Spinner dolphin ecotypes are divergent at a Y chromosome marker but not conventional mtDNA or autosomal markers

Abstract

The spinner dolphin (Stenella longirostris) contains six ecotypes (four recognized as subspecies) that exhibit striking differences in morphology, habitat, and mating system, despite having adjacent or overlapping ranges and little genetic differentiation at neutral markers. The enigma of morphological divergence in the face of genetic homogeneity is a challenge to both evolutionary theory and management of spinner dolphins. Management issues are especially prominent in the Eastern Tropical Pacific, where four of the six ecotypes occur, and where populations have failed to recover from depletions caused by the tuna fishery. To explore the relationship between phenotypic and genetic divergence within this species, we examined phylogeographic structure within and between all six described ecotypes across the species range (n=270, 17 geographic locations) using mtDNA control region, mtDNA cytochrome b, a nuclear intron, and a Y chromosome intron. Genetic analyses of mtDNA and autosomal markers revealed low levels of differentiation (most pairwise FST values less than 0.1) between ecotypes and geographic regions, concordant with previous studies indicating recent or ongoing gene flow. In contrast, Y intron analyses revealed fixed differences between the three most divergent ecotypes/subspecies defined by morphology, ecology, and behavior (S.l. longirostris vs. S.l. roseiventris vs. S.l. orientalis/S.l. centroamericana/Tres Marias ecotype). Another ecotype (whitebelly), previously postulated to be a hybrid between the two phenotypically most divergent ecotypes, had Y haplotypes from both putative parent ecotypes, supporting a hybrid designation. These Y chromosome results provide the first evidence of strong genetic divergence that corresponds with the phenotypic partitions observed in spinner dolphins. We propose that this genetic divergence reflects selective sweeps resulting from divergent selection on the Y chromosome for spinner dolphins in different habitats, despite ongoing interbreeding. These results demonstrate that loci under selection can aid in both the delineation of stock structure and the understanding of evolutionary pathways.