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ORIGINALARTICLE
Systematics and biogeography ofRhodniini (Heteroptera: Reduviidae:Triatominae) based on 16S mitochondrialrDNA sequences
Alexandre Silva de Paula1*, Lileia Diotaiuti1 and Cleber Galvao2
1Laboratorio de Triatomıneos e Epidemiologia
da Doenca de Chagas, Centro de Pesquisas
Rene Rachou/FIOCRUZ, Av. Augusto de Lima
1715, 30190-002 Belo Horizonte, MG and2Laboratorio Nacional e Internacional de
Referencia em Taxonomia de Triatomıneos,
Departamento de Protozoologia, Instituto
Oswaldo Cruz/FIOCRUZ, Av. Brasil 4365,
21040-900 Rio de Janeiro, RJ, Brazil
*Correspondence: Alexandre Silva de Paula,
Laboratorio de Triatomıneos e Epidemiologia
da Doenca de Chagas, Centro de Pesquisas Rene
Rachou/FIOCRUZ, Av. Augusto de Lima 1715,
30190-002 Belo Horizonte, MG, Brazil.
E-mail: alex@cpqrr.fiocruz.br
ABSTRACT
Aim The tribe Rhodniini is one of six comprising the subfamily Triatominae
(Heteroptera: Reduviidae), notorious as blood-sucking household pests and
vectors of Trypanosoma cruzi throughout Latin America. The human and
economic cost of this disease in the American tropics is considerable, and these
bugs are unquestionably of great importance to man. Studies of the evolution,
phylogeny, biogeography, ecology, physiology and behaviour of the Rhodniini are
needed to help improve existing Chagas’ disease control programmes. The
objective of the study reported here was to propose biogeographical hypotheses to
explain the modern geographical distribution of the species of Rhodniini.
Location Neotropical region.
Methods We employed mitochondrial rDNA sequences (16S) currently
available in GenBank to align sequences of Rhodniini species using ClustalX.
The analyses included 16S sequences from predatory reduviid subfamilies
(Stenopodainae, Ectrichodiinae, Harpactorinae, Reduviinae and Salyavatinae)
present in GenBank as an outgroup. Cladistic analysis used the program PAUP to
derive trees based on maximum parsimony (MP) and maximum likelihood (ML).
Known distribution data for Rhodniini species were obtained from reviews and
plotted on maps of South and Central America using the program iMap. An area
cladogram was derived from the cladistic result to show the historical connections
among the studied taxa and the endemic areas. The program TreeMap (Jungle
Edition) was used to deduce taxon–area associations where the optimal solutions
to explain the biogeographical hypothesis of the Rhodniini in the Neotropics were
those with lowest total cost.
Results Parsimony and maximum-likelihood analysis of 16S rDNA sequences
included 14 species of Rhodniini, as well as five species of predatory Reduviidae
representing five of the predatory subfamilies. Tanglegrams were used to show the
relationship between the Neotropical areas of endemism and Rhodniini species.
When TreeMap with codivergence (vicariance) events were weighted as 0 and
duplication (sympatry), lineage losses (extinction) and host switching (dispersal)
were all weighted as 1, 20 scenarios were found to explain the biogeographical
history of Rhodniini in the Neotropical region. Twelve of the optimal solutions
with the lowest total cost were used to explain the biogeography of the Rhodniini
in the Neotropics. These optimal reconstructions require six vicariance events, 20
duplications (sympatry), at least three dispersals, and at least one extinction
event.
Main conclusions The Rhodniini have a complex biogeographical history that
has involved vicariance, duplications (sympatry), dispersal and extinction events.
The main geological events affecting the origin and diversification of the
Rhodniini in the Neotropics were (1) uplift of the Central Andes in the Miocene
Journal of Biogeography (J. Biogeogr.) (2007) 34, 699–712
ª 2006 The Authors www.blackwellpublishing.com/jbi 699Journal compilation ª 2006 Blackwell Publishing Ltd doi:10.1111/j.1365-2699.2006.01628.x
INTRODUCTION
The tribe Rhodniini Pinto, 1926 is one of six comprising the
subfamily Triatominae (Heteroptera: Reduviidae), notorious
as blood-sucking household pests and vectors of Trypanosoma
cruzi Chagas, 1909 throughout the Neotropics (Galvao et al.,
2003). Their genera belong to a well defined monophyletic
group (Lent & Wygodzinsky, 1979). Morphological characters
can be used to distinguish Rhodnius Stal, 1859 and Psammo-
lestes Bergroth, 1911, the two genera of Rhodniini, particularly
the apically inserted antennae and the presence of distinct
callosities behind the eyes (Lent & Wygodzinsky, 1979).
Species of Rhodnius are primarily arboreal, often occupying
ecotopes in palm tree crowns or epiphytic bromeliads. The
genus is widely distributed in South and Central America. In
Central America and the northern Andean countries (Peru,
Ecuador, Colombia and Venezuela), Rhodnius species are
primary targets of Chagas’ disease vector control initiatives.
