Signatures of seaway closures and founder dispersal in the phylogeny of a circumglobally distributed seahorse lineage

BACKGROUND: The importance of vicariance events on the establishment of phylogeographic patterns in the marine environment is well documented, and generally accepted as an important cause of cladogenesis. Founder dispersal (i.e. long-distance dispersal followed by founder effect speciation) is also frequently invoked as a cause of genetic divergence among lineages, but its role has long been challenged by vicariance biogeographers. Founder dispersal is likely to be common in species that colonize remote habitats by means of rafting (e.g. seahorses), as long-distance dispersal events are likely to be rare and subsequent additional recruitment from the source habitat is unlikely. In the present study, the relative importance of vicariance and founder dispersal as causes of cladogenesis in a circumglobally distributed seahorse lineage was investigated using molecular dating. A phylogeny was reconstructed using sequence data from mitochondrial and nuclear markers, and the well-documented closure of the Central American seaway was used as a primary calibration point to test whether other bifurcations in the phylogeny could also have been the result of vicariance events. The feasibility of three other vicariance events was explored: a) the closure of the Indonesian Seaway, resulting in sister lineages associated with the Indian Ocean and West Pacific, respectively; b) the closure of the Tethyan Seaway, resulting in sister lineages associated with the Indo-Pacific and Atlantic Ocean, respectively, and c) continental break-up during the Mesozoic followed by spreading of the Atlantic Ocean, resulting in pairs of lineages with amphi-Atlantic distribution patterns. RESULTS: Comparisons of pairwise genetic distances among the seahorse species hypothesized to have diverged as a result of the closure of the Central American Seaway with those of published teleost sequences having the same distribution patterns show that the seahorses were among the last to diverge. This suggests that their cladogenesis was associated with the final closure of this seaway. Although two other divergence events in the phylogeny could potentially have arisen as a result of the closures of the Indonesian and Tethyan seaways, respectively, the timing of the majority of bifurcations in the phylogeny differed significantly from the dates of vicariance events suggested in the literature. Moreover, several divergence events that resulted in the same distribution patterns of lineages at different positions in the phylogeny did not occur contemporaneously. For that reason, they cannot be the result of the same vicariance events, a result that is independent of molecular dating. CONCLUSION: Interpretations of the cladogenetic events in the seahorse phylogeny based purely on vicariance biogeographic hypotheses are problematic. We conclude that the evolution of the circumglobally distributed seahorse lineage was strongly influenced by founder dispersal, and suggest that this mode of speciation may be particularly important in marine organisms that lack a pelagic dispersal phase and instead disperse by means of rafting.