our biogeo-
graphical reconstructions are consistent with such
distributions in Hydrochara (Palaearctic) Hydrophilus (Nearc-
tic and Palaearctic) and Tropisternus (Nearctic) the lack of
present-day Palaearctic Hydrobiomorpha suggests regional
extinction Thus although the DEC+j model receives a much
better likelihood than the DEC model it might not entirely
capture the complexity of the evolutionary history in this
group The DEC model on the other hand recovers extinction
and range expansion as important forces driving the biogeo-
graphical evolution of hydrophiline water beetles It also
implies biologically intricate biogeographical processes such as
repeated long-distance dispersal and regional extinction which
might be obscured by a potential role of Antarctica in shaping
the biogeography of the group Despite the stronger statistical
support for the DEC+j model over the DEC model it is not
clear which model is the most appropriate in the case of
Hydrophilini biogeographical history Unfortunately it is not
presently possible to place the described fossils in the present
phylogenetic framework because there is not enough morpho-
logical support for the inclusion of these taxa beyond generic
assignments Therefore it will be important to revise the
inferred patterns in the light of denser taxon sampling and bet-
ter knowledge of the fossil record as these can partly obscure
macroevolutionary patterns (eg Meseguer et al 2015 Tous-
saint amp Condamine 2016)
Comparison with other West Gondwana vicariance
patterns
Our ancestral range estimation recovers with moderate sup-
port a West Gondwana vicariant pattern with a joint ancestral
distribution in these two regions A recent study on Sericini
chafers (Coleoptera Scarabaeidae) recovered a similar pattern
with the best biogeographical model estimating a vicariant
split consistent with the West Gondwana vicariance hypothe-
sis (WGVH) (Eberle et al 2017 Fig 4) Likewise Luebert
et al (2017) recovered a potential case of vicariance support-
ing the WGVH in Boraginales (Asterids) with the upper
bound of their age estimate slightly overlapping with the tim-
ing of West Gondwana break-up (Fig 4) Flowering plants of
the families Combretaceae (Rosids Myrtales) and Elatinaceae
CentroplacaceaeMalpighiaceae (Rosids Malpighiales) have
also been recently suggested as a potential example of West
Gondwana vicariance (Berger et al 2016 Cai et al 2016)
Some clades with exclusive sister relationships between
Afrotropical and Neotropical lineages have been suggested as
good candidates for the WGVH For example the divergence
of the freshwater fish sister genera Arapaima and Heterosis
(Teleostei Osteoglossiformes) respectively found in South
America and Africa was dated from the Cretaceous (Fig 4)
Although the dating analyses were somewhat contradictory
these osteoglossiform fishes are amongst the best candidates
for the WGVH (Lavoue 2016) Aciliine diving beetles
(Coleoptera Dytiscidae) have also been suggested as a candi-
date for WGVH (Fig 4) although the results of dating anal-
yses were inconsistent when based on either crown or stem
fossil placement (Bukontaite et al 2014) A more compelling
example is found in the gecko family Sphaerodactylidae in
which Gamble et al (2008) recovered as split between Mor-
occo and Neotropical geckoes in the Upper Cretaceous con-
sistent with the WGVH In caecilians the family
Dermophiidae endemic to South America has been resolved
as sister to Siphonopidae distributed on each side of the
Atlantic Ocean with Neotropical siphonopids being the most
derived clade in the family The dating of the split between
the two families has been somewhat controversial with esti-
mates largely spanning the Lower Cretaceous (Kamei et al
2012) and younger ones postdating the West Gondwana
break-up (Pyron 2014)
In contrast other studies focusing on clades with a well-
supported sister-group relationship between Africa and South
America have rejected the WGVH For instance Givnish
et al (2004) suggested a very recent Miocene divergence
between the AfricanSouth American disjunct lineages in
Bromeliaceae and Rapateaceae suggesting long-distance dis-
persal Likewise the divergence between the African wild
almond genus Brabejum and its sister genus Panopsis from
South America was dated from the Eocene (Barker et al
2007) therefore rejecting the hypothesis of a West Gond-
wanan signature Other examples of molecular divergence
time estimates that are irreconcilable with the WGVH are
also found in cichlid fishes (Matschiner et al 2017 but see
Lopez-Fernandez et al 2013) amphisbaenian worm lizards
(Longrich et al 2015) Leguminosae (Meng et al 2014)
and Sapotaceae (Bartish et al 2011)
Although we relied on a rather limited fraction of the total
diversity of hydrophiline water beetles we included most of
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
10
E F A Toussaint et al
Figure 4 Examples of clades supporting the West Gondwana vicariance hypothesis Overview of clades for which the West Gondwanavicariance hypothesis (WGVH) was suggested based on molecular dating andor model-based biogeographical estimationreconstruction
The divergence times for the focal nodes representing the split between Africa and South America are given for each clade as credibilityintervals Names with an asterisk indicate that in the selected study an alternative analysis did not support the WGVH For more details
on these alternative analyses please refer to the original publications The timeframe of West Gondwana (Africa and South America)breakup is indicated by a large grey rectangle and a representation of the two landmasses c 100 Ma according to the model of Seton
et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
11
Biogeography of Hydrophilini giant water scavenger beetles
the taxonomic and geographical diversity for each genus
Given that the missing taxa can be morphologically assigned
to sampled clades and more specifically that missing
Neotropical taxa are morphologically supported as members
of sampled Neotropical clades the possibility that our bio-
geographical estimation is biased by incomplete taxon sam-
pling is very unlikely The lack of an exclusive sister
relationship and the moderate relative probability for a sce-
nario supporting the WGVH suggest that a conservative view
of hydrophiline biogeographical history is prudent Future
empirical studies with denser taxon sampling will help to
confirm or revise this evolutionary pattern This study adds
to the scarce literature supporting the WGVH and is thus
important to our understanding of the relationship between
Gondwanan tectonic events and biogeographical evolution of
clades in the Cretaceous There is no doubt that the increas-
ing number of empirical studies using molecular dating and
model-based approaches will shed new light on the heated
debate between ancient vicariance and dispersalism
ACKNOWLEDGEMENTS
We would like to acknowledge the editors Mike Dawson and
Isabel Sanmartın as well as three anonymous reviewers for
constructive comments on earlier drafts of this paper We
thank the many colleagues that contributed tissues for this
study Kelly Miller Ignacio Ribera Michael Balke Robert
Sites Yusuke Minoshima Johannes Bergsten and Michael
Caterino Martin Fikacek provided material as well as critical
analysis of the fossil calibrations This study was funded in
part by a University of Kansas General Research Fund grant
to AEZS
REFERENCES
Andujar C Faille A Perez-Gonzalez S Zaballos JP
Vogler AP amp Ribera I (2016) Gondwanian relicts and
oceanic dispersal in a cosmopolitan radiation of euedaphic
ground beetles Molecular Phylogenetics and Evolution 99
235ndash246Barker NP Weston PH Rutschmann F amp Sauquet H
(2007) Molecular dating of the lsquoGondwananrsquo plant family
Proteaceae is only partially congruent with the timing of
the break-up of Gondwana Journal of Biogeography 34
2012ndash2027Bartish IV Antonelli A Richardson JE amp Swenson U
(2011) Vicariance or long-distance dispersal historical bio-
geography of the pantropical subfamily Chrysophylloideae
(Sapotaceae) Journal of Biogeography 38 177ndash190Beaulieu JM Tank DC amp Donoghue MJ (2013) A
Southern Hemisphere origin for campanulid angiosperms
with traces of the break-up of Gondwana BMC Evolution-
ary Biology 13 1
Berger BA Kriebel R Spalink D amp Sytsma KJ (2016)
Divergence times historical biogeography and shifts in
speciation rates of Myrtales Molecular Phylogenetics and
Evolution 95 116ndash136Bloom DD Fikacek M amp Short AEZ (2014) Clade age
and diversification rate variation explain disparity in spe-
cies richness among water scavenger beetle (Hydrophili-
dae) lineages PLoS ONE 9 e98430
Bukontaite R Miller KB amp Bergsten J (2014) The utility
of CAD in recovering Gondwanan vicariance events and
the evolutionary history of Aciliini (Coleoptera Dytisci-
dae) BMC Evolutionary Biology 14 5
Cai L Xi Z Peterson K Rushworth C Beaulieu J amp
Davis CC (2016) Phylogeny of Elatinaceae and the tropi-
cal Gondwanan origin of the Centroplacaceae (Malpighi-
aceae Elatinaceae) clade PLoS ONE 11 e0161881
Drummond AJ Suchard MA Xie D amp Rambaut A
(2012) Bayesian phylogenetics with BEAUti and the
BEAST 17 Molecular Biology and Evolution 29 1969ndash1973
Eberle J Fabrizi S Lago P amp Ahrens D (2017) A histori-
cal biogeography of megadiverse Sericinimdashanother story
ldquoout of Africardquo Cladistics in press doi 101111cla12162
