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Causes & consequences of shifts in larval type: Reconsidering the role of dispersal in evolutionary processes Patrick J. Krug California State University, Los Angeles Evolutionary success is unevenly distributed Major goal of macroevolutionary studies: explain why some groups are more species-rich than others 3 spp. Can we identify the traits that explain why biodiversity is unevenly distributed among sister clades? 60 spp. 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 Woo-hoo! **Winners** colonizing dry land led to explosive radiations in many groups beetles: 350,000 spp. named (probably >1 million) Pulmonata: land / freshwater snails + slugs ~60,000 spp. (including marine members) vertebrates: ~45,000 spp. 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” sharks + rays: top marine predators cephalopods: pinnacle of invertebrate vision & intelligence Evolutionary success is unevenly distributed Diversification rate of a lineage (r) is the net difference between speciation (new spp. born) and extinction (existing spp. vanish) - thus, either of two things can lead to a lineage diversifying more: 1) increase in speciation rate (l) shift in rate of diversification (speciation extinction) Rabosky 2014 2) decrease in extinction rate (m) r=l-m Evolutionary success is unevenly distributed Diversification rate of a lineage (r) is the net difference between speciation (new spp. born) and extinction (existing spp. vanish) - thus, either of two things can lead to a lineage diversifying more: 1) increase in speciation rate (l) shift in rate of diversification (speciation extinction) Rabosky 2014 2) decrease in extinction rate (m) r=l-m Evolutionary success is unevenly distributed Diversification rate of a lineage is the net difference between speciation (new spp. born) and extinction (existing spp. vanish) 1) key innovation may lead to an adaptive radiation into many new ecological niches key innovation evolves, sets off burst of diversification Rabosky 2014 problem: typically a one-time event, not naturally replicated 2 living species of Bosellia - flat sea slugs - eat one algal genus - tropical only 134 species in 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 Rabosky & McCune 2010 Comparative methods can identify such traits 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) Rabosky & McCune 2010 - unrelated to fitness within species Identifying trait-dependent diversification l = 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? Species selection in plants Flowering plants repeatedly evolved self-compatible pollen, allowing selffertilization, from selfincompatible pollen (cannot self-fertilize) Selfing Non-selfing Goldberg et al. 2008, Science 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.. selfing non-selfing diversification rate (r) Goldberg et al. 2008, Science Species selection in plants In 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 selfing non-selfing diversification rate (r) Marine larval type and dispersal marine invertebrates produce microscopic larvae that swim for short periods (0 - 5 days) or long periods (>30 days) Planktotrophy lecithotrophy long-distance dispersal short-distance dispersal Consequences of long-distance dispersal planktotrophy lecithotrophy population connectivity gene flow local adaptation speciation rate extinction risk planktotrophic populations remain connected over evolutionary timescales Evolutionary consequences of larval type planktotrophy population connectivity gene flow local adaptation speciation rate extinction risk ancestral lecithotroph lecithotrophy Evolutionary consequences of larval type planktotrophy demographic connectivity gene flow local adaptation speciation rate extinction risk populations diverge... lecithotrophy Evolutionary consequences of larval type planktotrophy lecithotrophy demographic connectivity 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 demographic connectivity 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 demographic connectivity 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 Shuto 1974, Hansen 1978, 1980, 1982, Jablonski & Lutz 1983, Jablonski 1986 Six studies, cited >1,400 times, concluded lecithotrophs diversify more than planktotrophs, so benefit from species selection - that’s 1/12th the number of citations of the discovery of PCR! Paleontological Perspectives lecithotrophs planktotrophs each vertical line is a species, showing where it 1st appeared in the fossil record, and when it disappeared (went extinct) 65 million years ago Hansen 1978, Science Paleontological Perspectives lecithotrophic plankto. 