This is particularly true for Rhodnius prolixus Stal, 1872, as well
as Rhodnius ecuadoriensis Lent & Leon, 1958 in parts of
Ecuador and northern Peru and Rhodnius pallescens Barber,
1932 in Panama and parts of Colombia. Other Rhodnius
species have local epidemiological importance, including
Rhodnius neglectus Lent, 1954 and Rhodnius nasutus Stal,
1859 in central and northeastern Brazil; Rhodnius stali Lent
et al., 1993 in Bolivia; and Rhodnius brethesi Matta, 1919 in the
Brazilian Amazon (Schofield & Dujardin, 1999). The genus
Rhodnius was reviewed by Lent (1948), Lent & Jurberg (1969),
Lent & Wygodzinsky (1979). Three additional species have
since been described: R. stali (Lent et al., 1993), Rhodnius
colombiensis (Moreno et al., 1999) and Rhodnius milesi
(Valente et al., 2001). The genus Rhodnius currently has 16
recognized species, including Rhodnius dalessandroi Carcavallo
& Barreto, 1976 and Rhodnius paraensis Sherlock et al., 1977,
neither of which has been collected since its original descrip-
tion.
The genus Psammolestes includes Psammolestes arturi
(Pinto), 1926, Psammolestes coreodes Bergroth, 1911 and
Psammolestes tertius Lent & Jurberg, 1965 (Galvao et al.,
2003). The genus was reviewed by Lent & Jurberg (1965) and
Lent & Wygodzinsky (1979). Species of Psammolestes live in
birds’ nests. They do not associate with man, and only rarely
with other mammals; as such they are not important in
T. cruzi transmission (Lent & Wygodzinsky, 1979).
The importance of the Rhodniini lies in the fact that some of
its members feed on humans and many of these transmit
T. cruzi, the protozoan that causes Chagas’ disease. The human
and economic costs of this disease in the American tropics are
considerable (Schaefer, 2005).
A wide variety of reasons have been proposed for the high
biological diversity seen in the Neotropics (Amorim, in press).
Accepted causes of disjunction include: (1) tectonic displace-
ment, (2) sea-level fluctuations, (3) interspecific competition
together with climate change, (4) parapatric speciation along
environmental gradients, (5) pest pressure, and (6) fine-scale
habitat heterogeneity (for details see Amorim, 2006).
The first two of these causes are classed as palaeogeograph-
ical, being Mesozoic–Lower Tertiary events, while the latter
four occurred mainly in the Quaternary. Some of them
represent competing explanations for the same biological
events. Most of the causes proposed for species diversification
in these models were not inferred based on a given method of
biogeographical reconstruction, but rather were chosen a pri-
ori based on other sources of evidence (Amorim, in press).
Several Neotropical groups of organisms have species that
are widely distributed throughout South and Central America
(Amorim, in press). However, groups as divergent as mammals
and insects also contain species with restricted and overlapping
geographical distributions. The areas of endemism proposed
by dispersionists, refuge theory biogeographers and vicariance
biogeographers, based on studies of different groups such as
insects, arachnids, mammals and plants, are largely congruent.
Thus, despite disagreements about the causes of cladogeneses,
different biogeographical schools largely concur regarding the
boundaries of the main areas of endemism in the Neotropics
(Fig. 1). This strongly suggests common causes for the origin
of these patterns.
Methods that allow for both dispersal and vicariance have
been proposed to reconstruct biogeographical history
(Ronquist, 1997). Hence there is a growing plurality in the
theoretical and methodological tools of biogeography. Never-
theless, few empirical studies have documented the relative
roles of vicariance and dispersal (Zink et al., 2000). The aim of
the study reported here was to formulate biogeographical
or later, (2) break-up of the Andes into three separate cordilleras (Eastern,
Central and Western) in the Plio-Pleistocene, (3) formation of a land corridor
connecting South and North America in the Pliocene, and (4) uplift of the Serra
do Mar and Serra da Mantiqueira mountain systems between the Oligocene and
Pleistocene. The relationships and biogeographical history of the species of
Rhodniini in the Neotropical region probably arose from the areas of endemism
shown in our work.
Keywords
Chagas’ disease control, Hemiptera, historical biogeography, Neotropical,
Psammolestes, rDNA mitochondrial gene, Rhodnius, Triatominae.
A. S. Paula, L. Diotaiuti and C. Galvao
700 Journal of Biogeography 34, 699–712ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd
hypotheses to explain the modern geographical distribution of
Rhodniini species. Both systematic and biogeographical
approaches were used to construct testable hypotheses, using
area cladograms (Cracraft, 1994) and the program TreeMap
2.02 (Charleston & Page, 2001). The biogeographical hypoth-
esis was formulated using Amorim’s (in press) historical
reconstruction of the Neotropical region (Fig. 2).
METHODS
Systematics
In the present study we used mitochondrial rDNA sequences
(16S) currently available in the NCBI genetic database. Other
genes currently available in the NCBI database (e.g. 12S,
cytochrome oxidase 1, cytochrome b, and nuclear rDNA
sequences 18S and ITS2) were not considered because of the
methodological difficulties of combining sequence information
from different genes (Kitching et al., 1998; Sanderson &
Shaffer, 2002), and the fact that different genes were
represented by unequal taxon sets in the construction of the
outgroup. Initial analyses were made by aligning groups of
sequences using ClustalX 1.83 (Thompson et al., 1997) under
gap-opening/gap-extension penalties 15/9, 15/6, 15/3, 9/6, 9/3,
6/3, and by treating the gaps as missing (?). The analyses
included the available 16S sequences from predatory reduviid
subfamilies present in GenBank as an outgroup: Stenopoda
spinulosa Giacchi, 1969 (Stenopodainae); Ectrychotes andreae
(Thunberg), 1784 (Ectrichodiinae); Sycanus croceus Hsiao,
1979 (Harpactorinae); Tiarodes venenatus Matsumura, 1913
(Reduviinae); Lisarda rhypara Stal, 1858 (Salyavatinae)
(Table 1). The outgroup was chosen based on the findings of
Paula et al. (2005) and the fact that the ancestral form of
Rhodnius was placed in the Stenopodainae by Schofield &
Dujardin (1999).