Edgar RC (2004) MUSCLE multiple sequence alignment
with high accuracy and high throughput Nucleic Acids
Research 32 1792ndash1797Fikacek M Wedmann S amp Schmied H (2010) Diversifica-
tion of the greater hydrophilines clade of giant water scav-
enger beetles dated back to the Middle
Eocene (Coleoptera Hydrophilidae Hydrophilina) Inver-
tebrate Systematics 24 9ndash22Fikacek M Prokin A Yan E Yue Y Wang B Ren D
amp Beattie R (2014) Modern hydrophilid clades present
and widespread in the Late Jurassic and Early Cretaceous
(Coleoptera Hydrophiloidea Hydrophilidae) Zoological
Journal of the Linnean Society 170 710ndash734Gamble T Bauer AM Greenbaum E amp Jackman TR
(2008) Evidence for Gondwanan vicariance in an ancient
clade of gecko lizards Journal of Biogeography 35 88ndash104Gibbons AD Whittaker JM amp Meurouller RD (2013) The
breakup of East Gondwana assimilating constraints from
Cretaceous ocean basins around India into a best-fit tec-
tonic model Journal of Geophysical Research Solid Earth
118 808ndash822Givnish TJ Millam KC Evans TM Hall JC Pires
JC Berry PE amp Sytsma KJ (2004) Ancient vicariance
or recent long-distance dispersal Inferences about phy-
logeny and South American-African disjunctions in Rap-
ateaceae and Bromeliaceae based on ndhF sequence data
International Journal of Plant Sciences 165 S35ndashS54Hansen M (1999) World catalogue of insects Volume 2
Hydrophiloidea (s str) (Coleoptera) Apollo Books Sten-
strup Denmark
Kamei RG San Mauro D Gower DJ Van Bocxlaer I
Sherratt E Thomas A Babu S Bossuyt F Wilkinson
M amp Biju SD (2012) Discovery of a new family of
amphibians from northeast India with ancient links to
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
12
E F A Toussaint et al
Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
toward South America (Toussaint et al 2017) In clade C5
the dispersal from South America toward the Oriental region
(Fig 3) has to be explained by long-distance dispersal in the
Upper Cretaceous possibly toward India that at this time was
part of East Gondwana (Gibbons et al 2013) The lineages
would have persisted on the Indian plate until its docking
with Eurasia 30 Myr later (Seton et al 2012) Despite the
intense volcanism recorded during the drifting of India
examples of clades that survived such dramatic conditions
have been suggested (eg Toussaint et al 2016) The African
continent was later recolonized via range expansion in the
genus Hydrophilus (Fig 3) The colonization of the Palaearctic
region out of South America in C5 is puzzling and could
either result from a long-distance dispersal event or from dis-
persal via the Nearctic region followed by regional extinction
In clade C6 the Palaearctic region was colonized from Africa
when both landmasses were very close (Fig 1) The genus
Sternolophus also presents some intriguing biogeographical
patterns such as a dispersal event from Africa toward Aus-
tralasia in the OligoceneMiocene possibly using the Kergue-
len plateau as a stepping-stone as hypothesized in allodapine
bees (Hymenoptera Apidae) (Schwarz et al 2006)
Our results moderately support the West Gondwanan
vicariant scenario (relative probability P = 18) with two
slightly less likely origins Afrotropical (P = 15) or wide-
spread (Africa+South America+Oriental P = 15) Consid-
ering the incomplete sampling in Hydrophilus and the
equiprobable Afrotropical origin (P = 29 Fig 3) of the
clade supported as being Oriental (P = 30) in the DEC+janalyses we believe that the widespread origin scenario is
less plausible than the two other alternatives (West Gond-
wana and Africa) In the Afrotropical origin scenario the
tribe would have dispersed across the Atlantic Ocean toward
South America This scenario is less straightforward than the
West Gondwana vicariant one but does not seem completely
implausible considering that such dispersal occurred at least
another time with the ancestor of Tropisternus (Fig 3)
Though the DEC model received significantly less support
than the DEC+J model in lsquoBioGeoBEARSrsquo it is relevant to
Table 2 Partitioning scheme and substitution models for the
beast analyses
Partition name PF AICc model
ARK GTR+I+GCO1 GTR+I+G18S TrN+I+G28S GTR+I+G
PF PartitionFinder AICc Akaike information criterion corrected
Table 3 Median divergence time estimates of major nodes
within Hydrophilini as recovered in the beast analyses
Node
Yule model
(95 HPD)
Birth-death model
(95 HPD)
Root 13845 (13460ndash15083) 13846 (13460ndash15125)Hydrobiusini 8493 (6518ndash10765) 8552 (6508ndash10891)C1 (Hydrophilini) 12385 (10308ndash14349) 12253 (10067ndash14149)C2 11781 (9670ndash13649) 11630 (9600ndash13629)C3 11471 (9377ndash13529) 11396 (9183ndash13350)C4 (Hydrobiomorpha) 6598 (4721ndash8474) 6547 (4758ndash8526)C5 (Hydrophilus) 9512 (7676ndash11305) 9397 (7604ndash11247)C6 (Hydrochara) 4264 (2980ndash5793) 4256 (2973ndash5809)C7 (Sternolophus) 3770 (2712ndash5006) 3728 (2710ndash4989)C8 (Tropisternus) 5778 (4348ndash7329) 5717 (4348ndash7300)
Median ages in millions of years (Myr) HPD highest posterior
density
Table 4 Rates of the different gene fragments in Hydrophilini as estimated from the beast analyses using Bayesian lognormal relaxedclocks
Gene
Yule model Birth-death model
Mean rate ( SD) ucldmean ( SD) Mean rate ( SD) ucldmean ( SD)
CO1 001041 000136 001123 000172 001045 000134 001135 000174
ARK 000060 000007 000061 000008 000060 000007 000061 000008
18S 000006 000001 000007 000001 000006 000001 000007 000001
28S 000052 000006 000060 000011 000052 000006 000060 000010
Mean rate number of substitutions per site divided by the tree length ucldmean mean of branch rates SD standard deviation
Figure 3 Divergence times and palaeobiogeography of the tribe Hydrophilini Chronogram derived from the MCC tree beast analysis
presenting the median ages estimated as well as the 95 credibility intervals (horizontal grey bars) Range distribution of each species isgiven on the right of the chronogram following the colour-coded caption inserted at the bottom of the figure The most likely ancestral
range as estimated under the DEC+j model in lsquoBioGeoBEARSrsquo is presented at each node as a coloured square Nodes for which the
likelihood of the ancestral state is superior to 50 are highlighted with an asterisk For major nodes with lower probability the threemost likely states are presented in a box For more derived nodes with low probability only the second most likely state is given with a
letter corresponding to the inserted caption The results of the DEC model are also presented with coloured circles for each node wherethe ancestral estimated range differs from the one estimated under the DEC+j model For more details on the relative probabilities of
both models refer to Appendix S3 The timeframe of West Gondwana (Africa and South America) breakup is indicated by a large greyrectangle and a representation of the two landmasses c 100 Ma according to the model of Seton et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
8
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
9
Biogeography of Hydrophilini giant water scavenger beetles
compare results from the two methods here The founder-
event jump dispersal parameter j has been proven to be par-
ticularly relevant in island systems (Matzke 2014) where it
often significantly improves the likelihood of the model
However it is not entirely clear if or how this parameter is
relevant in continental island-like settings and more impor-
tantly in non-island-like continental settings In Hydrophi-
lini the j parameter is the main factor explaining the
biogeographical history of the group whereas the role of
extinction and range expansion is much reduced (see
Results) Considering the inferred negligible value of the
extinction parameter e in DEC+j it seems difficult to invoke
range expansion followed by extinction in hydrophilines In
contrast in the DEC model extinction and range expansion
play a crucial role as illustrated by the complex biogeo-
graphical scenario inferred (Fig 3 see Appendix S3) Indeed
most range expansion and vicariant events inferred by the
DEC model are difficult to reconciliate with the arrangement
of landmasses at the time without invoking regional
extinction
The fossil record indicates that at least some regional extinc-
tion has occurred in Hydrophilini (Fikacek et al 2010) Four
genera of Hydrophilini have Eocene representatives that have
been found in the Palaearctic region and two have Eocene rep-
resentatives from the Nearctic region Although our biogeo-
graphical reconstructions are consistent with such
distributions in Hydrochara (Palaearctic) Hydrophilus (Nearc-
tic and Palaearctic) and Tropisternus (Nearctic) the lack of
present-day Palaearctic Hydrobiomorpha suggests regional
extinction Thus although the DEC+j model receives a much
better likelihood than the DEC model it might not entirely
capture the complexity of the evolutionary history in this
group The DEC model on the other hand recovers extinction
and range expansion as important forces driving the biogeo-
graphical evolution of hydrophiline water beetles It also
implies biologically intricate biogeographical processes such as
repeated long-distance dispersal and regional extinction which
might be obscured by a potential role of Antarctica in shaping
the biogeography of the group Despite the stronger statistical
support for the DEC+j model over the DEC model it is not
