Patrick J. Krug California State University, Los Angeles Challenging a textbook case of species selection: Does loss of dispersal make evolutionary winners,

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...?


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


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


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


populationconnectivity

gene flow

local adaptation

speciation rate

extinction risk

ancestrallecithotroph



demographicconnectivity

gene flow

local adaptation

speciation rate

extinction risk

populationsdiverge...




gene flow

local adaptation

speciation rate

extinction risk

theory and genetic data suggest lecithotrophic populations will split and diverge into new species...




gene flow

local adaptation

speciation rate

extinction risk

theory and pop-gen data suggest lecithotrophic populations will split and divergence into new species...




gene flow

local adaptation

speciation rate

extinction risk

...but may also go extinct more often


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


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


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



2. Limapontioidea: only planktotrophs diversified! (rL<0)

- lecithotrophs arose exclusively from character change

rP rL q1




plankto lecitho



3. Plakobranchoidea: high rates of overall diversification for photosynthetic clade, and frequent character change

however, rP was still ~twice rL

rP rL q1




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


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?


“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)


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)


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


Feeding larvae are produced

during the rainy season in

southern California


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

Documents

Patrick J. Krug California State University, Los Angeles Challenging a textbook case of species selection: Does loss of dispersal make evolutionary winners,