The Evolution of Reproductive Divergence in the Sea

Understanding how speciation occurs in the ocean is challenging because the high dispersal potential of marine larvae, and the scarcity of absolute physical barriers to their dispersal, suggest that gene flow should slow or prevent the evolution of divergence among populations. However, spatial heterogeneity in gene flow and localized sexual selection are two potential drivers of divergence among marine populations. Here I investigate how gene flow and sexual selection contribute to reproductive divergence in a coastal seastar with a long larval pelagic phase, Patiria miniata. I first use microsatellite markers to assess genetic population structure across the species range along the west coast of North America, and find a genetic disjunction near the central coast of British Columbia consistent with two hypotheses about the effects of historical climate events and contemporary gene flow. I next use an oceanographic dispersal model to assess the extent to which variation in larval dispersal can account for this structure. I find that oceanographic features predict the genetic structure observed better than dispersal distance between populations alone. Given this genetic structure, I next test the hypothesis that fertilization proteins of this broadcast spawner have diversified among the two (northern and southern) populations, as predicted under a hypothesis of sexual conflict. My findings reveal divergent, positive selection in the sperm protein bindin, which suggest that sexual selection has lead to localized divergence at this fertilization compatibility gene. Finally, I test fertilization compatibility between males and females as a function of population source and male bindin genotype. I find that localized coevolution has occurred in the southern population, and that southern females have a greater affinity than northern females for male bindin genotypes found in the south. Together, these findings provide evidence that patterns in larval dispersal and sexual selection can lead to reproductive divergence in a marine species in spite of its high dispersal potential. Characterizing both genetic structure and adaptive molecular evolution among populations is a powerful approach for understanding incipient speciation in the sea.