clear which model is the most appropriate in the case of
Hydrophilini biogeographical history Unfortunately it is not
presently possible to place the described fossils in the present
phylogenetic framework because there is not enough morpho-
logical support for the inclusion of these taxa beyond generic
assignments Therefore it will be important to revise the
inferred patterns in the light of denser taxon sampling and bet-
ter knowledge of the fossil record as these can partly obscure
macroevolutionary patterns (eg Meseguer et al 2015 Tous-
saint amp Condamine 2016)
Comparison with other West Gondwana vicariance
patterns
Our ancestral range estimation recovers with moderate sup-
port a West Gondwana vicariant pattern with a joint ancestral
distribution in these two regions A recent study on Sericini
chafers (Coleoptera Scarabaeidae) recovered a similar pattern
with the best biogeographical model estimating a vicariant
split consistent with the West Gondwana vicariance hypothe-
sis (WGVH) (Eberle et al 2017 Fig 4) Likewise Luebert
et al (2017) recovered a potential case of vicariance support-
ing the WGVH in Boraginales (Asterids) with the upper
bound of their age estimate slightly overlapping with the tim-
ing of West Gondwana break-up (Fig 4) Flowering plants of
the families Combretaceae (Rosids Myrtales) and Elatinaceae
CentroplacaceaeMalpighiaceae (Rosids Malpighiales) have
also been recently suggested as a potential example of West
Gondwana vicariance (Berger et al 2016 Cai et al 2016)
Some clades with exclusive sister relationships between
Afrotropical and Neotropical lineages have been suggested as
good candidates for the WGVH For example the divergence
of the freshwater fish sister genera Arapaima and Heterosis
(Teleostei Osteoglossiformes) respectively found in South
America and Africa was dated from the Cretaceous (Fig 4)
Although the dating analyses were somewhat contradictory
these osteoglossiform fishes are amongst the best candidates
for the WGVH (Lavoue 2016) Aciliine diving beetles
(Coleoptera Dytiscidae) have also been suggested as a candi-
date for WGVH (Fig 4) although the results of dating anal-
yses were inconsistent when based on either crown or stem
fossil placement (Bukontaite et al 2014) A more compelling
example is found in the gecko family Sphaerodactylidae in
which Gamble et al (2008) recovered as split between Mor-
occo and Neotropical geckoes in the Upper Cretaceous con-
sistent with the WGVH In caecilians the family
Dermophiidae endemic to South America has been resolved
as sister to Siphonopidae distributed on each side of the
Atlantic Ocean with Neotropical siphonopids being the most
derived clade in the family The dating of the split between
the two families has been somewhat controversial with esti-
mates largely spanning the Lower Cretaceous (Kamei et al
2012) and younger ones postdating the West Gondwana
break-up (Pyron 2014)
In contrast other studies focusing on clades with a well-
supported sister-group relationship between Africa and South
America have rejected the WGVH For instance Givnish
et al (2004) suggested a very recent Miocene divergence
between the AfricanSouth American disjunct lineages in
Bromeliaceae and Rapateaceae suggesting long-distance dis-
persal Likewise the divergence between the African wild
almond genus Brabejum and its sister genus Panopsis from
South America was dated from the Eocene (Barker et al
2007) therefore rejecting the hypothesis of a West Gond-
wanan signature Other examples of molecular divergence
time estimates that are irreconcilable with the WGVH are
also found in cichlid fishes (Matschiner et al 2017 but see
Lopez-Fernandez et al 2013) amphisbaenian worm lizards
(Longrich et al 2015) Leguminosae (Meng et al 2014)
and Sapotaceae (Bartish et al 2011)
Although we relied on a rather limited fraction of the total
diversity of hydrophiline water beetles we included most of
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
10
E F A Toussaint et al
Figure 4 Examples of clades supporting the West Gondwana vicariance hypothesis Overview of clades for which the West Gondwanavicariance hypothesis (WGVH) was suggested based on molecular dating andor model-based biogeographical estimationreconstruction
The divergence times for the focal nodes representing the split between Africa and South America are given for each clade as credibilityintervals Names with an asterisk indicate that in the selected study an alternative analysis did not support the WGVH For more details
on these alternative analyses please refer to the original publications The timeframe of West Gondwana (Africa and South America)breakup is indicated by a large grey rectangle and a representation of the two landmasses c 100 Ma according to the model of Seton
et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
11
Biogeography of Hydrophilini giant water scavenger beetles
the taxonomic and geographical diversity for each genus
Given that the missing taxa can be morphologically assigned
to sampled clades and more specifically that missing
Neotropical taxa are morphologically supported as members
of sampled Neotropical clades the possibility that our bio-
geographical estimation is biased by incomplete taxon sam-
pling is very unlikely The lack of an exclusive sister
relationship and the moderate relative probability for a sce-
nario supporting the WGVH suggest that a conservative view
of hydrophiline biogeographical history is prudent Future
empirical studies with denser taxon sampling will help to
confirm or revise this evolutionary pattern This study adds
to the scarce literature supporting the WGVH and is thus
important to our understanding of the relationship between
Gondwanan tectonic events and biogeographical evolution of
clades in the Cretaceous There is no doubt that the increas-
ing number of empirical studies using molecular dating and
model-based approaches will shed new light on the heated
debate between ancient vicariance and dispersalism
ACKNOWLEDGEMENTS
We would like to acknowledge the editors Mike Dawson and
Isabel Sanmartın as well as three anonymous reviewers for
constructive comments on earlier drafts of this paper We
thank the many colleagues that contributed tissues for this
study Kelly Miller Ignacio Ribera Michael Balke Robert
Sites Yusuke Minoshima Johannes Bergsten and Michael
Caterino Martin Fikacek provided material as well as critical
analysis of the fossil calibrations This study was funded in
part by a University of Kansas General Research Fund grant
to AEZS
REFERENCES
Andujar C Faille A Perez-Gonzalez S Zaballos JP
Vogler AP amp Ribera I (2016) Gondwanian relicts and
oceanic dispersal in a cosmopolitan radiation of euedaphic
ground beetles Molecular Phylogenetics and Evolution 99
235ndash246Barker NP Weston PH Rutschmann F amp Sauquet H
(2007) Molecular dating of the lsquoGondwananrsquo plant family
Proteaceae is only partially congruent with the timing of
the break-up of Gondwana Journal of Biogeography 34
2012ndash2027Bartish IV Antonelli A Richardson JE amp Swenson U
(2011) Vicariance or long-distance dispersal historical bio-
geography of the pantropical subfamily Chrysophylloideae
(Sapotaceae) Journal of Biogeography 38 177ndash190Beaulieu JM Tank DC amp Donoghue MJ (2013) A
Southern Hemisphere origin for campanulid angiosperms
with traces of the break-up of Gondwana BMC Evolution-
ary Biology 13 1
Berger BA Kriebel R Spalink D amp Sytsma KJ (2016)
Divergence times historical biogeography and shifts in
speciation rates of Myrtales Molecular Phylogenetics and
Evolution 95 116ndash136Bloom DD Fikacek M amp Short AEZ (2014) Clade age
and diversification rate variation explain disparity in spe-
cies richness among water scavenger beetle (Hydrophili-
dae) lineages PLoS ONE 9 e98430
Bukontaite R Miller KB amp Bergsten J (2014) The utility
of CAD in recovering Gondwanan vicariance events and
the evolutionary history of Aciliini (Coleoptera Dytisci-
dae) BMC Evolutionary Biology 14 5
Cai L Xi Z Peterson K Rushworth C Beaulieu J amp
Davis CC (2016) Phylogeny of Elatinaceae and the tropi-
cal Gondwanan origin of the Centroplacaceae (Malpighi-
aceae Elatinaceae) clade PLoS ONE 11 e0161881
Drummond AJ Suchard MA Xie D amp Rambaut A
(2012) Bayesian phylogenetics with BEAUti and the
BEAST 17 Molecular Biology and Evolution 29 1969ndash1973
Eberle J Fabrizi S Lago P amp Ahrens D (2017) A histori-
cal biogeography of megadiverse Sericinimdashanother story
ldquoout of Africardquo Cladistics in press doi 101111cla12162
Edgar RC (2004) MUSCLE multiple sequence alignment
with high accuracy and high throughput Nucleic Acids
Research 32 1792ndash1797Fikacek M Wedmann S amp Schmied H (2010) Diversifica-
tion of the greater hydrophilines clade of giant water scav-
enger beetles dated back to the Middle
Eocene (Coleoptera Hydrophilidae Hydrophilina) Inver-
tebrate Systematics 24 9ndash22Fikacek M Prokin A Yan E Yue Y Wang B Ren D
amp Beattie R (2014) Modern hydrophilid clades present
and widespread in the Late Jurassic and Early Cretaceous
(Coleoptera Hydrophiloidea Hydrophilidae) Zoological
Journal of the Linnean Society 170 710ndash734Gamble T Bauer AM Greenbaum E amp Jackman TR
(2008) Evidence for Gondwanan vicariance in an ancient
clade of gecko lizards Journal of Biogeography 35 88ndash104Gibbons AD Whittaker JM amp Meurouller RD (2013) The
breakup of East Gondwana assimilating constraints from
