Evolutionary success is unevenly distributedEcological success is measured as population growth rate - how fast does one population grow, compared to others?

Microevolutionary success is measured as fitness – how many of your offspring survive to reproductive age?

Macroevolutionary success equals clade biodiversity, or number of surviving species in a clade

- typical animal phyla have ~5,000 species (=spp.)

- lineages below the phylum level with >5,000 spp. are thus unusually successful

Identifying characteristics that make one lineage especially successful is a major goal of evolutionary biology

populations species lineages(clades of species)

microevolution macroevolution

- genetic drift- natural selection- migration

allelefrequencies reproductive

isolation

How do _____ evolve?

adaptation

diversification

why do some groupshave more species

than related groups?

one commonancestor

2 daughter lineages,of equal age

clade of 3 extant species (surviving today)

1 surviving species

Evolutionary success = number of living species

Why does one lineage diversify into many more species than its less-successful sister lineage?

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 is unevenly distributed among sister clades?

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. (including marine members)

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

Some lineages undergo adaptive radiations, filling all available ecological niches and diversifying into many species

1) opportunity: ancestor colonized an empty habitat with many unoccupied niches...

- went from marine into terrestrial + freshwater habitats

- got onto an empty continent, early

- survived mass extinction of dominant competitors

2) specialization: when related species exploit different ecological niches (i.e., food or host), many related species can co-exist in one place without competing

3) key innovation: evolution of a trait that allows exploitation of new niches, or greater competitive ability

Some lineages undergo adaptive radiations, filling all available ecological niches and diversifying into many species

4) evolved a trait that promotes rapid speciation:- sexual signaling or mating system- strong host or habitat association- tendency to get allopatrically isolated (dispersal)- fast-evolving gamete recognition proteins

5) being biogeographically widespread – meaning, some member species are distributed across different regions and biomes across the globe - lineage is more likely to survive local wipe-outs, and global mass extinction events

Evolutionary success is unevenly distributed

shift in rate ofdiversification(speciation - extinction)

- thus, either of two things can lead to a lineage diversifying more:

1) increase in speciation rate ()

2) decrease in extinction rate ()

Rabosky 2014

Diversification rate of a lineage (r) is the net difference between speciation (new spp. born) and extinction (existing spp. vanish)

r =

Evolutionary success is unevenly distributed

shift in rate ofdiversification(speciation - extinction)

- thus, either of two things can lead to a lineage diversifying more:

1) increase in speciation rate ()

2) decrease in extinction rate ()

Rabosky 2014

Diversification rate of a lineage (r) is the net difference between speciation (new spp. born) and extinction (existing spp. vanish)

r =

Evolutionary success is unevenly distributed

key innovationevolves, sets off burst of diversification

1) 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 is the net difference between speciation (new spp. born) and extinction (existing spp. vanish)

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

Why only 2 Bosellia but 134 plakos?

- flat sea slugs

- eat one algal genus

- tropical only

134 species in clade Plakobranchidae...

- parapodia (sides of body rolled up) may protect stored chloroplasts from too much sun (possible key innovation?)

- each species feeds on just one of >20 kinds of algae (specialized)

- species live and mate on their host (host choice may promote speciation)

Candidate key innovation: antifreeze proteins

9 species, non-Antarctic (no anti-freeze)

123 species, Antarctic - anti-freeze glycoproteins

One group of fish diversified in the Antarctic after evolving anti-freeze glycoproteins, allowing them to survive water temperatures below freezing

- within Antarctic, species also diversified into benthic (bottom) and pelagic (open water) forms

- again, however, only happened once so hard to test hypothesis

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

Identifying trait-dependent diversification

= speciation rate

From a model-fitting perspective, the question is:

Does a model with two different speciation rates (one for state “blue”, one for “red”) fit the data better than a default model with the same speciation rate for both states?

Goldberg et al. 2008, Science

Species selection in plants

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. 2008, 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

- that’s 1/12th the number of citations of the discovery of PCR!

Paleontological Perspectives

short-distance long-distance

Hansen 1978, Science

65 million years ago

each vertical line is a species,showing where it 1st appearedin the fossil record, and when itdisappeared (went extinct)

Paleontological Perspectives

1. short-distance dispersers speciate more often, but survive for short periods

2. long-distance dispersers survive for longer, but speciate less

lecithotrophic plankto.

Hansen 1978, Science

However, these studies never calculated diversification rate:

r = speciation - extinction short-distance 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 >450 times, and become a textbook example of species selection

Paleontological ProblemsStudies also did not address the fact that short-distance migration arises in two ways: 1) when a short-distance ancestor speciates, or 2) when a long-distance species undergoes character change

short-distance dispersal evolves once, triggers rapid diversification

‘species-selection’hypothesis

short-distance evolves 4 times from different long-distance ancestors; short-distance species don’t diversify

‘character-change’ hypothesis –accumulation w/out diversification

Paleontological Problemsi) studies did not factor in rates of character change

ii) paleontological studies never calculated diversification rate

short-distance may increase both speciation and extinction rates, but it is the net difference between the two that matters

speciation rate ()

extinction rate ()

diversification rate (r), the rate at which a lineage accumulates species (the measure of evolutionary success)

r = net gain in species over time

Paleontological Problemsi) studies did not factor in rates of character change

ii) paleontological studies never calculated diversification rate

short-distance may increase both speciation and extinction rates, but it is the net difference between the two that matters

extinction rate ()

speciation rate ()

r = 2

r = 1

both and go up, yet r decreases

long-distance short-distance

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 (long turns into short)

Using sea slugs to study macroevolution

Objective: identify traits that promote diversification, using herbivorous slugs in clade Sacoglossa as a model

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

short-distance

long-distance

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!

short-distance

long-distance

1. Testing for shifts in

diversification rate

Software ‘Medusa’ used to model diversification across 32 genus-level clades, using total # of known spp.

Medusa identifies shifts in the overall rate of diversification, not taking into considerating character state

two branches where rate of diversification accelerated:

1) after loss of shell

2) after photosynthesis evolved

Alfaro et al. 2008

1

2

We then modeled rates of speciation, extinction, and change between long- and short-distance larvae

Tested whether data better fit a model in which rates depended on larval dispersal, or if ignoring larval type fit the data just as well

Considered the three superfamilies of Sacoglossa as distinct, since they diversify at different background rates

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 changeMaddison et al. 2007, FitzJohn 2012

Species selection favors planktotrophy

diversification rate (speciation – extinction) was always higher for long-distance (rP) than short-distance (rL) dispersers

most short-distance dispersers arose recently by character change, when a long-distance species evolved into a short- distance species

rP rL q1

Oxynoacea 3.2 1.8 4.3

Limapontioidea 10.4 <0 1.1

Plakobranchoidea 26.1 10.1 9.8

long- short-distance distance

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

Short-term solutions to a long-term problemSpecies selection favors long-distance dispersal in Sacoglossa, and perhaps (probably?) in 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:

short-lived lineages that go extinct before they can diversify into daughter species

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!