Oceanographic heterogeneity influences an ecological radiation in elasmobranchs

Aim: During ecological speciation, reproductive isolation is predicted to evolve between populations adapted to different biotic or abiotic environments despite the absence of geographical isolation. Regions of oceanographic heterogeneity (e.g. current interfaces, habitat transition zones, ecological gradients) are strong candidates for the presence of ecologically divergent natural selection, but their role in the radiation of elasmobranch species is yet to be tested. We used an integrative framework to assess the relative influence of oceanographic heterogeneity and geological history on the diversification of an elasmobranch genus. Location: Gulf of California (GC) and Baja California Peninsula (BCP), Mexico. Taxon: Shovelnose guitarfish (genus Pseudobatos). Methods: We sampled 210 Pseudobatos specimens from four distinct but physically connected oceanographic regions within the GC and in the BCP. We used genetic (mtDNA sequences and AFLP genotypes) and environmental (six oceanographic variables) datasets to clarify phylogenetic relationships, demographic history and evolutionary divergence among populations, and to test for associations between ecologically driven selection and reproductive isolation. Results: Phylogenetic and population genetic evidence exposed five distinct lineages of Pseudobatos in the region, including four cryptic lineages in the GC. Phylogeographic analyses indicate a recent history of ecologically driven diversification associated with the Gulf's young oceanographic environment and its four ecologically discrete regions. This hypothesis was supported by seascape genetics, ecological niche modelling and by tests of selection. Main conclusions: We propose an adaptive radiation for the genus Pseudobatos linked with habitat heterogeneity of the GC. Our study likely represents the first assessment of an ecological radiation in the highly diverse elasmobranch group. It capitalizes on the environmental and biogeographic settings of the GC to offer a new perspective about the application of integrative approaches to study divergent natural selection and diversification in the sea.