Patrick J. Krug California State University, Los Angeles Challenging a textbook case of species...
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Transcript of Patrick J. Krug California State University, Los Angeles Challenging a textbook case of species...
Patrick J. Krug
California State University,
Los Angeles
Challenging a textbook case of species selection: Does loss of dispersal make evolutionary
winners, or the walking dead?
Evolutionary success is unevenly distributed
Major goal of macroevolutionary studies: explain why some groups are more species-rich than others
3 spp.
60 spp.
Can we identify the traits that explain why biodiversity (the number of living species) is unevenly distributed among sister lineages?
what led this group to out-radiate its sister group by 20 to 1?
- change in habitat, feeding method, traits involved in competition or reproduction...?
Evolutionary success is unevenly distributed
Major goal of macroevolutionary studies: explain why some groups are more species-rich than others
**Winners**Woo-hoo!
beetles: 350,000 spp.named (probably >1 million)
Pulmonata: land / freshwater snails + slugs~60,000 spp.
vertebrates: ~45,000 spp.
colonizing dry land led to explosive radiations in many groups
Evolutionary success is unevenly distributed
other lineages can hover at low species numbers despite being ecologically abundant and important
- may survive unchanged for hundreds of millions of years and be very well adapted to their niche, yet never diversify
Losers – the “200 club”
cephalopods: pinnacle of invertebrate vision & intelligence
sharks + rays: top marine predators
Evolutionary success is unevenly distributed
key innovationevolves, sets off burst of diversification
- for instance, a key innovation may lead to an adaptive radiation into many new ecological niches
problem: typically a one-time event, not naturally replicated
Rabosky 2014
Diversification rate of a lineage (r) is the net difference between
speciation () and extinction ()
Diversification happens when
2 living species of Bosellia
- flat sea slugs
- eat one algal genus
- tropical only
134 speciesin sister clade Plakobranchidae
- parapodia: sides rolled up
- eat >20 algal genera
- tropics to poles
Identifying trait-dependent diversification
Easier to test hypotheses if diversification rate is character state-dependent, and character state changes often ancestral state
derived state 3x higher rate of diversification
repeated, independent shifts between states naturally replicated experiment
Comparative methods can identify such traitsRabosky
& McCune 2010
Identifying trait-dependent diversification
Easier to test hypotheses if diversification rate is character state-dependent, and character state changes often derived state 3x higher rate of diversification
Traits that cause greater diversification result in species selection
- form of selection acting on trait(s) shared by all members of a species, or that are a species property (e.g., range)
- unrelated to fitness within species
Rabosky& McCune 2010
Goldberg et al. 2010, Science
Selfing
Non-selfing
Flowering plants repeatedly evolved self-compatible pollen, allowing self- fertilization, from self- incompatible pollen (cannot self-fertilize)
Species selection in plants
In non-selfing plants, estimated speciation rate is higher than extinction rate – thus, lineages diversify (r > 0)
- however, some non-selfers are always gradually evolving into self-fertilizers by character change..
non-selfing
selfing
diversificationrate (r)
Goldberg et al. 2010, Science
Species selection in plantsIn selfing plants, rates of both speciation and extinction increase... however, extinction increased more than speciation
- selfing plants have decreased diversification rates (r < 0)
- this explains why non-selfing plants persist, even though some keep turning into selfers: the remaining non-selfers outcompete the species that undergo character change and become selfers
non-selfing
selfing
diversificationrate (r)
Marine larval type and dispersalmarine invertebrates produce microscopic larvae that swim for
short periods (0 - 5 days) or long periods (>30 days)
Planktotrophy
long-distance dispersal
lecithotrophy
short-distance dispersal
Consequences of long-distance dispersal
planktotrophy lecithotrophy
populationconnectivity
gene flow
local adaptation
speciation rate
extinction risk
planktotrophic populations remain connected over evolutionary timescales
Evolutionary consequences of larval type
planktotrophy lecithotrophy
populationconnectivity
gene flow
local adaptation
speciation rate
extinction risk
ancestrallecithotroph
Evolutionary consequences of larval type
planktotrophy lecithotrophy
demographicconnectivity
gene flow
local adaptation
speciation rate
extinction risk
populationsdiverge...
Evolutionary consequences of larval type
planktotrophy lecithotrophy
demographicconnectivity
gene flow
local adaptation
speciation rate
extinction risk
theory and genetic data suggest lecithotrophic populations will split and diverge into new species...
Evolutionary consequences of larval type
planktotrophy lecithotrophy
demographicconnectivity
gene flow
local adaptation
speciation rate
extinction risk
theory and pop-gen data suggest lecithotrophic populations will split and divergence into new species...
