Testing comparative phylogeographic models of marine vicariance and dispersal using a hierarchical Bayesian approach

Background: Marine allopatric speciation is an enigma because pelagic larval dispersal can potentially connect disjunct populations thereby preventing reproductive and morphological divergence. Here we present a new hierarchical approximate Bayesian computation model (HABC) that tests two hypotheses of marine allopatric speciation: 1.) "soft vicariance", where a speciation involves fragmentation of a large widespread ancestral species range that was previously connected by long distance gene flow; and 2.) peripatric colonization, where speciations in peripheral archipelagos emerge from sweepstakes colonizations from central source regions. The HABC approach analyzes all the phylogeographic datasets at once in order to make across taxon-pair inferences about biogeographic processes while explicitly allowing for uncertainty in the demographic differences within each taxon-pair. Our method uses comparative phylogeographic data that consists of single locus mtDNA sequences from multiple co-distributed taxa containing pairs of central and peripheral populations. We use the method on two comparative phylogeographic data sets consisting of cowrie gastropod endemics co-distributed in the Hawaiian (11 taxon-pairs) and Marquesan archipelagos (7 taxon-pairs). Results: Given the Marquesan data, we find strong evidence of simultaneous colonization across all seven cowrie gastropod endemics co-distributed in the Marquesas. In contrast, the lower sample sizes in the Hawaiian data lead to greater uncertainty associated with the Hawaiian estimates. Although, the hyper-parameter estimates point to soft vicariance in a subset of the 11 Hawaiian taxon-pairs, the hyper-prior and hyper-posterior are too similar to make a definitive conclusion. Both results are not inconsistent with what is known about the geologic history of the archipelagos. Simulations verify that our method can successfully distinguish these two histories across a wide range of conditions given sufficient sampling. Conclusion: Although soft vicariance and colonization are likely to produce similar genetic patterns when a single taxon-pair is used, our hierarchical Bayesian model can potentially detect if either history is a dominant process across co-distributed taxon-pairs. As comparative phylogeographic datasets grow to include > 100 co-distributed taxon-pairs, the HABC approach will be well suited to dissect temporal patterns in community assembly and evolution, thereby providing a bridge linking comparative phylogeography with community ecology.