The species R. dalessandroi, R. paraensis, Rhodnius amazo-
nicus, R. milesi and P. arturi were not included in this analysis
because there were no gene sequences for them in GenBank.
Cladistic analysis used the program PAUP 4.0b10 (Swofford,
2002) to derive trees based on maximum parsimony (MP) and
Figure 1 Simplified picture of main areas of
endemism for Neotropical organisms based
on vertebrates, insects and other groups. The
mere existence and the limits of areas of
endemism are always hypotheses that may be
corrected with additional studies. Although
there may be additional areas, there are
insufficient data to attain a minimally reliable
hypothesis. (Source: artwork provided by Dr
Dalton de Souza Amorim – Faculdade de
Filosofia, Ciencias e Letras de Ribeirao Preto/
USP; see Amorim & Pires, 1996).
Systematics and biogeography of Rhodniini
Journal of Biogeography 34, 699–712 701ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd
maximum likelihood (ML). Parsimony branch-and-bound
searches were performed on the alignments using the chosen
outgroup. Characters were treated as unordered and of equal
weight, and the trees were rooted at an internal node with basal
polytomy. Strict consensus trees were then obtained for each
branch-and-bound search. Parsimony bootstrap analyses were
conducted employing a heuristic search with 100 bootstrap
replicates using 10 random stepwise addition (tree-bisection-
reconnection, TBR). Strict consensus trees were obtained from
all the retained trees in the branch-and-bound searches, and
Figure 2 General biogeographical pattern of
the Neotropical region based on different
groups of vertebrates, insects and plants. The
first vicariant event corresponds to the
separation of the Caribbean arc from the
continental Neotropical region. The second
event divides north-west South America,
Central America and coastal Mexico (NW)
from south-east South America (SE). The
third event separates Central America and the
Choco regions from the Amazonian forest in
the NW Neotropical component, and south-
east Amazonia from the Atlantic Forest in the
SE Neotropical component. (Source: artwork
provided by Dr Dalton de Souza Amorim –
Faculdade de Filosofia, Ciencias e Letras de
Ribeirao Preto/USP; Amorim, in press).
Table 1 Species and 16S ribosomal DNA
gene (mitochondrial gene) sequences used in
maximum parsimony and maximum likeli-
hood analyses
Taxa Accession no. Length %GC
Outgroup
Stenopodainae
Stenopoda spinulosa Giacchi, 1969 AY252684 314 28.0
Ectrichodiinae
Ectrychotes andreae (Thunberg, 1784) AY127035 508 27.0
Harpactorinae
Sycanus croceus Hsiao, 1979 AY127043 510 30.0
Reduviinae
Tiarodes venenatus Matsumura, 1913 AY127045 509 32.0
Salyavatinae
Lisarda rhypara Stal, 1858 AY127039 508 29.0
Ingroup
Rhodnius pallescens Barber, 1932 AF045706 374 24.0
Rhodnius ecuadoriensis Lent & Leon, 1958 AF028746 285 23.0
Rhodnius colombiensis Mejia, Galvao & Jurberg, 1999 AY035438 510 28.0
Rhodnius pictipes Stal, 1872 AF045709 373 26.0
Rhodnius stali Lent, Jurberg & Galvao, 1993 AY035437 508 29.0
Rhodnius prolixus Stal, 1859 AF045707 373 27.0
Rhodnius nasutus Stal, 1859 AF028749 284 24.0
Rhodnius neglectus Lent, 1954 AF045704 372 29.0
Rhodnius robustus Larrousse, 1927 AF045705 372 30.0
Rhodnius domesticus Neiva & Pinto, 1923 AY035440 508 32.0
Rhodnius brethesi Matta, 1919 AF045710 374 27.0
Rhodnius neivai Lent, 1953 AY035441 508 31.0
Psammolestes coreodes Bergroth, 1911 AF045708 371 27.0
Psammolestes tertius Lent & Jurberg, 1965 AY035439 503 30.0
Species of subfamilies Stenopodainae, Ectrichodiinae, Harpactorinae, Reduviinae and Salyava-
tinae were used as outgroups (see Methods). Length ¼ DNA sequence length; %GC ¼ guanine/
cytosine content.
A. S. Paula, L. Diotaiuti and C. Galvao
702 Journal of Biogeography 34, 699–712ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd
the topology of each tree under individual gap-opening/gap-
extension penalties was tested with ML, using a model of
estimated gamma distribution (discrete approximation),
HKY85 variant to allow for transition/transversion bias,
unequal base frequencies and different substitution rates (Page
& Homes, 1998), empirical base frequencies and an estimated
substitution model following heuristic stepwise addition using
TBR branch-swapping.
Biogeography
Distributional data for Rhodnius species were obtained from
reviews by Lent (1948), Lent & Jurberg (1969), Lent
& Wygodzinsky (1979). Additional localities for R. stali,
R. colombiensis, R. milesi and R. amazonicus were obtained
from Lent et al. (1993), Moreno et al. (1999), Valente et al.