Cretaceous ocean basins around India into a best-fit tec-
tonic model Journal of Geophysical Research Solid Earth
118 808ndash822Givnish TJ Millam KC Evans TM Hall JC Pires
JC Berry PE amp Sytsma KJ (2004) Ancient vicariance
or recent long-distance dispersal Inferences about phy-
logeny and South American-African disjunctions in Rap-
ateaceae and Bromeliaceae based on ndhF sequence data
International Journal of Plant Sciences 165 S35ndashS54Hansen M (1999) World catalogue of insects Volume 2
Hydrophiloidea (s str) (Coleoptera) Apollo Books Sten-
strup Denmark
Kamei RG San Mauro D Gower DJ Van Bocxlaer I
Sherratt E Thomas A Babu S Bossuyt F Wilkinson
M amp Biju SD (2012) Discovery of a new family of
amphibians from northeast India with ancient links to
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
12
E F A Toussaint et al
Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
9
Biogeography of Hydrophilini giant water scavenger beetles
compare results from the two methods here The founder-
event jump dispersal parameter j has been proven to be par-
ticularly relevant in island systems (Matzke 2014) where it
often significantly improves the likelihood of the model
However it is not entirely clear if or how this parameter is
relevant in continental island-like settings and more impor-
tantly in non-island-like continental settings In Hydrophi-
lini the j parameter is the main factor explaining the
biogeographical history of the group whereas the role of
extinction and range expansion is much reduced (see
Results) Considering the inferred negligible value of the
extinction parameter e in DEC+j it seems difficult to invoke
range expansion followed by extinction in hydrophilines In
contrast in the DEC model extinction and range expansion
play a crucial role as illustrated by the complex biogeo-
graphical scenario inferred (Fig 3 see Appendix S3) Indeed
most range expansion and vicariant events inferred by the
DEC model are difficult to reconciliate with the arrangement
of landmasses at the time without invoking regional
extinction
The fossil record indicates that at least some regional extinc-
tion has occurred in Hydrophilini (Fikacek et al 2010) Four
genera of Hydrophilini have Eocene representatives that have
been found in the Palaearctic region and two have Eocene rep-
resentatives from the Nearctic region Although our biogeo-
graphical reconstructions are consistent with such
distributions in Hydrochara (Palaearctic) Hydrophilus (Nearc-
tic and Palaearctic) and Tropisternus (Nearctic) the lack of
present-day Palaearctic Hydrobiomorpha suggests regional
extinction Thus although the DEC+j model receives a much
better likelihood than the DEC model it might not entirely
capture the complexity of the evolutionary history in this
group The DEC model on the other hand recovers extinction
and range expansion as important forces driving the biogeo-
graphical evolution of hydrophiline water beetles It also
implies biologically intricate biogeographical processes such as
repeated long-distance dispersal and regional extinction which
might be obscured by a potential role of Antarctica in shaping
the biogeography of the group Despite the stronger statistical
support for the DEC+j model over the DEC model it is not
clear which model is the most appropriate in the case of
Hydrophilini biogeographical history Unfortunately it is not
presently possible to place the described fossils in the present
phylogenetic framework because there is not enough morpho-
logical support for the inclusion of these taxa beyond generic
assignments Therefore it will be important to revise the
inferred patterns in the light of denser taxon sampling and bet-
ter knowledge of the fossil record as these can partly obscure
macroevolutionary patterns (eg Meseguer et al 2015 Tous-
saint amp Condamine 2016)
Comparison with other West Gondwana vicariance
patterns
Our ancestral range estimation recovers with moderate sup-
port a West Gondwana vicariant pattern with a joint ancestral
distribution in these two regions A recent study on Sericini
chafers (Coleoptera Scarabaeidae) recovered a similar pattern
with the best biogeographical model estimating a vicariant
split consistent with the West Gondwana vicariance hypothe-
sis (WGVH) (Eberle et al 2017 Fig 4) Likewise Luebert
et al (2017) recovered a potential case of vicariance support-
ing the WGVH in Boraginales (Asterids) with the upper
bound of their age estimate slightly overlapping with the tim-
ing of West Gondwana break-up (Fig 4) Flowering plants of
the families Combretaceae (Rosids Myrtales) and Elatinaceae
CentroplacaceaeMalpighiaceae (Rosids Malpighiales) have
also been recently suggested as a potential example of West
Gondwana vicariance (Berger et al 2016 Cai et al 2016)
Some clades with exclusive sister relationships between
Afrotropical and Neotropical lineages have been suggested as
good candidates for the WGVH For example the divergence
of the freshwater fish sister genera Arapaima and Heterosis
(Teleostei Osteoglossiformes) respectively found in South
America and Africa was dated from the Cretaceous (Fig 4)
Although the dating analyses were somewhat contradictory
these osteoglossiform fishes are amongst the best candidates
for the WGVH (Lavoue 2016) Aciliine diving beetles
(Coleoptera Dytiscidae) have also been suggested as a candi-
date for WGVH (Fig 4) although the results of dating anal-
yses were inconsistent when based on either crown or stem
fossil placement (Bukontaite et al 2014) A more compelling
example is found in the gecko family Sphaerodactylidae in
which Gamble et al (2008) recovered as split between Mor-
occo and Neotropical geckoes in the Upper Cretaceous con-
sistent with the WGVH In caecilians the family
Dermophiidae endemic to South America has been resolved
as sister to Siphonopidae distributed on each side of the
Atlantic Ocean with Neotropical siphonopids being the most
derived clade in the family The dating of the split between
the two families has been somewhat controversial with esti-
mates largely spanning the Lower Cretaceous (Kamei et al
2012) and younger ones postdating the West Gondwana
break-up (Pyron 2014)
In contrast other studies focusing on clades with a well-
supported sister-group relationship between Africa and South
America have rejected the WGVH For instance Givnish
et al (2004) suggested a very recent Miocene divergence
between the AfricanSouth American disjunct lineages in
Bromeliaceae and Rapateaceae suggesting long-distance dis-
persal Likewise the divergence between the African wild
almond genus Brabejum and its sister genus Panopsis from
South America was dated from the Eocene (Barker et al
2007) therefore rejecting the hypothesis of a West Gond-
wanan signature Other examples of molecular divergence
time estimates that are irreconcilable with the WGVH are
also found in cichlid fishes (Matschiner et al 2017 but see
Lopez-Fernandez et al 2013) amphisbaenian worm lizards
(Longrich et al 2015) Leguminosae (Meng et al 2014)
and Sapotaceae (Bartish et al 2011)
Although we relied on a rather limited fraction of the total
diversity of hydrophiline water beetles we included most of
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
10
E F A Toussaint et al
Figure 4 Examples of clades supporting the West Gondwana vicariance hypothesis Overview of clades for which the West Gondwanavicariance hypothesis (WGVH) was suggested based on molecular dating andor model-based biogeographical estimationreconstruction
The divergence times for the focal nodes representing the split between Africa and South America are given for each clade as credibilityintervals Names with an asterisk indicate that in the selected study an alternative analysis did not support the WGVH For more details
on these alternative analyses please refer to the original publications The timeframe of West Gondwana (Africa and South America)breakup is indicated by a large grey rectangle and a representation of the two landmasses c 100 Ma according to the model of Seton
et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
11
Biogeography of Hydrophilini giant water scavenger beetles
the taxonomic and geographical diversity for each genus
Given that the missing taxa can be morphologically assigned
to sampled clades and more specifically that missing
Neotropical taxa are morphologically supported as members
of sampled Neotropical clades the possibility that our bio-
geographical estimation is biased by incomplete taxon sam-
pling is very unlikely The lack of an exclusive sister
relationship and the moderate relative probability for a sce-
nario supporting the WGVH suggest that a conservative view
of hydrophiline biogeographical history is prudent Future
empirical studies with denser taxon sampling will help to
confirm or revise this evolutionary pattern This study adds
to the scarce literature supporting the WGVH and is thus
important to our understanding of the relationship between
Gondwanan tectonic events and biogeographical evolution of
clades in the Cretaceous There is no doubt that the increas-
ing number of empirical studies using molecular dating and
model-based approaches will shed new light on the heated
debate between ancient vicariance and dispersalism
ACKNOWLEDGEMENTS
We would like to acknowledge the editors Mike Dawson and
Isabel Sanmartın as well as three anonymous reviewers for
constructive comments on earlier drafts of this paper We
