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

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

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 K2P COI

Synapta maculata

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

Actinopyga obesa complex

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

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

1.Two deeply divergent clades: A & B sympatric on 8 island groups 2.30 ESUs so far 3.Pigmentation separates major and minor clades. Astralium rhodostomum complex

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

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

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