(2001) and Berenger & Pluot-Sigwalt (2002), respectively.
Distributional data for Psammolestes species were obtained
from Lent & Jurberg (1965) and Lent & Wygodzinsky (1979).
Coordinates of the localities were obtained from Vanzolini &
Papavero (1969) and Brown (1979). Species distributions were
plotted on maps of South and Central America using the
program iMap 3.1 for Apple Macintosh.
Phylogenetic analysis of Rhodniini species was required to
test biogeographical patterns, and the areas of endemism
proposed by Amorim (in press) (Fig. 2) were used to produce
a derived-area cladogram to show the historical connections
among the taxa studied and the endemic areas.
In the biogeographical context, the four events used in most
of the models were (1) vicariance, allopatric speciation caused
by the origin of a dispersal barrier affecting many organisms
simultaneously; (2) duplication (speciation within an area),
which is usually allopatric and associated with a local or
temporary dispersal barrier within an area; (3) dispersal,
occurring between isolated areas and associated with speci-
ation; and (4) extinction, which leads to the disappearance of a
lineage from an area where it was predicted to occur
(Sanmartın & Ronquist, 2004).
The reconstruction can best be illustrated by using a
trackogram that displays the organisms’ phylogeny on top of
the area cladogram, with symbols denoting the four kinds of
event. Historical associations can be divided into three basic
categories (Page & Charleston, 1998): genes and organisms;
organisms and organisms; and organisms and areas. Similar-
ities among the event categories for the different kinds of
association need not imply close analogies among the proces-
ses; rather the analogy is among the patterns these processes
produce. Page & Charleston (1998) acknowledged that
equivalent processes among different associations could be
applied to historical biogeography. Following their view, ‘host–
associate’ can be accepted as ‘organism–area’; ‘codivergence’ as
‘vicariance’; ‘duplication’ as ‘sympatry’; ‘host transfer’ as
‘dispersal; and ‘sorting event’ as ‘extinction’.
The reconciled trees used in the previous versions of
TreeMap have some limitations, the most severe being that
they do not accommodate horizontal transfer (dispersal).
Charleston (1998) developed a solution to this problem that
employs a mathematical structure called ‘jungles’, which
contains all possible ways in which an associate tree (¼ taxa)
can be mapped into a host tree (¼ areas), given the four
processes of codivergence, duplication, sorting and horizontal
transfer. This was implemented in TreeMap (Jungle Edition)
ver. 2.02 (Charleston & Page, 2001) and the program was used
to deduce taxon–area associations in our study. The optimal
solutions to explain the biogeographical hypothesis of the
Rhodniini in the Neotropics were those with lowest total cost
(Charleston, 1998).
Information from the studies of van der Hammen (1974),
Clapperton (1993), Hallam (1994), Lundberg et al. (1998),
Aleman & Ramos (2000) and Ramos & Aleman (2000) were
accessed to fit the phylogenetic hypothesis to the geological
events related to the historical distribution of the species
studied here.
RESULTS
Systematics
Parsimony and ML analyses of 16S rDNA sequences included
14 species of Rhodniini and five species of predatory
Reduviidae, representing five of the predatory subfamilies:
Stenopodainae, Ectrichodiinae, Harpactorinae, Reduviinae and
Salyavatinae.
The branch-and-bound search under gap-opening/gap-
extension penalties 15/9, 15/6, 15/3, 9/6, 9/3, 6/3, and using
the outgroup above, resulted in 12 optimal trees (Table 2). The
strict consensus tree for these 12 trees is shown in Fig. 3a. All
the retained trees had the same topology except for the clade
including R. brethesi, R. colombiensis and R. pictipes, which
was unsolved in the strict consensus. Maximum-likelihood
analysis under the same gap penalties resulted in eight trees
(Table 3): the strict consensus of these is shown in Fig. 3b.
Unlike the MP analysis, the strict consensus from the trees
retained in the ML did not show resolution for most of the
Rhodniini species, except for the clade including R. brethesi,
R. stali and R. pictipes. To compare both results of the strict
consensus and combine their resolution, the topology from the
Table 2 Parsimony branch-and-bound search results
GO/GE BP PBP „ TREE L CI RI RC HI
15/9 547 144 3 545 0.607 0.565 0.343 0.393
15/6 550 139 3 524 0.620 0.569 0.353 0.380
15/3 550 136 1 515 0.617 0.563 0.348 0.383
9/6 551 134 1 502 0.620 0.573 0.355 0.380
9/3 554 129 1 491 0.623 0.580 0.362 0.377
6/3 560 129 3 474 0.631 0.593 0.374 0.369
GO/GE, gap-opening/gap-extension penalties; BP, total characters;
PBP, parsimony-informative characters; „ TREE, number of trees
retained; L, length; CI, consistency index; RI, retention index; RC,
rescaled consistency index; HI, homoplasy index.
Systematics and biogeography of Rhodniini
Journal of Biogeography 34, 699–712 703ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd
retained trees was chosen using the alignments 15/3, 9/6 and
9/3 (Fig. 4). Parsimony bootstrap values were obtained for the
alignments 9/6 and 9/3, the consistency indexes of which were
0.620 and 0.623, respectively (Fig. 4). Only Rhodnius domes-
ticus and the clade including Psammolestes species did not
show bootstrap values over 50%. The members of these genera
are morphologically very distinct, and our study suggests that
Psammolestes should be included in the genus Rhodnius.