thank the many colleagues that contributed tissues for this
study Kelly Miller Ignacio Ribera Michael Balke Robert
Sites Yusuke Minoshima Johannes Bergsten and Michael
Caterino Martin Fikacek provided material as well as critical
analysis of the fossil calibrations This study was funded in
part by a University of Kansas General Research Fund grant
to AEZS
REFERENCES
Andujar C Faille A Perez-Gonzalez S Zaballos JP
Vogler AP amp Ribera I (2016) Gondwanian relicts and
oceanic dispersal in a cosmopolitan radiation of euedaphic
ground beetles Molecular Phylogenetics and Evolution 99
235ndash246Barker NP Weston PH Rutschmann F amp Sauquet H
(2007) Molecular dating of the lsquoGondwananrsquo plant family
Proteaceae is only partially congruent with the timing of
the break-up of Gondwana Journal of Biogeography 34
2012ndash2027Bartish IV Antonelli A Richardson JE amp Swenson U
(2011) Vicariance or long-distance dispersal historical bio-
geography of the pantropical subfamily Chrysophylloideae
(Sapotaceae) Journal of Biogeography 38 177ndash190Beaulieu JM Tank DC amp Donoghue MJ (2013) A
Southern Hemisphere origin for campanulid angiosperms
with traces of the break-up of Gondwana BMC Evolution-
ary Biology 13 1
Berger BA Kriebel R Spalink D amp Sytsma KJ (2016)
Divergence times historical biogeography and shifts in
speciation rates of Myrtales Molecular Phylogenetics and
Evolution 95 116ndash136Bloom DD Fikacek M amp Short AEZ (2014) Clade age
and diversification rate variation explain disparity in spe-
cies richness among water scavenger beetle (Hydrophili-
dae) lineages PLoS ONE 9 e98430
Bukontaite R Miller KB amp Bergsten J (2014) The utility
of CAD in recovering Gondwanan vicariance events and
the evolutionary history of Aciliini (Coleoptera Dytisci-
dae) BMC Evolutionary Biology 14 5
Cai L Xi Z Peterson K Rushworth C Beaulieu J amp
Davis CC (2016) Phylogeny of Elatinaceae and the tropi-
cal Gondwanan origin of the Centroplacaceae (Malpighi-
aceae Elatinaceae) clade PLoS ONE 11 e0161881
Drummond AJ Suchard MA Xie D amp Rambaut A
(2012) Bayesian phylogenetics with BEAUti and the
BEAST 17 Molecular Biology and Evolution 29 1969ndash1973
Eberle J Fabrizi S Lago P amp Ahrens D (2017) A histori-
cal biogeography of megadiverse Sericinimdashanother story
ldquoout of Africardquo Cladistics in press doi 101111cla12162
Edgar RC (2004) MUSCLE multiple sequence alignment
with high accuracy and high throughput Nucleic Acids
Research 32 1792ndash1797Fikacek M Wedmann S amp Schmied H (2010) Diversifica-
tion of the greater hydrophilines clade of giant water scav-
enger beetles dated back to the Middle
Eocene (Coleoptera Hydrophilidae Hydrophilina) Inver-
tebrate Systematics 24 9ndash22Fikacek M Prokin A Yan E Yue Y Wang B Ren D
amp Beattie R (2014) Modern hydrophilid clades present
and widespread in the Late Jurassic and Early Cretaceous
(Coleoptera Hydrophiloidea Hydrophilidae) Zoological
Journal of the Linnean Society 170 710ndash734Gamble T Bauer AM Greenbaum E amp Jackman TR
(2008) Evidence for Gondwanan vicariance in an ancient
clade of gecko lizards Journal of Biogeography 35 88ndash104Gibbons AD Whittaker JM amp Meurouller RD (2013) The
breakup of East Gondwana assimilating constraints from
Cretaceous ocean basins around India into a best-fit tec-
tonic model Journal of Geophysical Research Solid Earth
118 808ndash822Givnish TJ Millam KC Evans TM Hall JC Pires
JC Berry PE amp Sytsma KJ (2004) Ancient vicariance
or recent long-distance dispersal Inferences about phy-
logeny and South American-African disjunctions in Rap-
ateaceae and Bromeliaceae based on ndhF sequence data
International Journal of Plant Sciences 165 S35ndashS54Hansen M (1999) World catalogue of insects Volume 2
Hydrophiloidea (s str) (Coleoptera) Apollo Books Sten-
strup Denmark
Kamei RG San Mauro D Gower DJ Van Bocxlaer I
Sherratt E Thomas A Babu S Bossuyt F Wilkinson
M amp Biju SD (2012) Discovery of a new family of
amphibians from northeast India with ancient links to
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
12
E F A Toussaint et al
Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
compare results from the two methods here The founder-
event jump dispersal parameter j has been proven to be par-
ticularly relevant in island systems (Matzke 2014) where it
often significantly improves the likelihood of the model
However it is not entirely clear if or how this parameter is
relevant in continental island-like settings and more impor-
tantly in non-island-like continental settings In Hydrophi-
lini the j parameter is the main factor explaining the
biogeographical history of the group whereas the role of
extinction and range expansion is much reduced (see
Results) Considering the inferred negligible value of the
extinction parameter e in DEC+j it seems difficult to invoke
range expansion followed by extinction in hydrophilines In
contrast in the DEC model extinction and range expansion
play a crucial role as illustrated by the complex biogeo-
graphical scenario inferred (Fig 3 see Appendix S3) Indeed
most range expansion and vicariant events inferred by the
DEC model are difficult to reconciliate with the arrangement
of landmasses at the time without invoking regional
extinction
The fossil record indicates that at least some regional extinc-
tion has occurred in Hydrophilini (Fikacek et al 2010) Four
genera of Hydrophilini have Eocene representatives that have
been found in the Palaearctic region and two have Eocene rep-
resentatives from the Nearctic region Although our biogeo-
graphical reconstructions are consistent with such
distributions in Hydrochara (Palaearctic) Hydrophilus (Nearc-
tic and Palaearctic) and Tropisternus (Nearctic) the lack of
present-day Palaearctic Hydrobiomorpha suggests regional
extinction Thus although the DEC+j model receives a much
better likelihood than the DEC model it might not entirely
capture the complexity of the evolutionary history in this
group The DEC model on the other hand recovers extinction
and range expansion as important forces driving the biogeo-
graphical evolution of hydrophiline water beetles It also
implies biologically intricate biogeographical processes such as
repeated long-distance dispersal and regional extinction which
might be obscured by a potential role of Antarctica in shaping
the biogeography of the group Despite the stronger statistical
support for the DEC+j model over the DEC model it is not
clear which model is the most appropriate in the case of
Hydrophilini biogeographical history Unfortunately it is not
presently possible to place the described fossils in the present
phylogenetic framework because there is not enough morpho-
logical support for the inclusion of these taxa beyond generic
assignments Therefore it will be important to revise the
inferred patterns in the light of denser taxon sampling and bet-
ter knowledge of the fossil record as these can partly obscure
macroevolutionary patterns (eg Meseguer et al 2015 Tous-
saint amp Condamine 2016)
Comparison with other West Gondwana vicariance
patterns
Our ancestral range estimation recovers with moderate sup-
port a West Gondwana vicariant pattern with a joint ancestral
distribution in these two regions A recent study on Sericini
chafers (Coleoptera Scarabaeidae) recovered a similar pattern
with the best biogeographical model estimating a vicariant
split consistent with the West Gondwana vicariance hypothe-
sis (WGVH) (Eberle et al 2017 Fig 4) Likewise Luebert
et al (2017) recovered a potential case of vicariance support-
ing the WGVH in Boraginales (Asterids) with the upper
bound of their age estimate slightly overlapping with the tim-
ing of West Gondwana break-up (Fig 4) Flowering plants of
the families Combretaceae (Rosids Myrtales) and Elatinaceae
CentroplacaceaeMalpighiaceae (Rosids Malpighiales) have
also been recently suggested as a potential example of West
Gondwana vicariance (Berger et al 2016 Cai et al 2016)
Some clades with exclusive sister relationships between
Afrotropical and Neotropical lineages have been suggested as
good candidates for the WGVH For example the divergence
of the freshwater fish sister genera Arapaima and Heterosis
(Teleostei Osteoglossiformes) respectively found in South
America and Africa was dated from the Cretaceous (Fig 4)
Although the dating analyses were somewhat contradictory
these osteoglossiform fishes are amongst the best candidates
for the WGVH (Lavoue 2016) Aciliine diving beetles
(Coleoptera Dytiscidae) have also been suggested as a candi-
date for WGVH (Fig 4) although the results of dating anal-
yses were inconsistent when based on either crown or stem
fossil placement (Bukontaite et al 2014) A more compelling
example is found in the gecko family Sphaerodactylidae in
which Gamble et al (2008) recovered as split between Mor-
occo and Neotropical geckoes in the Upper Cretaceous con-
sistent with the WGVH In caecilians the family
Dermophiidae endemic to South America has been resolved
as sister to Siphonopidae distributed on each side of the
Atlantic Ocean with Neotropical siphonopids being the most
derived clade in the family The dating of the split between
the two families has been somewhat controversial with esti-
mates largely spanning the Lower Cretaceous (Kamei et al
2012) and younger ones postdating the West Gondwana
break-up (Pyron 2014)
In contrast other studies focusing on clades with a well-