Evolutionary consequences of larval type
planktotrophy lecithotrophy
demographicconnectivity
gene flow
local adaptation
speciation rate
extinction risk
...but may also go extinct more often
Evolutionary consequences of larval type
For 40 years, paleontological studies of snail fossils have inferred larval type from the shape of the larval shell, at the tip of adult shell
lecithotrophic shape
Shuto 1974
Six studies, cited >1,400 times, concluded lecithotrophs diversify more than planktotrophs, so benefit from species selection
Shuto 1974, Hansen 1978, 1980, 1982, Jablonski & Lutz 1983, Jablonski 1986
Paleontological Perspectives
1. lecithotrophs speciate, but also go extinct, more often
2. planktotrophs survive longer, speciate less
lecithotrophic plankto.
Hansen 1978, Science
However, these studies never calculated diversification rate:
r = speciation - extinction less dispersal may increase speciation and extinction rates, but the net difference between the two is what matters
Paleontological Perspectives
long-distance (n = 50)
short-distance (n = 50)
duration (m. y.)
%
%
Jablonski (1982, 1986) confirmed for several groups of snails that lecithotrophs have higher rates of both speciation and extinction
inferred that species selection favors lecithotrophs, because:
i) they speciate faster
ii) they accumulate in fossil record over time
Has been cited >750 times, and become a textbook example of species selection
Paleontological ProblemsStudies also did not address the fact that lecithotrophy arises in two ways: 1) when a lecithotrophic ancestor speciates, or 2) when a planktotroph undergoes character change
lecithotrophy evolves once, triggers rapid diversification
‘species-selection’hypothesis
lecithotrophy evolves 4 times from different planktotrophic ancestors; lecithotrophs don’t diversify
‘character-change’ hypothesis –accumulation w/out diversification
Paleontological Problemslong-distance (n = 50)
short-distance (n = 50)
duration (m. y.)
%
%
speciation rate () = 0.23extinction rate () = 0.17
diversification rate: (r) = = 0.06
Jablonski 1986
speciation rate () = 0.43extinction rate () = 0.34
diversification rate: (r) = = 0.09
1) minimal difference (if any...)
2) assumes all “appearances” of short- distance dispersers reflect speciation, but some must result from character change (plankto turns into lecitho)
Using sea slugs to study macroevolution
Objective: identify traits that promote diversification, using herbivorous slugs in clade Sacoglossa as a model
Using sea slugs to study macroevolution
Several facets of sacoglossan biology suggest development mode is evolutionarily free to evolve in this group:
- includes 5 of 8 species in which development mode varies within a species, due to dimorphism in egg size
- sister species often differ in development
- per-offspring investment varies widely among species, with some investing heavily in extra-capsular yolk (similar to nurse eggs)
7 10
4 gene phylogeny of Sacoglossa
- data: mtDNA: COI, 16S (1,062 bp)
nuclear: H3, 28S (1,720 bp)
- Maximum Likelihood (RaxML) - one data partition, GTR + Γ
- Bayesian Inference with 3 mixture models (BayesPhylogenies), 108 generations, 4 independent runs
- all nodes shown had >90% support (BI)
- 202 ingroup species (74 undescribed)
- developmental data for 114 spp.
Oxynoacea - 6 genera, 74 spp.
Plakobranchoidea- 4 genera, 137 spp.
(103 in Elysia)
Limapontiodea - 18 genera, 152 spp.
shelled
cerata-bearing
photosynthetic
Ancestral devel. modeinferred usingevolutionary quantitative genetics modelprobability that an ancestor had a
given type of larval dispersal
lecithotrophic
(low dispersal)
planktotrophic
(high dispersal)Limapontioidea
- more lecithotrophs in Plakobranchoidea, but only two pairs of lecithotrophic sister species
Plakobranchoidea
species-selection hypothesis predicts (a) clades of short-distance dispersers, which (b) should contain more species
NOT the case!