The outgroup species did not show any sister-group
relationship with the Rhodniini, so that no hypothesis could
be provided to explain the relationship between this tribe and
the subfamilies of Reduviidae. The inclusion of additional
subfamilies of Reduviidae as outgroups in future studies could
resolve this question, although Paula et al. (2005) postulated
an apparent link between Rhodniini, Salyavatinae and Harp-
actorinae.
Biogeography
The distributions of Rhodniini species in the Neotropical
region are shown in Figs 5 and 6, with R. ecuadoriensis,
R. pallescens and R. colombiensis to the west, and R. brethesi,
R. pictipes and R. stali to the east of the Andes (Fig. 5). The
ranges of Rhodnius neivai and R. domesticus are widely
separated, the former occurring in northern South America
and the latter in Atlantic forest in the south-east of the
continent (Fig. 6). Both P. tertius and P. coreodes are found in
south-east South America (Fig. 6), while R. nasutus is restric-
ted to arid regions in the north-east of the continent;
R. prolixus occurs throughout South and Central America;
R. neglectus appears to be restricted to the Serra do Mar and
Serra da Mantiqueira; and R. robustus is widespread in the
Amazon basin (Fig. 6).
An area cladogram for the species of Rhodniini is shown in
Fig. 7, as it is not possible to observe an unambiguous
vicariant pattern for all the species. The first clade, including
R. colombiensis, R. ecuadoriensis and R. pallescens, showed the
latter two species to be sympatric in the Andean/Mesoameri-
can (AnMA) area (Amorim & Pires, 1996). The presence of
R. colombiensis in north-western Amazonia (NWAm) is prob-
ably the result of a vicariance event in the north-west
Neotropical region (Fig. 2), and suggests speciation by vica-
riance following the Andean and Central American uplifts. The
next clade links R. brethesi, R. stali and R. pictipes, three
species with wide geographical ranges overlapping more than
one endemic area, and does not provide a robust explanation
of the biogeographical history of these species in the
Neotropics. Rhodnius neivai occurs in the NWAm area and
R. domesticus in the Atlantic Forest (AtlFor). The species
P. tertius, P. coreodes and R. nasutus are found in AtlFor and
speciated by duplication (paralogy) in this region. Rhodnius
prolixus and R. robustus appear to have dispersed from the
AtlFor, while R. neglectus also appear to have arisen by
duplication in the AtlFor (Fig. 7).
The tanglegram in Fig. 8 shows the relationship between the
areas of endemism proposed by Amorim (in press) and the
phylogeny of the Rhodniini species studied.
Figure 3 (a) Strict consensus tree from
parsimony branch-and-bound searches
resulting in 12 retained trees; (b) strict con-
sensus tree from maximum-likelihood sear-
ches resulting in eight retained trees – in both
cases, total number of trees retained in all
alignments (see Tables 2 & 3).
Table 3 Maximum-likelihood results using the strict consensus
tree retained by parsimony branch-and-bound searches
GO/GE „ TREE )ln L T/T Time
15/9 1 3053.47534 1.60428 06:14.9
15/6 1 2970.87875 1.68883 03:38.5
15/3 1 2936.86807 1.75882 07:06.9
9/6 3 2891.43064 1.86062 10:20.2
9/3 1 2864.50300 1.93612 05:40.6
6/3 1 2811.05100 2.05809 05:50.0
GO/GE, gap opening/gap extension penalties; „ TREE, number of
trees retained; )ln L, likelihood scores; T/T, transition/transversion
ratio; Time, time used (h).
A. S. Paula, L. Diotaiuti and C. Galvao
704 Journal of Biogeography 34, 699–712ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd
TreeMap 2.02 (Charleston & Page, 2001), with codiver-
gence (vicariance) events weighted as 0 and duplication
(sympatry), lineage losses (extinction) and host switching
(dispersal) all weighted as 1 found 20 scenarios to explain the
biogeographical history of Rhodniini in the Neotropical
region (Table 4). The 12 optimal solutions with the lowest
total cost to explain the biogeographical hypothesis of the
Rhodniini are shown in Fig. 9 (reconstructions 5–16 in
Table 4). These optimal reconstructions require six vicariance
events (black circles), 20 duplications (sympatry; squares), at
least three dispersals (arrows) and at least one extinction
event (grey circles).
TreeMap provided several patterns to explain the species/
area relationships of Rhodniini; thus R. ecuadorensis showed a
vicariance event in the AnMA (Fig. 9a–h) and became extinct
in the NWAm + SWAm (Fig. 9i–l), while R. pallescens
dispersed from NWAm to AnMA (Fig. 9a–d), or speciated
by vicariance when the R. ecuadoriensis lineage disappeared
from those areas (Fig. 9i–l).