supported sister-group relationship between Africa and South
America have rejected the WGVH For instance Givnish
et al (2004) suggested a very recent Miocene divergence
between the AfricanSouth American disjunct lineages in
Bromeliaceae and Rapateaceae suggesting long-distance dis-
persal Likewise the divergence between the African wild
almond genus Brabejum and its sister genus Panopsis from
South America was dated from the Eocene (Barker et al
2007) therefore rejecting the hypothesis of a West Gond-
wanan signature Other examples of molecular divergence
time estimates that are irreconcilable with the WGVH are
also found in cichlid fishes (Matschiner et al 2017 but see
Lopez-Fernandez et al 2013) amphisbaenian worm lizards
(Longrich et al 2015) Leguminosae (Meng et al 2014)
and Sapotaceae (Bartish et al 2011)
Although we relied on a rather limited fraction of the total
diversity of hydrophiline water beetles we included most of
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
10
E F A Toussaint et al
Figure 4 Examples of clades supporting the West Gondwana vicariance hypothesis Overview of clades for which the West Gondwanavicariance hypothesis (WGVH) was suggested based on molecular dating andor model-based biogeographical estimationreconstruction
The divergence times for the focal nodes representing the split between Africa and South America are given for each clade as credibilityintervals Names with an asterisk indicate that in the selected study an alternative analysis did not support the WGVH For more details
on these alternative analyses please refer to the original publications The timeframe of West Gondwana (Africa and South America)breakup is indicated by a large grey rectangle and a representation of the two landmasses c 100 Ma according to the model of Seton
et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
11
Biogeography of Hydrophilini giant water scavenger beetles
the taxonomic and geographical diversity for each genus
Given that the missing taxa can be morphologically assigned
to sampled clades and more specifically that missing
Neotropical taxa are morphologically supported as members
of sampled Neotropical clades the possibility that our bio-
geographical estimation is biased by incomplete taxon sam-
pling is very unlikely The lack of an exclusive sister
relationship and the moderate relative probability for a sce-
nario supporting the WGVH suggest that a conservative view
of hydrophiline biogeographical history is prudent Future
empirical studies with denser taxon sampling will help to
confirm or revise this evolutionary pattern This study adds
to the scarce literature supporting the WGVH and is thus
important to our understanding of the relationship between
Gondwanan tectonic events and biogeographical evolution of
clades in the Cretaceous There is no doubt that the increas-
ing number of empirical studies using molecular dating and
model-based approaches will shed new light on the heated
debate between ancient vicariance and dispersalism
ACKNOWLEDGEMENTS
We would like to acknowledge the editors Mike Dawson and
Isabel Sanmartın as well as three anonymous reviewers for
constructive comments on earlier drafts of this paper We
thank the many colleagues that contributed tissues for this
study Kelly Miller Ignacio Ribera Michael Balke Robert
Sites Yusuke Minoshima Johannes Bergsten and Michael
Caterino Martin Fikacek provided material as well as critical
analysis of the fossil calibrations This study was funded in
part by a University of Kansas General Research Fund grant
to AEZS
REFERENCES
Andujar C Faille A Perez-Gonzalez S Zaballos JP
Vogler AP amp Ribera I (2016) Gondwanian relicts and
oceanic dispersal in a cosmopolitan radiation of euedaphic
ground beetles Molecular Phylogenetics and Evolution 99
235ndash246Barker NP Weston PH Rutschmann F amp Sauquet H
(2007) Molecular dating of the lsquoGondwananrsquo plant family
Proteaceae is only partially congruent with the timing of
the break-up of Gondwana Journal of Biogeography 34
2012ndash2027Bartish IV Antonelli A Richardson JE amp Swenson U
(2011) Vicariance or long-distance dispersal historical bio-
geography of the pantropical subfamily Chrysophylloideae
(Sapotaceae) Journal of Biogeography 38 177ndash190Beaulieu JM Tank DC amp Donoghue MJ (2013) A
Southern Hemisphere origin for campanulid angiosperms
with traces of the break-up of Gondwana BMC Evolution-
ary Biology 13 1
Berger BA Kriebel R Spalink D amp Sytsma KJ (2016)
Divergence times historical biogeography and shifts in
speciation rates of Myrtales Molecular Phylogenetics and
Evolution 95 116ndash136Bloom DD Fikacek M amp Short AEZ (2014) Clade age
and diversification rate variation explain disparity in spe-
cies richness among water scavenger beetle (Hydrophili-
dae) lineages PLoS ONE 9 e98430
Bukontaite R Miller KB amp Bergsten J (2014) The utility
of CAD in recovering Gondwanan vicariance events and
the evolutionary history of Aciliini (Coleoptera Dytisci-
dae) BMC Evolutionary Biology 14 5
Cai L Xi Z Peterson K Rushworth C Beaulieu J amp
Davis CC (2016) Phylogeny of Elatinaceae and the tropi-
cal Gondwanan origin of the Centroplacaceae (Malpighi-
aceae Elatinaceae) clade PLoS ONE 11 e0161881
Drummond AJ Suchard MA Xie D amp Rambaut A
(2012) Bayesian phylogenetics with BEAUti and the
BEAST 17 Molecular Biology and Evolution 29 1969ndash1973
Eberle J Fabrizi S Lago P amp Ahrens D (2017) A histori-
cal biogeography of megadiverse Sericinimdashanother story
ldquoout of Africardquo Cladistics in press doi 101111cla12162
Edgar RC (2004) MUSCLE multiple sequence alignment
with high accuracy and high throughput Nucleic Acids
Research 32 1792ndash1797Fikacek M Wedmann S amp Schmied H (2010) Diversifica-
tion of the greater hydrophilines clade of giant water scav-
enger beetles dated back to the Middle
Eocene (Coleoptera Hydrophilidae Hydrophilina) Inver-
tebrate Systematics 24 9ndash22Fikacek M Prokin A Yan E Yue Y Wang B Ren D
amp Beattie R (2014) Modern hydrophilid clades present
and widespread in the Late Jurassic and Early Cretaceous
(Coleoptera Hydrophiloidea Hydrophilidae) Zoological
Journal of the Linnean Society 170 710ndash734Gamble T Bauer AM Greenbaum E amp Jackman TR
(2008) Evidence for Gondwanan vicariance in an ancient
clade of gecko lizards Journal of Biogeography 35 88ndash104Gibbons AD Whittaker JM amp Meurouller RD (2013) The
breakup of East Gondwana assimilating constraints from
Cretaceous ocean basins around India into a best-fit tec-
tonic model Journal of Geophysical Research Solid Earth
118 808ndash822Givnish TJ Millam KC Evans TM Hall JC Pires
JC Berry PE amp Sytsma KJ (2004) Ancient vicariance
or recent long-distance dispersal Inferences about phy-
logeny and South American-African disjunctions in Rap-
ateaceae and Bromeliaceae based on ndhF sequence data
International Journal of Plant Sciences 165 S35ndashS54Hansen M (1999) World catalogue of insects Volume 2
Hydrophiloidea (s str) (Coleoptera) Apollo Books Sten-
strup Denmark
Kamei RG San Mauro D Gower DJ Van Bocxlaer I
Sherratt E Thomas A Babu S Bossuyt F Wilkinson
M amp Biju SD (2012) Discovery of a new family of
amphibians from northeast India with ancient links to
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
12
E F A Toussaint et al
Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
Figure 4 Examples of clades supporting the West Gondwana vicariance hypothesis Overview of clades for which the West Gondwanavicariance hypothesis (WGVH) was suggested based on molecular dating andor model-based biogeographical estimationreconstruction
The divergence times for the focal nodes representing the split between Africa and South America are given for each clade as credibilityintervals Names with an asterisk indicate that in the selected study an alternative analysis did not support the WGVH For more details
on these alternative analyses please refer to the original publications The timeframe of West Gondwana (Africa and South America)breakup is indicated by a large grey rectangle and a representation of the two landmasses c 100 Ma according to the model of Seton
et al (2012)
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
11
Biogeography of Hydrophilini giant water scavenger beetles
the taxonomic and geographical diversity for each genus
Given that the missing taxa can be morphologically assigned
to sampled clades and more specifically that missing
Neotropical taxa are morphologically supported as members
of sampled Neotropical clades the possibility that our bio-
geographical estimation is biased by incomplete taxon sam-
pling is very unlikely The lack of an exclusive sister
relationship and the moderate relative probability for a sce-
nario supporting the WGVH suggest that a conservative view
of hydrophiline biogeographical history is prudent Future
empirical studies with denser taxon sampling will help to
confirm or revise this evolutionary pattern This study adds
to the scarce literature supporting the WGVH and is thus
important to our understanding of the relationship between
Gondwanan tectonic events and biogeographical evolution of
clades in the Cretaceous There is no doubt that the increas-
ing number of empirical studies using molecular dating and
model-based approaches will shed new light on the heated
debate between ancient vicariance and dispersalism
ACKNOWLEDGEMENTS
We would like to acknowledge the editors Mike Dawson and