low dispersal
high dispersal
1. Testing for shifts in
diversification rate
Software ‘Medusa’ used to model diversification across 32 genus-level clades, using:
total # of described spp. in each genus
cryptic taxa identified via molecular species delimitation
Medusa just identifies shifts in the overall rate of diversification, not taking into account any effects of character state
Alfaro et al. 2008
1. Testing for shifts in
diversification rate
Medusa identified two branches on which the rate of diversification accelerated:
1) just after loss of the shell
- coincides with shift from ancestral host alga, Caulerpa, to diverse food sources (niche expansion)
2) after photosynthesis evolved
- 2nd increase in diversity of food sources, at the species level
Alfaro et al. 2008
1
2
2. Testing state-dependent
diversification rate
BiSSE used to model rates of speciation, extinction, and character change
Test fit of alternative models with either:
i) 2 rates, depending on larval type
or
ii) one rate, independent of larval type
Considered the three superfamilies of Sacoglossa as distinct, since they diversify at different background rates
Maddison et al. 2007, FitzJohn 2012
Speciation rate depends on larval type df ln(L) AIC χ2 P a) unrestricted BiSSE (1), (1), q (1) 9 -68.73 155.46 n/a n/a (1), (2), q (1) 12 -66.06 156.12 5.33 0.149 (2), (1), q (1) 12 -61.90 147.79 13.67 0.003 (2), (2), q (1) 15 -61.20 152.40 15.06 0.020 b) restricted BiSSE (1), (1), q (1) 9 -70.33 158.66 n/a n/a (1), (2), q (1) 12 -66.87 157.75 6.91 0.075 (2), (1), q (1) 12 -63.78 151.55 13.10 0.004 (2), (2), q (1) 15 -63.29 156.58 14.08 0.029
best-fitmodel
- model which allowed speciation rate to vary with larval type was highly preferred over model which ignored larval type
- letting extinction rate covary with larval type did not improve fit
= speciation rate
= extinction rate
q = rate of character changeKrug et al., Systematic Biology, in press
Speciation rate depends on larval type df ln(L) AIC χ2 P a) unrestricted BiSSE (1), (1), q (1) 9 -68.73 155.46 n/a n/a (1), (2), q (1) 12 -66.06 156.12 5.33 0.149 (2), (1), q (1) 12 -61.90 147.79 13.67 0.003 (2), (2), q (1) 15 -61.20 152.40 15.06 0.020 b) restricted BiSSE (1), (1), q (1) 9 -70.33 158.66 n/a n/a (1), (2), q (1) 12 -66.87 157.75 6.91 0.075 (2), (1), q (1) 12 -63.78 151.55 13.10 0.004 (2), (2), q (1) 15 -63.29 156.58 14.08 0.029
best-fitmodel
- same result whether reversals to planktotrophy were free to occur (top), or were constrained to be very rare (bottom)
But which larval type actually benefited from species selection??
Species selection favors planktotrophy
diversification rate (speciation – extinction) was always higher for planktotrophs (rP) than lecithotrophs (rL)
1. Oxynoacea: overall diversification was low, but rP was ~twice rL
rP rL q1
Oxynoacea 3.2 1.8 4.3
Limapontioidea 10.4 <0 1.1
Plakobranchoidea 26.1 10.1 9.8
plankto lecitho
Species selection favors planktotrophy
diversification rate (speciation – extinction) was always higher for planktotrophs (rP) than lecithotrophs (rL)
2. Limapontioidea: only planktotrophs diversified! (rL<0)
- lecithotrophs arose exclusively from character change
rP rL q1
Oxynoacea 3.2 1.8 4.3
Limapontioidea 10.4 <0 1.1
Plakobranchoidea 26.1 10.1 9.8
plankto lecitho
Species selection favors planktotrophy
diversification rate (speciation – extinction) was always higher for planktotrophs (rP) than lecithotrophs (rL)
3. Plakobranchoidea: high rates of overall diversification for photosynthetic clade, and frequent character change
however, rP was still ~twice rL
rP rL q1
Oxynoacea 3.2 1.8 4.3
Limapontioidea 10.4 <0 1.1
Plakobranchoidea 26.1 10.1 9.8
plankto lecitho
Are sacoglossans just weird, though?
“This is not a group that appears to have speciation rates driven by lecithotrophy: lecithotrophy is the much rarer state in this group. Presumably this is not the case for many other clades.”
“You are characterizing patterns in a single somewhat odd clade of mollusks, with relatively poor fossilization.”
- anonymous reviewer comments about this work
Are sacoglossans just weird, though?
Heterobranchia #P #L % P Anaspidea 17 2 89.5 Cephalaspidea 47 13 78.3 Notaspidea 7 3 70.0 Nudibranchia 171 60 74.0 Sacoglossa 108 35 75.5
Caenogastropoda Calyptraeidae 39 39 50.0 Conidae 56 35 61.5 Fasciolariidae 9 25 26.5 Littorininae 139 13 91.4 Muricidae 36 46 43.9 Volutidae 0 9 0.0
% of known species with planktotrophic development
outliers are some clades in Neogastropoda that have few surviving planktotrophs
...but guess who paleontological studies focused on?
Are sacoglossans just weird, though?
“This is not a group that appears to have speciation rates driven by lecithotrophy: lecithotrophy is the much rarer state in this group. Presumably this is not the case for many other clades.”