This can be explained by the uplift of the Isthmus of
Panama acting as a vicariance event that allowed the
lineage, including R. ecuadoriensis and R. pallescens, to
spread. R. colombiensis dispersed from NWAm (Fig. 9a–d)
and became extinct in the SWAm area (Fig. 9a–l). The
history of the lineage, including R. brethesi, R. pictipes
and R. stali, is puzzling. TreeMap indicated vicariance of
R. brethesi in NWAm and also of R. stali in SWAm, whereas
R. pictipes could have arisen through vicariance in NWAm.
This seems the most robust scenario to explain the present-
day geographical distribution of these species. All the
solutions showed R. neivai in the AnMA endemic area
following dispersal of the lineage R. domesticus–R. neglectus
from AnMA. This clade showed duplication (speciation by
sympatry) in AtlFor, followed by dispersal of R. prolixus and
R. robustus to NWAm, or dispersal of R. neglectus from
NWAm to AtlFor. This last solution deserves more study to
explain the presence of R. prolixus in AtlFor, which has been
interpreted by several epidemiologists as being due to
laboratory escapes. TreeMap could elucidate the biogeo-
graphical history of the Rhodniini more effectively if more
taxa and areas were included to generate the ‘jungles’.
DISCUSSION
Systematics
We refute the idea of an ancestral triatomine similar to extant
Stenopodainae, as well as R. pictipes being the species closest to
the ancestor of Rhodnius, as proposed by Schofield & Dujardin
(1999). Although the sister group of Rhodnius may be the
Salyavatinae or Harpactorinae (Paula et al., 2005), there is still
no conclusive evidence to support this.
According to Schaefer (2005), the main problems to be
resolved in triatomine systematics are whether the subfamily
has a truly independent origin and how it is related to the
other subfamilies of the Reduviidae. We currently have no
idea which of these subfamilies is most closely related to the
Triatominae. The surprisingly few studies of reduviid
subfamilies have allied the Triatominae with the Harpactor-
inae, Peiratinae, Physoderinae, Reduviinae and Stenopodai-
nae.
Ambrose (1999) suggested that the reduviids could be
broadly divided into two groups based on whether or not
they possessed tibial pads (fossulae espongiosae, or tibiarola).
Reduviids with tibial pads may have evolved in the following
sequence: Holoptilinae, Emesinae, Tribelocephalinae, Saici-
nae, Stenopodainae, Harpactorinae. Those without tibial pads
live in tropical forest ecosystems and are known as timid
predators that do not use their forelegs to capture prey,
instead impaling prey items with their long rostra (Ambrose,
1999). Rain forest reduviids may have developed tibial pads
and other features that made them more efficient predators
when they migrated to deciduous scrub forest and other
semi-arid habitats. The most advanced, aggressive predators,
such as members of the Peiratinae and Reduviinae, live in
Figure 4 Selected topology from parsimony branch-and-bound
search to show the phylogenetic hypothesis for the relationship
among Rhodniini species. Numbers above and below branches are
bootstrap support; frequencies ‡ 50%. Gap-opening/gap-exten-
sion penalties were 9/6 and 9/3, respectively, and are shown above
and below the branches.
Systematics and biogeography of Rhodniini
Journal of Biogeography 34, 699–712 705ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd
semi-arid, prey-scarce situations where such features would
be most needed.
The Salyavatinae possess the least developed tibial pads,
which may be rudimentary, consist of mere apical projections
or be distinctly formed. Ambrose (1999) considered the
members of this subfamily to be the most primitive of the
predatory reduviids, ancestral to the subfamilies Triatominae
and Ectrichodiinae (see his Figure 54). Although the Rhodniini
and Salyavatinae could have shared the same Neotropical
ancestor, the results of our study do not provide sufficient
evidence to corroborate this. An alternative, and possibly more
robust hypothesis, is that the Rhodniini and Harpactorinae are
closely related.
Biogeography
Vicariance and dispersalist schools of biogeographical analysis
are both compatible with the dominance of allopatric speci-
ation, but differ in how they construe the interaction between
dispersal and allopatry. In the vicariance paradigm, rare but
extensive dispersal (range expansion) is followed by a series of
allopatric isolation events, interrupted by occasional random
Figure 5 Known distribution of Rhodniini species in South and Central America. See text for data sources.
A. S. Paula, L. Diotaiuti and C. Galvao
706 Journal of Biogeography 34, 699–712ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd
dispersals (Zink et al., 2000). If the isolation events affect many
organisms simultaneously, this process will generate congruent
tree topologies. Dispersalists consider range expansion to be a
more common and regularly occurring phenomenon. Both
dispersal and vicariance processes are viewed as possibly
resulting in predictable as well as unpredictable (random)
events. Conflicting or incongruent trees can be explained by
differential dispersal across pre-existing barriers. Trees may
also appear to conflict if they have unequal numbers of
terminal taxa, which can result from failure of differentiation
in response to a barrier (widespread species), or because some
lineages have experienced extinctions. However, such trees can
be compatible with vicariance. The strongest statements about
dispersal events can be made when they are rare and mixed
with vicariance between areas of endemism. Under such
conditions, there will be strong phylogenetic constraints on
distributional patterns.
Humphries & Ebach (2004) discussed the current state of
cladistic biogeography and highlighted two critical points that
require investigation: the definition of endemic areas and
geographical congruence. Many other authors have discussed
the concepts of endemic areas (Nelson & Platnick, 1981;
Platnick, 1991; Harold & Mooi, 1994; Morrone, 1994;
Humphries & Parenti, 1999; Hausdorf, 2002) without reaching
Figure 6 Known distribution of Rhodniini species in South and Central America. See text for data sources.