1. lecithotrophs speciate, but also go extinct, more often 2. planktotrophs survive longer, speciate less However, these studies never calculated diversification rate: r = speciation - extinction Hansen 1978, Science 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) 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 % duration (m. y.) Has been cited >750 times, and become a textbook example of species selection Paleontological Problems Studies 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 ‘species-selection’ hypothesis short-distance dispersal evolves once, triggers rapid diversification ‘character-change’ hypothesis – accumulation w/out diversification short-distance evolves 4 times from different long-distance ancestors; short-distance species don’t diversify Molecular phylogenetics & development Phylogenies of diverse invertebrate groups show many independent gains of lecithotrophy, often with little subsequent diversification slipper shells: - 23 origins of lecithotrophy - 1 reversal to planktotrophy - only one radiation (8 spp.) Collin 2004 Paleontological Problems i) 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 (l) diversification rate (r), the rate at which a lineage accumulates species (the measure of evolutionary success) extinction rate (m) r = net gain in species over time Paleontological Problems i) 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 (l) planktotrophs lecithotrophs? r=1 r=2 extinction rate (m) both l and m go up, yet r decreases Paleontological Problems long-distance (n = 50) % speciation rate (l) = 0.23 extinction rate (m) = 0.17 diversification rate: (r) = l - m = 0.06 short-distance (n = 50) speciation rate (l) = 0.43 extinction rate (m) = 0.34 diversification rate: (r) = l - m = 0.09 % 1) minimal difference (if any...) duration (m. y.) Jablonski 1986 2) assumes all “appearances” of shortdistance 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 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) 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. shelled Limapontiodea - 18 genera, 152 spp. cerata-bearing Plakobranchoidea - 4 genera, 137 spp. (103 in Elysia) photosynthetic short-distance long-distance Ancestral devel. mode Limapontioideainferred using evolutionary quantitative probability genetics that an model ancestor had given type of larval dispersal a short-distance long-distance Plakobranchoidea - more lecithotrophs in Plakobranchoidea, but only two pairs of lecithotrophic sister species species-selection hypothesis predicts (a) clades of short-distance dispersers, which (b) should contain more species NOT the case! 1. Testing for shifts in diversification rate Software ‘Medusa’ used to model diversification across 32 genus-level clades, using total # of known spp. 1 Medusa identifies shifts in the overall rate of diversification, not taking into considerating character state 2 two branches where rate of diversification accelerated: 1) after loss of shell 2) after photosynthesis evolved Alfaro et al. 2008 2. Testing state-dependent diversification rate BiSSE used to model rates of speciation, extinction, and character change Tested fit of alternative models with: a) 2 rates, depending on larval type or b) 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 a) unrestricted BiSSE l (1), m (1), q (1) l (1), m (2), q (1) l (2), m (1), q (1) l (2), m (2), q (1) df ln(L) AIC χ2 P 9 12 12 15 -68.73 -66.06 -61.90 -61.20 155.46 156.12 147.79 152.40 n/a 5.33 13.67 15.06 n/a 0.149 0.003 0.020 best-fit model b) restricted BiSSE l- (1), m (1),which q (1) allowed 9 -70.33 158.66 n/a vary n/a model speciation rate to with larval type l (1), m (2), q (1) preferred 12 -66.87 157.75 which 6.91 ignored 0.075 larval type was highly over model l (2), m (1), q (1) 12 -63.78 151.55 13.10 0.004 l (2), m (2), q (1) 15 -63.29 156.58 14.08 0.029 - letting extinction rate covary with larval type did not improve fit l = speciation rate m = extinction rate q = rate of character change Krug et al., Systematic Biology, in press Speciation rate depends on larval type df ln(L) AIC χ2 P a) unrestricted BiSSE l (1), m (1), q (1) l (1), m (2), q (1) l (2), m (1), q (1) l (2), m (2), q (1) 9 12 12 15 -68.73 -66.06 -61.90 -61.20 155.46 156.12 147.79 152.40 n/a 5.33 13.67 15.06 n/a 0.149 0.003 0.020 b) restricted BiSSE l (1), m (1), q (1) l (1), m (2), q (1) l (2), m (1), q (1) l (2), m (2), q (1) 9 12 12 15 -70.33 -66.87 -63.78 -63.29 158.66 157.75 151.55 156.58 n/a 6.91 13.10 14.08 n/a 0.075 0.004 0.029 best-fit model - 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 plankto rP Oxynoacea Limapontioidea Plakobranchoidea 3.2 10.4 26.1 lecitho rL 1.8 <0 10.1 q1 4.3 1.1 9.8 diversification rate (speciation – extinction) was always higher for planktotrophs (rP) than lecithotrophs (rL) 1. Oxynoacea: overall diversification was low, but rP was ~twice rL Species selection favors planktotrophy plankto rP Oxynoacea Limapontioidea Plakobranchoidea 3.2 10.4 26.1 lecitho rL 1.8 <0 10.1 q1 4.3 1.1 9.8 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 Species selection favors planktotrophy plankto rP Oxynoacea Limapontioidea Plakobranchoidea 3.2 10.4 26.1 lecitho rL 1.8 <0 10.1 q1 4.3 1.1 9.8 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 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 Anaspidea Cephalaspidea Notaspidea Nudibranchia Sacoglossa #P 17 47 7 171 108 #L 2 13 3 60 35 %P 89.5 78.3 70.0 74.0 75.5 Caenogastropoda Calyptraeidae Conidae Fasciolariidae Littorininae Muricidae Volutidae 39 56 9 139 36 0 39 35 25 13 46 9 50.0 61.5 26.5 91.4 43.9 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 evolution Changes in a trait like larval type can be: a) strongly affected by phylogenetic relationships – close relatives tend to share similar traits - a pre-requisite for species selection to favor lecithotrophy is that it must be heritable at the species level - i.e., lecithotrophs must give rise to daughter species that are also lecithotrophic Tempo and mode of larval evolution Changes in a trait like larval type can be: a) strongly affected by phylogenetic relationships – close relatives tend to share similar traits test: compare model fit allowing egg size to evolve across tree with vs. without Pagel’s scaling parameter l - reflects the expected covariance of close relatives, who should have similar egg sizes l= 0, relatives aren’t similar in egg size l = 1, relatives share egg size (larval type) Tempo and mode of larval evolution Changes in a trait like larval type can be: a) strongly affected by phylogenetic relationships – close relatives tend to share similar traits result: l= 0 l= ML value (0.38 ± 0.18) model likelihood -428.14 BF test -428.01 0.25 BF <2 means, no support for model that corrects for relatedness relatives are not similar in larval type Tempo and mode of larval evolution Changes in a trait like larval type can: b) occur early or late in history of a group - early change = adaptive radiation, followed by slow-down in evolution - late change = species-specific adaption occurring near tips of the tree (change is disproportionately recent) Tempo and mode of larval evolution Changes in a trait like larval type can: b) 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 d d < 1, most change occurs on short branches (near root of tree) d = 1 (default), change in larval type equally likely anywhere on tree d > 1, change in larval type gets more likely as branches get longer (most change is near tips) Tempo and mode of larval evolution Changes in a trait like larval type can: b) occur early or late in history of a group result: d=1 d = ML value (2.8 ± 0.2) model likelihood -448.42 BF test -435.46 25.9 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 problem Species selection favors long-distance dispersal in Sacoglossa, and perhaps 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 Then why does lecithotrophy evolve so often? 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 Short-term solutions to a long-term problem Species 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! Thanks... Jann Vendetti DEB (Systematics) OCE Ryan Ellingson Diane Rico Cynthia Trowbridge Oregon Inst. Marine Biology Julia Vo Angel Valdes Cal Poly Pomona Nerida Wilson Australian Museum Danielle Trathen Elena Hidalgo Albert Rodriguez