“You are characterizing patterns in a single somewhat odd clade of mollusks, with relatively poor fossilization.”
As a function of changes per branch, larval type changed about as often in Sacoglossa (0.067) as in cone snails (0.067), and less often than in slipper shells (0.176)
Thus, Sacoglossa is typical in its % of planktotrophs, and in its rate of developmental evolution
Tempo and mode of larval evolutionChanges in a trait like larval type can occur early or late in history of a group
- early change = adaptive radiation, followed by slow-down in evolution (lecithotrophy persists in the long run)
- late change = species-specific adaption occurring near tips of the tree (change is disproportionately recent)
Tempo and mode of larval evolutionChanges in a trait like larval type can occur early or late in history of a group
test: compare model fit allowing egg size to evolve across tree with vs. without Pagel’s scaling parameter < 1, most change occurs on short branches (near root of tree) = 1 (default), change in larval type equally likely anywhere on tree > 1, change in larval type gets more likely as branches get longer (most change is near tips)
Tempo and mode of larval evolutionChanges in a trait like larval type can occur early or late in history of a group
result: model BF likelihood test
= 1 -448.42
= ML value -435.46 25.9 (2.8 ± 0.2)
BF >5 = strong support for model with change concentrated near tips
larval type changes as species-specific adaptation, recently in history
Short-term solutions to a long-term problemSpecies selection favors dispersal by planktrotophic larvae in Sacoglossa, and perhaps in many or most invertebrate groups
Loss of dispersive larvae is..
i) favored at ecological timescales, so change is frequent
ii) a dead-end at macro-evolutionary timescales
Most short-distance dispersers are the Walking Dead:
lecithotrophic lineages that go extinct before they can diversify into daughter species
A trait that confers high fitness within species (individual-level) doesn’t necessarily produce evolutionary success (speciation)
1) studies of poecilogonous species (variable development) indicate planktotrophy is selected against when dispersal is unlikely to succeed due to oceanographic constraints
- Alderia willowi expresses lecithotrophy when Californian estuaries close during the dry season (Krug et al. 2012)
- C. ocellifera is lecithotrophic in enclosed Caribbean lagoons (Ellingson & Krug, in revision)
selection may be imposed by larval environments that make planktonic dispersal unlikely to succeed
Then why does lecithotrophy evolve so often?
A trait that confers high fitness within species (individual-level) doesn’t necessarily produce evolutionary success (speciation)
2) Models of correlated trait evolution revealed that increased per-offspring investment in planktotrophs increased rate at which lecithotrophy evolved in Sacoglossa (Krug et al., in press)
adult reproductive traits may impose correlated selection on larval type, which affects fecundity
Then why does lecithotrophy evolve so often?
Short-term solutions to a long-term problemSpecies selection favors:
1) self-incompatible pollen in plants
2) long-distance larval dispersal in molluscs in both cases, the derived state (selfing in plants, short-distance larvae in sea slugs) evolves frequently, but increases extinction more than speciation, so dooms that lineage
thus, what’s favored by selection in the short-term or within a species may not be an evolutionarily “winning strategy” in the long term
>1,400 citations support a hypothesis that our results indicate is wrong. Don’t believe everything you read!
Albert Rodriguez
DEB (Systematics)OCE
RyanEllingson
Thanks...
Angel ValdesCal Poly Pomona
Cynthia TrowbridgeOregon Inst. Marine Biology
Nerida WilsonAustralian Museum
Jann Vendetti
Danielle ElenaTrathen Hidalgo
Lecithotrophic
Planktotrophic
Mixed clutch
0
20
4060
80
100
1996-1997
1997-1998
Per
cen
tage
of
adu
lt p
opu
lati
on
oct nov jan feb mar apr may jun jul aug sep
020
4060
80100
oct nov jan feb mar apr may jun jul aug sep
% o
f p
opu
lati
on
feeding
non-feeding
food not there food there???San Diego
Larval type changes seasonally in A. willowi
Larval type changes seasonally in A. willowi
Feeding larvae are produced
during the rainy season in
southern California
Larval type changes seasonally in A. willowi
Feeding larvae are also
long-lived (1 month)
Good at dispersal --
travel long distances
while feeding in the ocean
Seasonal closure of Californian estuaries
Historically, mouths of Californian estuaries would close up with sand in summer, when rivers feeding the estuary dried out
Lake Earl, summer Lake Earl, winter
Seasonal closure of Californian estuaries
We now dredge the mouths of most bays to keep them open,
but local species are adapted to the old, seasonal cycle
Bataquitos Lagoon, 1989 Bataquitos, 2006