Isabel Sanmartın as well as three anonymous reviewers for
constructive comments on earlier drafts of this paper We
thank the many colleagues that contributed tissues for this
study Kelly Miller Ignacio Ribera Michael Balke Robert
Sites Yusuke Minoshima Johannes Bergsten and Michael
Caterino Martin Fikacek provided material as well as critical
analysis of the fossil calibrations This study was funded in
part by a University of Kansas General Research Fund grant
to AEZS
REFERENCES
Andujar C Faille A Perez-Gonzalez S Zaballos JP
Vogler AP amp Ribera I (2016) Gondwanian relicts and
oceanic dispersal in a cosmopolitan radiation of euedaphic
ground beetles Molecular Phylogenetics and Evolution 99
235ndash246Barker NP Weston PH Rutschmann F amp Sauquet H
(2007) Molecular dating of the lsquoGondwananrsquo plant family
Proteaceae is only partially congruent with the timing of
the break-up of Gondwana Journal of Biogeography 34
2012ndash2027Bartish IV Antonelli A Richardson JE amp Swenson U
(2011) Vicariance or long-distance dispersal historical bio-
geography of the pantropical subfamily Chrysophylloideae
(Sapotaceae) Journal of Biogeography 38 177ndash190Beaulieu JM Tank DC amp Donoghue MJ (2013) A
Southern Hemisphere origin for campanulid angiosperms
with traces of the break-up of Gondwana BMC Evolution-
ary Biology 13 1
Berger BA Kriebel R Spalink D amp Sytsma KJ (2016)
Divergence times historical biogeography and shifts in
speciation rates of Myrtales Molecular Phylogenetics and
Evolution 95 116ndash136Bloom DD Fikacek M amp Short AEZ (2014) Clade age
and diversification rate variation explain disparity in spe-
cies richness among water scavenger beetle (Hydrophili-
dae) lineages PLoS ONE 9 e98430
Bukontaite R Miller KB amp Bergsten J (2014) The utility
of CAD in recovering Gondwanan vicariance events and
the evolutionary history of Aciliini (Coleoptera Dytisci-
dae) BMC Evolutionary Biology 14 5
Cai L Xi Z Peterson K Rushworth C Beaulieu J amp
Davis CC (2016) Phylogeny of Elatinaceae and the tropi-
cal Gondwanan origin of the Centroplacaceae (Malpighi-
aceae Elatinaceae) clade PLoS ONE 11 e0161881
Drummond AJ Suchard MA Xie D amp Rambaut A
(2012) Bayesian phylogenetics with BEAUti and the
BEAST 17 Molecular Biology and Evolution 29 1969ndash1973
Eberle J Fabrizi S Lago P amp Ahrens D (2017) A histori-
cal biogeography of megadiverse Sericinimdashanother story
ldquoout of Africardquo Cladistics in press doi 101111cla12162
Edgar RC (2004) MUSCLE multiple sequence alignment
with high accuracy and high throughput Nucleic Acids
Research 32 1792ndash1797Fikacek M Wedmann S amp Schmied H (2010) Diversifica-
tion of the greater hydrophilines clade of giant water scav-
enger beetles dated back to the Middle
Eocene (Coleoptera Hydrophilidae Hydrophilina) Inver-
tebrate Systematics 24 9ndash22Fikacek M Prokin A Yan E Yue Y Wang B Ren D
amp Beattie R (2014) Modern hydrophilid clades present
and widespread in the Late Jurassic and Early Cretaceous
(Coleoptera Hydrophiloidea Hydrophilidae) Zoological
Journal of the Linnean Society 170 710ndash734Gamble T Bauer AM Greenbaum E amp Jackman TR
(2008) Evidence for Gondwanan vicariance in an ancient
clade of gecko lizards Journal of Biogeography 35 88ndash104Gibbons AD Whittaker JM amp Meurouller RD (2013) The
breakup of East Gondwana assimilating constraints from
Cretaceous ocean basins around India into a best-fit tec-
tonic model Journal of Geophysical Research Solid Earth
118 808ndash822Givnish TJ Millam KC Evans TM Hall JC Pires
JC Berry PE amp Sytsma KJ (2004) Ancient vicariance
or recent long-distance dispersal Inferences about phy-
logeny and South American-African disjunctions in Rap-
ateaceae and Bromeliaceae based on ndhF sequence data
International Journal of Plant Sciences 165 S35ndashS54Hansen M (1999) World catalogue of insects Volume 2
Hydrophiloidea (s str) (Coleoptera) Apollo Books Sten-
strup Denmark
Kamei RG San Mauro D Gower DJ Van Bocxlaer I
Sherratt E Thomas A Babu S Bossuyt F Wilkinson
M amp Biju SD (2012) Discovery of a new family of
amphibians from northeast India with ancient links to
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
12
E F A Toussaint et al
Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
the taxonomic and geographical diversity for each genus
Given that the missing taxa can be morphologically assigned
to sampled clades and more specifically that missing
Neotropical taxa are morphologically supported as members
of sampled Neotropical clades the possibility that our bio-
geographical estimation is biased by incomplete taxon sam-
pling is very unlikely The lack of an exclusive sister
relationship and the moderate relative probability for a sce-
nario supporting the WGVH suggest that a conservative view
of hydrophiline biogeographical history is prudent Future
empirical studies with denser taxon sampling will help to
confirm or revise this evolutionary pattern This study adds
to the scarce literature supporting the WGVH and is thus
important to our understanding of the relationship between
Gondwanan tectonic events and biogeographical evolution of
clades in the Cretaceous There is no doubt that the increas-
ing number of empirical studies using molecular dating and
model-based approaches will shed new light on the heated
debate between ancient vicariance and dispersalism
ACKNOWLEDGEMENTS
We would like to acknowledge the editors Mike Dawson and
Isabel Sanmartın as well as three anonymous reviewers for
constructive comments on earlier drafts of this paper We
thank the many colleagues that contributed tissues for this
study Kelly Miller Ignacio Ribera Michael Balke Robert
Sites Yusuke Minoshima Johannes Bergsten and Michael
Caterino Martin Fikacek provided material as well as critical
analysis of the fossil calibrations This study was funded in
part by a University of Kansas General Research Fund grant
to AEZS
REFERENCES
Andujar C Faille A Perez-Gonzalez S Zaballos JP
Vogler AP amp Ribera I (2016) Gondwanian relicts and
oceanic dispersal in a cosmopolitan radiation of euedaphic
ground beetles Molecular Phylogenetics and Evolution 99
235ndash246Barker NP Weston PH Rutschmann F amp Sauquet H
(2007) Molecular dating of the lsquoGondwananrsquo plant family
Proteaceae is only partially congruent with the timing of
the break-up of Gondwana Journal of Biogeography 34
2012ndash2027Bartish IV Antonelli A Richardson JE amp Swenson U
(2011) Vicariance or long-distance dispersal historical bio-
geography of the pantropical subfamily Chrysophylloideae
(Sapotaceae) Journal of Biogeography 38 177ndash190Beaulieu JM Tank DC amp Donoghue MJ (2013) A
Southern Hemisphere origin for campanulid angiosperms
with traces of the break-up of Gondwana BMC Evolution-
ary Biology 13 1
Berger BA Kriebel R Spalink D amp Sytsma KJ (2016)
Divergence times historical biogeography and shifts in
speciation rates of Myrtales Molecular Phylogenetics and
Evolution 95 116ndash136Bloom DD Fikacek M amp Short AEZ (2014) Clade age
and diversification rate variation explain disparity in spe-
cies richness among water scavenger beetle (Hydrophili-
dae) lineages PLoS ONE 9 e98430
Bukontaite R Miller KB amp Bergsten J (2014) The utility
of CAD in recovering Gondwanan vicariance events and
the evolutionary history of Aciliini (Coleoptera Dytisci-
dae) BMC Evolutionary Biology 14 5
Cai L Xi Z Peterson K Rushworth C Beaulieu J amp
Davis CC (2016) Phylogeny of Elatinaceae and the tropi-
cal Gondwanan origin of the Centroplacaceae (Malpighi-
aceae Elatinaceae) clade PLoS ONE 11 e0161881
Drummond AJ Suchard MA Xie D amp Rambaut A
(2012) Bayesian phylogenetics with BEAUti and the
BEAST 17 Molecular Biology and Evolution 29 1969ndash1973
Eberle J Fabrizi S Lago P amp Ahrens D (2017) A histori-
cal biogeography of megadiverse Sericinimdashanother story
ldquoout of Africardquo Cladistics in press doi 101111cla12162
Edgar RC (2004) MUSCLE multiple sequence alignment
with high accuracy and high throughput Nucleic Acids
Research 32 1792ndash1797Fikacek M Wedmann S amp Schmied H (2010) Diversifica-
tion of the greater hydrophilines clade of giant water scav-
enger beetles dated back to the Middle
Eocene (Coleoptera Hydrophilidae Hydrophilina) Inver-
tebrate Systematics 24 9ndash22Fikacek M Prokin A Yan E Yue Y Wang B Ren D
amp Beattie R (2014) Modern hydrophilid clades present
and widespread in the Late Jurassic and Early Cretaceous
(Coleoptera Hydrophiloidea Hydrophilidae) Zoological
Journal of the Linnean Society 170 710ndash734Gamble T Bauer AM Greenbaum E amp Jackman TR
(2008) Evidence for Gondwanan vicariance in an ancient
clade of gecko lizards Journal of Biogeography 35 88ndash104Gibbons AD Whittaker JM amp Meurouller RD (2013) The
breakup of East Gondwana assimilating constraints from
Cretaceous ocean basins around India into a best-fit tec-
tonic model Journal of Geophysical Research Solid Earth
118 808ndash822Givnish TJ Millam KC Evans TM Hall JC Pires
JC Berry PE amp Sytsma KJ (2004) Ancient vicariance
or recent long-distance dispersal Inferences about phy-
logeny and South American-African disjunctions in Rap-
ateaceae and Bromeliaceae based on ndhF sequence data
International Journal of Plant Sciences 165 S35ndashS54Hansen M (1999) World catalogue of insects Volume 2
Hydrophiloidea (s str) (Coleoptera) Apollo Books Sten-
strup Denmark
Kamei RG San Mauro D Gower DJ Van Bocxlaer I
Sherratt E Thomas A Babu S Bossuyt F Wilkinson