Systematics and biogeography of Rhodniini
Journal of Biogeography 34, 699–712 707ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd
a consensus. Cox & Moore (2005) pointed out that some
plants and animals are confined to the areas in which they
evolved and are said to be endemic to that region. Their
confinement may be due to physical barriers to dispersal, as in
the case of many island faunas and floras (palaeoendemics), or
to the fact that they have evolved only recently and have not
yet had time to spread (neoendemics). The concept of endemic
areas requires more investigation and discussion, although
Amorim & Pires (1996) and Amorim (2001, in press) have
published interesting papers on the delimitation of endemic
areas in the Neotropics. Similar vicariance patterns have been
postulated for Coleoptera (Morrone, 2002) and Diptera (Nihei
& Carvalho, 2004).
Vicariance-induced and dispersion-induced elements
explain the present diversity of the Neotropical region
(Amorim, in press). Congruence of the distributions of
different groups of organisms and the Cretaceous–Tertiary
Figure 8 Tanglegram showing relationship between areas of
endemism and phylogeny of Rhodniini species. Areas of ende-
mism as proposed by Amorim (in press).
Table 4 Twenty optimal reconstructions satisfying the following
event costs constraints: codivergences, 0; host switches, 1; dupli-
cations, 1; losses, 1
No. C D L S E z
1 4 22 0 6 28 28
2 4 22 0 6 28 28
3 4 22 0 6 28 28
4 4 22 0 6 28 28
5 6 20 1 5 26 26
6 6 20 1 5 26 26
7 6 20 2 4 26 26
8 6 20 2 4 26 26
9 6 20 1 5 26 26
10 6 20 1 5 26 26
11 6 20 2 4 26 26
12 6 20 2 4 26 26
13 6 20 2 4 26 26
14 6 20 2 4 26 26
15 6 20 3 3 26 26
16 6 20 3 3 26 26
17 6 20 8 2 30 30
18 6 20 8 2 30 30
19 6 20 15 1 36 36
20 6 20 20 0 40 40
No., reconstruction number; C, number of codivergence events
(vicariance); D, number of duplication events (sympatry); L, number
of losses (extinction); S, number of host switch events (dispersal); E,
total number of non-codivergence events; z, total cost.
a b
Figure 7 Area cladogram of Rhodniini species using areas of endemism proposed by Amorim (in press) for the Neotropical region.
A. S. Paula, L. Diotaiuti and C. Galvao
708 Journal of Biogeography 34, 699–712ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd
a b c
d e f
g h i
j k l
Figure 9 Twelve optimal reconstructions with the lowest cost for the tanglegram shown in Fig. 8. Vicariance events (d); duplications
(sympatry) (j); dispersals (arrows); extinction events (d).
Systematics and biogeography of Rhodniini
Journal of Biogeography 34, 699–712 709ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd
geological history of the Neotropical region point to a number
of vicariance events having caused the disjunction patterns
observed today (Fig. 2). Most events were associated with
tectonic movements and inundations, with long-term and
local dispersions also having some impact.
A general pattern shows a separation between Caribbean–
Antillean elements from a continental Neotropical component,
followed by a division between the south-east Amazonia–
Atlantic Forest and north-west South America–Central Amer-
ica components (Fig. 2). Other, more regional events follow.
There is evidence of repeated inundation of the Neotropical
region that may have resulted in vicariance events in the
Cretaceous as well as the Eocene, Miocene and Pleistocene
epochs of the Quaternary period (Amorim, in press).
Amorim & Pires (1996) and Amorim (2001, in press)
showed many more endemic areas in the Neotropical region,
but lacked information to reconstruct their histories. Accord-
ing to these authors, additional studies are needed to add new
areas of endemism; subdivide some existing areas into smaller
units (e.g. AnMA, SWAm); and establish a sequence for area
components that can be subdivided into polytomies (as for
SWAm).
Although the Neotropical region may conveniently be
considered as a single biogeographical unit, it is geologically
complex. The Neotropics include not only the South American
continental plate, but also the southern portion of the North
American and Caribbean plates (Clapperton, 1993). The
complicated geological history of the region, in which these
plates intermittently separated and collided throughout the
Cretaceous and the Tertiary, provides the milieu within which
interactions between organisms have occurred. South America
has been an island continent for most of the evolutionary
history of some organisms (e.g. angiosperms), whereas Central
America constitutes one of the two tropical parts of the
Laurasian ‘supercontinent’. The outstanding geological feature
of South America is the Andes, the longest mountain range in
the world. Andean tectonic history is extremely important in
understanding biogeographical process and pattern. It is now
known that the Andes were built by compressional tectonics
during the last 90 Myr or even longer. It is, therefore, overly
simplistic to view Andean vicariance as a singular event
occurring with the Miocene uplift (Lundberg et al., 1998).
The Andes essentially represent a classical tectonic upthrust
of continental rock, the result of a collision between the
leading edge of the westward-moving South American and
oceanic Pacific Plates (Lundberg et al., 1998). The southern
Andes are the oldest, with significant uplift already present in
the early Cenozoic, prior to the Oligocene. Most of the uplift of
the Central Andes was in the Miocene or later, whereas that
of the northern portion of the range was mostly Plio-
Pleistocene (van der Hammen, 1974). Rhodnius ecuadoriensis
could have speciated following the Central Andean uplift.
As they extend northwards the Andes become more
geologically complex, breaking into three separate cordilleras
(Aleman & Ramos, 2000). The Western and Central Cordil-
leras of the Andes are typical subduction-related mountain
chains developed along the continental margin. However, the
Eastern Cordillera was formed as a result of the interaction
between the Paleogene Caribbean thrusting and Neogene
tectonic inversion during Andean compression. These struc-
tures were greatly affected by a complex system of strike–slip
faults and folds. We think that the break-up of the Andes into
three separate cordilleras was a geological event leading to the
evolution of R. colombiensis, R. brethesi and R. neivai within
their respective geographical ranges.
