Phylogeography of Emerita analoga (Crustacea, Decapoda, Hippidae), an eastern Pacific Ocean sand crab with long-lived pelagic larvae

Aim Phylogeographic analyses have confirmed high dispersal in many marine taxa but have also revealed many cryptic lineages and species, raising the question of how population and regional genetic diversity arise and persist in dynamic oceanographic settings. Here we explore the geographic evolution of Emerita analoga, an inter-tidal sandy beach crab with an exceptionally long pelagic larval phase and wide latitudinal, amphitropical, distribution. We test the hypothesis that eastern Pacific E. analoga constitute a single panmictic population and examine the location(s), timing and cause(s) of phylogeographic differentiation. Location Principally the eastern Pacific Ocean. Methods We sequenced cytochrome c oxidase subunit I (COI) from 742 E. analoga specimens collected between 1997 and 2000 and downloaded homologous sequences of congeners from GenBank. We reconstructed a phylogeny for Emerita species using maximum likelihood and Bayesian methods and estimated times to most recent common ancestors (TMRCAs), using a COI divergence rate of 1% Myr(-1) and timing of closure of the Central American Seaway. We constructed the COI haplotype network of E. analoga using statistical parsimony, calculated population genetic and spatial structure statistics in ARLEQUIN, and estimated the demographic history of E. analoga using Bayesian skyline analysis. Results Population subdivision and allele frequency differences were insignificant among north-eastern Pacific locations over 2000 km apart (Phi(ST) = 0.00, P = 0.70), yet two distinct phylogroups were recovered from the north-eastern and southeastern Pacific (Phi(CT) = 0.87, P < 0.001). Amphitropical differentiation of these temperate clades occurred after TMRCA 1.9 +/- 0.02 (mean +/- SE) Ma and E. analoga has expanded into its present-day north-eastern Pacific range since c. 250 ka. Main conclusions Emerita analoga is not panmictic but is very widely dispersed and approaching genetic homogeneity, i.e. 'eurymixis', in the north-eastern Pacific. North-eastern and south-eastern Pacific populations of E. analoga probably became isolated c. 1.5 Ma as the tropical eastern Pacific Ocean warmed and expanded, intensifying barriers to gene flow. The fragmentation of a widespread ancestral species previously connected by long-distance gene flow ('soft vicariance') coincident with changing oceanographic conditions may be a common theme in the evolution of Emerita species and in other highly dispersive taxa. Highly dispersive species may differentiate because of, not despite, the dynamic oceanographic setting.