M amp Biju SD (2012) Discovery of a new family of
amphibians from northeast India with ancient links to
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
12
E F A Toussaint et al
Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
Africa Proceedings of the Royal Society B Biological
Sciences 279 2396ndash2401Kass RE amp Raftery AE (1995) Bayes factors Journal of the
American Statistical Association 90 773ndash795Kim SI amp Farrell BD (2015) Phylogeny of world stag bee-
tles (Coleoptera Lucanidae) reveals a Gondwanan origin
of Darwinrsquos stag beetle Molecular Phylogenetics and Evolu-
tion 86 35ndash48Lanfear R Calcott B Ho SY amp Guindon S (2012) Parti-
tionFinder combined selection of partitioning schemes
and substitution models for phylogenetic analyses Molecu-
lar Biology and Evolution 29 1695ndash1701Lavoue S (2016) Was Gondwanan breakup the cause of the
intercontinental distribution of Osteoglossiformes A
time-calibrated phylogenetic test combining molecular
morphological and paleontological evidence Molecular
Phylogenetics and Evolution 99 34ndash43Lomolino MV Riddle BR Whittaker RJ amp Brown JH
(2010) Biogeography 4th edn Sinauer Associated Inc Sun-
derland MA
Longrich NR Vinther J Pyron RA Pisani D amp Gau-
thier JA (2015) Biogeography of worm lizards (Amphis-
baenia) driven by end-Cretaceous mass extinction
Proceedings of the Royal Society B Biological Sciences 282
20143034
Lopez-Fernandez H Arbour JH Winemiller K amp Honey-
cutt RL (2013) Testing for ancient adaptive radiations in
neotropical cichlid fishes Evolution 67 1321ndash1337Luebert F Couvreur TL Gottschling M Hilger HH
Miller JS amp Weigend M (2017) Historical biogeography
of Boraginales West Gondwanan vicariance followed by
long-distance dispersal Journal of Biogeography 44 158ndash169
Matschiner M Musilova Z Barth JM Starostova Z Sal-
zburger W Steel M amp Bouckaert R (2017) Bayesian
phylogenetic estimation of clade ages supports trans-Atlan-
tic dispersal of cichlid fishes Systematic Biology in press
DOI 101093sysbiosyw076
Matzke NJ (2013a) Probabilistic historical biogeography
new models for founder-event speciation imperfect detec-
tion and fossils allow improved accuracy and model-test-
ing Frontiers of Biogeography 5 242ndash248Matzke NJ (2013b) BioGeoBEARS BioGeography with Baye-
sian (and Likelihood) evolutionary analysis in R scripts
University of California Berkeley Berkeley CA Available
at httpCRAN R-project orgpackage= BioGeoBEARS
(Last accessed May 5 2016)
Matzke NJ (2014) Model selection in historical biogeogra-
phy reveals that founder-event speciation is a crucial pro-
cess in island clades Systematic Biology 63 951ndash970McCulloch GA Wallis GP amp Waters JM (2016) A time-
calibrated phylogeny of southern hemisphere stoneflies
testing for Gondwanan origins Molecular Phylogenetics
and Evolution 96 150ndash160Meng HH Jacques FM Su T Huang YJ Zhang ST
Ma HJ amp Zhou ZK (2014) New Biogeographic insight
into Bauhinia sl (Leguminosae) integration from fossil
records and molecular analyses BMC Evolutionary Biology
14 1
Mennes CB Lam VKY Rudall PJ Lyon SP Graham
SW Smets EF amp Merckx SFT (2015) Ancient Gond-
wana break-up explains the distribution of the myco-
heterotrophic family Corsiaceae (Liliales) Journal of
Biogeography 42 1123ndash1136Mertz DF amp Renne PR (2005) A numerical age for the
Messel fossil deposit (UNESCO World Heritage Site)
derived from 40Ar39Ar dating on a basaltic rock frag-
ment Courier Forschungsinstitut Senckenberg 255 67ndash75Meseguer AS Lobo JM Ree R Beerling DJ amp San-
martın I (2015) Integrating fossils phylogenies and niche
models into biogeography to reveal ancient evolutionary
history the case of Hypericum (Hypericaceae) Systematic
Biology 64 215ndash232Miller MA Pfeiffer W amp Schwartz T (2010) Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees Proceedings of the Gateway Computing Environ-
ments Workshop (GCE) 14 November 2010 pp 1ndash8 NewOrleans LA
Milner ML Weston PH Rossetto M amp Crisp MD
(2015) Biogeography of the Gondwanan genus Lomatia
(Proteaceae) vicariance at continental and intercontinental
scales Journal of Biogeography 42 2440ndash2451Minh BQ Nguyen MAT amp von Haeseler A (2013)
Ultrafast approximation for phylogenetic bootstrap Molec-
ular Biology and Evolution 30 1188ndash1195Nguyen LT Schmidt HA von Haeseler A amp Minh BQ
(2015) IQ-tree a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies Molecular
Biology and Evolution 32 268ndash274Pyron RA (2014) Biogeographic analysis reveals ancient
continental vicariance and recent oceanic dispersal in
amphibians Systematic Biology 63 779ndash797R Core Team (2016) R A language and environment for sta-
tistical computing R Foundation for Statistical Computing
Vienna Austria Available at httpswwwR-projectorg
(Last accessed October 19 2016)
Ree RH amp Sanmartın I (2009) Prospects and challenges
for parametric models in historical biogeographical infer-
ence Journal of Biogeography 36 1211ndash1220Ree RH amp Smith SA (2008) Maximum likelihood infer-
ence of geographic range evolution by dispersal local
extinction and cladogenesis Systematic Biology 57 4ndash14Ree RH Moore BR Webb CO amp Donoghue MJ
(2005) A likelihood framework for inferring the evolution
of geographic range on phylogenetic trees Evolution 59
2299ndash2311Ronquist F amp Sanmartın I (2011) Phylogenetic methods in
biogeography Annual Review of Ecology Evolution and
Systematics 42 441
Ronquist F Teslenko M van der Mark P Ayres DL
Darling A Heuroohna S Larget B Liu L
Suchard MA amp Huelsenbeck JP (2012) MrBayes 32
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
13
Biogeography of Hydrophilini giant water scavenger beetles
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
efficient Bayesian phylogenetic inference and model
choice across a large model space Systematic Biology
61 539ndash542Schwarz MP Fuller S Tierney SM amp Cooper SJ (2006)
Molecular phylogenetics of the exoneurine allodapine bees
reveal an ancient and puzzling dispersal from Africa to
Australia Systematic Biology 55 31ndash45Seton M Meurouller RD Zahirovic S Gaina C Torsvik T
Shephard G Talsma A Gurnis M Turner M Maus
S amp Chandler M (2012) Global continental and ocean
basin reconstructions since 200 Ma Earth-Science Reviews
113 212ndash270Short AEZ (2010) Phylogeny evolution and classification
of the giant water scavenger beetles (Coleoptera
Hydrophilidae Hydrophilini Hydrophilina) Systematics
and Biodiversity 8 17ndash37Short AEZ amp Fikacek M (2011) World catalogue of the
Hydrophiloidea (Coleoptera) additions and corrections II
(2006ndash2010) Acta Entomologica Musei Nationalis Pragae
51 83ndash122Short AEZ amp Fikacek M (2013) Molecular phylogeny
evolution and classification of the Hydrophilidae (Coleop-
tera) Systematic Entomology 38 723ndash752Tamura K Stecher G Peterson D Filipski A amp Kumar S
(2013) MEGA6 molecular evolutionary genetics analysis
version 60 Molecular Biology and Evolution 30 2725ndash2729Thomas N Bruhl JJ Ford A amp Weston PH (2014)
Molecular dating of Winteraceae reveals a complex biogeo-
graphical history involving both ancient Gondwanan
vicariance and long-distance dispersal Journal of Biogeog-
raphy 41 894ndash904Toussaint EFA amp Condamine FL (2016) To what extent
do new fossil discoveries change our understanding of
clade evolution A cautionary tale from burying beetles
(Coleoptera Nicrophorus) Biological Journal of the Linnean
Society 117 686ndash704Toussaint EFA Fikacek M amp Short AEZ (2016)
India-Madagascar vicariance explains cascade beetle bio-
geography Biological Journal of the Linnean Society 118
982ndash991Toussaint EFA Hendrich L Hajek J Michat MC Pan-
jaitan R Short AEZ amp Balke M (2017) Evolution of
Pacific Rim diving beetles sheds light on Amphi-Pacific
biogeography Ecography in press doi 101111ecog
02195
Trifinopoulos J Nguyen LT von Haeseler A amp Minh
BQ (2016) W-IQ-TREE a fast online phylogenetic tool
for maximum likelihood analysis Nucleic Acids Research
44 W232ndashW235
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article
Appendix S1 Taxon sampling used in this study
Appendix S2 Maximum likelihood gene fragment trees
inferred with W-Iq-Tree
Appendix S3 Details of the lsquoBioGeoBEARSrsquo analyses
conducted with the DEC and DEC+j models
BIOSKETCH
Emmanuel FA Toussaint is a Postdoctoral researcher at
the University of Kansas in Lawrence USA His main
research interest focuses on the origin and evolution of bio-
diversity at global and regional scales He combines ecologi-
cal and molecular data to study lineage diversification and
biogeography of insects mainly aquatic beetles and tropical
butterflies Devin Bloom is an assistant professor at Wes-
tern Michigan University in Kalamazoo MI USA His main
research focuses on the biogeography evolution and diversi-
fication of fishes Andrew EZ Short is an associate profes-
sor at the University of Kansas in Lawrence USA His
research focuses on the diversity distribution and evolution
of aquatic beetles particularly in South America
Author contributions EFAT DB and AEZS conceived
the study DB and AEZS contributed the data EFAT
analysed them designed the figures and wrote the article
AEZS made significant comments on and improvements
to the manuscript
Editor Isabel Sanmartın
Journal of Biogeographyordf 2017 John Wiley amp Sons Ltd
14
E F A Toussaint et al
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