The major geological events believed to have occurred at the
intersection of South, Central and North America are
described by Hallam (1994). In the Jurassic, North and South
America were joined and Central America as we know it today
did not exist. In the early Cretaceous, North and South
America separated just to the south of the Yucatan peninsula.
Volcanic islands subsequently appeared in the gap between
southern Mexico and Colombia. These were pushed north-
eastwards by the Farallon Plate, which in the mid-Cretaceous
began to form Cuba, the Greater Antilles and the islands off the
Venezuelan coast. By the early Oligocene, another archipelago
had been created between South and North America, the
widest gap between islands being in the Panama region. The
land corridor between South and North America was com-
pleted in the Pliocene with the emergence of the Isthmus of
Panama and north-west Colombia. Rhodnius pallescens occurs
only in Central America and could only have speciated after
the isthmus was formed.
The Serra do Mar and Serra da Mantiqueira mountain
systems are younger than the Andes, having formed between
the Oligocene and Pleistocene (Amorim & Pires, 1996). The
results of our study indicate that many duplication events
(speciations within an area) occurred in AtlFor. As these events
are usually allopatric and associated with a local or temporary
dispersal barrier within an area, the uplift of the Serra do Mar
and Serra da Mantiqueira could have resulted in the speciation
of R. domesticus, P. tertius, P. coreodes and R. nasutus. Uplift
of these mountains may also explain the origin and dispersal of
R. prolixus and R. robustus from AtlFor.
Pinho et al. (1998) collected R. prolixus in Atlantic rain
forest near Teresopolis, in the Serra do Mar. The specimens
(adults, nymphs and eggs) were found in the axils of
Pteridophyta leaves, in foliage and on the trunks of palm
trees. This was the first report of Rhodnius colonizing
Pteridophyta, and some researchers have suggested that these
insects were descended from escaped laboratory-bred speci-
mens. Based on previous studies and our own findings (Fig. 9),
R. prolixus could have speciated in the Atlantic Forest of the
Serra do Mar, following dispersal to north-west South America
and Central America. The distribution of this species in the
Serra do Mar should be studied further as it is the main target
of Chagas’ disease vector control initiatives.
CONCLUSIONS
The Rhodniini have a complex biogeographical history that
has involved vicariance, duplications (sympatry), dispersal and
A. S. Paula, L. Diotaiuti and C. Galvao
710 Journal of Biogeography 34, 699–712ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd
extinction events. The main geological events affecting the
origin and diversification of the Rhodniini in the Neotropics
were: (1) uplift of the Central Andes in the Miocene or later,
(2) break-up of the Andes into three separate cordilleras
(Eastern, Central and Western) in the Plio-Pleistocene, (3)
formation of a land corridor connecting South and North
America in the Pliocene, and (4) uplift of the Serra do Mar and
Serra da Mantiqueira mountain systems between the Oligocene
and Pleistocene. The relationships and biogeographical history
of the species of Rhodniini to the Neotropical region probably
arose from the areas of endemism proposed by Amorim (2001,
in press).
ACKNOWLEDGEMENTS
We thank Dr Carl Schaefer (University of Connecticut) and
Dr Thomas Henry (Smithsonian Institution) for comments
on an early version of the manuscript. Dr Dalton de Souza
Amorim (Faculdade de Filosofia, Ciencias e Letras de Ribeirao
Preto/USP) provided us with figures from his studies (Figs 1
& 2). Dr Gustavo Graciolli (Universidade Federal de Mato
Grosso do Sul) commented on the TreeMap results. Dr Malte
C. Ebach, Dr Juan J. Morrone and Dr John Grehan made
constructive criticisms in reviewing our manuscript. Dr Bruce
Alexander (Liverpool School of Tropical Medicine) made the
English revision and provided comments that improved our
manuscript. The study was supported by grants from the
Centro de Pesquisas Rene Rachou/FIOCRUZ, Fundacao de
Amparo a Pesquisa de Minas Gerais (FAPEMIG), and
Conselho Nacional de Desenvolvimento Cientıfico e Tec-
nologico (CNPq).
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BIOSKETCHES
Alexandre Silva de Paula has a DS in Entomology from
Universidade Federal de Vicosa, Brazil. His research focuses on
the systematics and biogeography of Triatominae. He teaches
Systematics at Centro de Pesquisas Rene Rachou/FIOCRUZ.
Lileia Diotaiuti has a DS in Parasitology from Universidade
Federal de Minas Gerais, Brazil. Her research focuses on
Chagas disease vectors control in Latin America. She teaches
Biology and Control of Triatominae, and Scientific Methodo-
logy at Centro de Pesquisas Rene Rachou/FIOCRUZ.
Cleber Galvao has a DS in Veterinary Science from
Universidade Federal Rural do Rio de Janeiro, Brazil. His
research focuses on biology, systematics and comparative
morphology of Triatominae. He teaches Medical Entomology
and Protozoology at Instituto Oswaldo Cruz/FIOCRUZ.
Editor: Malte C. Ebach
A. S. Paula, L. Diotaiuti and C. Galvao
712 Journal of Biogeography 34, 699–712ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd