Sexual selection paves the road to sexual isolation during ecological speciation

Background: Divergent natural selection between ecologically different environments often drives speciation. An unanswered question concerns the importance of sexual selection in generating sexual isolation during this process. We illustrate that four distinct mechanisms can drive sexual isolation: (I) divergent sexual selection, (II) uniform sexual selection, (III) intrapopulation assortative mating, and (IV) divergent mate recognition signals. Currently, we lack empirical studies designed to disentangle their relative importance in the wild. Question: What is the relative importance of the four mechanisms in generating sexual isolation during ecological speciation in the post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi)? Organisms: Bahamas mosquitofish (Gambusia hubbsi) from five inland blue holes on Andros Island, the Bahamas (three without predatory fish, two with predatory fish). Prior work has demonstrated replicated evolution of adaptive phenotypes in the different predation regimes, with strong sexual isolation between divergent predation regimes that is associated with body shape differences between populations. Methods: We conducted a mate-choice experiment using video animations to test for withinpopulation mating preferences for male body shape. Holding all other traits constant, we digitally manipulated body shapes of animations to present each female with two subtly different options: (1) a male with a relatively streamlined body shape (10% confidence limit for the female’s respective population along a multivariate morphological axis), and (2) a male with a relatively large mid-body/caudal region (corresponding 90% confidence limit). These shapes mirror the differences observed between predation regimes, but only utilize within-population variation. Results and conclusions: We found that divergent within-population mating preferences (not any other mechanism) explain observed patterns of sexual isolation between populations. Male body shape and female preference for male body shape have co-evolved across populations, resulting in sexual isolation between divergent predatory environments. In combination with previous research, this study reveals that divergent natural and sexual selection on body shape between predation regimes has incidentally increased reproductive isolation as a by-product.