Integrative taxonomy Gustav Paulay Florida Museum of Natural

Integrative taxonomy Gustav Paulay Florida Museum of Natural History University of Florida

BSC and ESU • Biological species concept – No gene flow – Independent evolutionary tracks – Reproductive isolation – Tested experimentally or sympatric • Evolutionary Significant Unit – No gene flow – Independent evolutionary tracks – Untested for reproductive isolation, allopatric

Speciation • Formation of species • Requires isolation of two populations leading to no/little mating between them • Leads to divergence of populations • Divergence of genotype • Mutations – changes in DNA • Fixation of mutations: – Genetic drift or selection • Mutations accumulate – interbreeding becomes impossible – or leads to poor hybrids – speciation

ESU: demonstrate lack of gene flow • Defined as reciprocally monophyletic populations – i. e. fixed for different traits

ESU: demonstrate lack of gene flow • Reciprocally monophyletic in at least independent 2 traits

ESU: 2 independent traits • Any two independent traits w/ genetic basis • Morphological characters • Genetic characters – Independent loci (mt. DNA – all one) • Geography • Any combination of these

Integrative taxonomy • Use of multiple lines of evidence • Field - museum - lab • Ecology - behavior - morphology - genetics - geography • Distinguishing between morphs and species • Two or more independent characters showing distinction between species

Integrative taxonomy: Actinopyga mauritiana - guamensis

Two major types of challenges • Not seeing species where there are • Seeing species where there aren’t • Cause: rate of evolution varies among traits – phenotype: morphology, behavior, color pattern. . . – genotype: sequence divergence – reproductive isolation

Not seeing species where there are • unequal rates of evolution – phenotype divergence - SLOW – sequence divergence – reproductive isolation • cryptic species

Cukes vs. primates • Different foci for sensory perception • Humans – visual cues • Cukes - chemical cues • Do cukes care about each other’s colors or ossicles when meeting?

Supposed distribution of Scutellastra flexuosa and exusta Powell, 1968

but what is really going on. . . NJ K 2 P COI

Synapta maculata

Not seeing species where there are • unequal rates of evolution – phenotype divergence – sequence divergence – reproductive isolation - FAST

Actinopyga obesa complex

Echinometra mathaei complex Rapid secondary sympatry Facilitated by rapid evolution of fertilization proteins? COI ~1 Ma Bindin COI Landry et al. 2003 Proc Roy Soc

Seeing species where there aren’t • • ecophenotypic variation ontogenetic variation geographic variation ecological variation - depth, habitat, etc polymorphism paralogous loci former divergence now united

Polymorphism / phenotypic variation

Paralogous loci: mitochondrial genes gone nuclear in Alpheus Williams & Knowlton 2001 Mol Biol Evol

ESU vs. BS • Need demonstration of no possibility for reuniting into one species • No problem when sympatric as gene flow is tested • Can’t assume reproductively isolated in allopatry – need test experimentally – mating essays

Cypraea tigris a species differentiated, then united • 15% divergence in COI • Type A – Indian only • Type B – mostly Pacific – some Indian • A and B in Indian identical in all other characters

BS test – marginal overlap

ESU - reciprocal monophyly • DNA - gene flow - BSC • reciprocal monophyly implies lack of recent genetic connections • need several samples of each form to test • reliability of conclusion depends on depth of intra- vs. inter-specific variation • in sympatry - separate biological species • in allopatry - separate ESUs, species status subjective

Where are the species limits?

Lack of reciprocal monophyly • morphs rather than species • distinct species, but: – introgression – insufficient time for sorting • deep coalescent • rapid speciation

Introgression in Astralium

Introgression in Bohadschia argus? • Unusual form only in W Pacific; never seen in Polynesia, etc. • Need compare independent markers to test

Insufficient time for sorting Gene trees vs. species trees: coalescence theory Avise 1999 Phylogeography

Evolution of reproductive isolation • Slow – most gastropod – deep divergence among allopatric ESUs – clear reciprocal monophyly – slow to secondary sympatry / biological species • Rapid – echinoids, holothuroids – shallow divergence among sympatric species – potential paraphyletic species – rapid to secondary sympatry / biological species

Astralium rhodostomum complex 1. 2. 3. Two deeply divergent clades: A & B sympatric on 8 island groups 30 ESUs so far Pigmentation separates major and minor clades.

Persistence of allopatry - Cypraeidae 94% divergences < 10 Ma retain allopatry (115 of 122) 94% divergences < 10 Ma retain signal (115 of 122) Geographic signal no signal

Echinometra mathaei complex Rapid secondary sympatry Facilitated by rapid evolution of fertilization proteins? COI ~1 Ma Bindin COI Landry et al. 2003 Proc Roy Soc

Stichopus variegatus complex

Advantages of sequence data • • Directly test genetic connections Very large number of characters Independent markers - independent sources “Independent” of morphology - so can trace evolution of form, etc on gene tree without circularity

Potential problems with sequence data • depth of coalescent vs. interspecific divergence • paralogous sequences • introgression – selective sweeps – homogenization through drift