Origins of female genital diversity: predation risk and lock-and-key explain rapid divergence during an adaptive radiation

The study of male genital diversity has long overshadowed evolutionary inquiry of female genitalia, despite its non-trivial diversity. Here we identify four non-mutually exclusive mechanisms that could lead to genital divergence in females, and potentially generate patterns of correlated male-female genital evolution: (1) ecological variation alters the context of sexual selection (“ecology hypothesis”), (2) sexually antagonistic selection (“sexual-conflict hypothesis”), (3) female preferences for male genitalia mediated by female genital traits (“female-choice hypothesis”), and (4) selection against inter-population mating (“lock-and-key hypothesis”). We performed an empirical investigation of all four hypotheses using the model system of Bahamas mosquitofish inhabiting blue holes that vary in predation risk. We found unequivocal support for the ecology hypothesis, with females exhibiting a smaller genital opening in blue holes containing piscivorous fish. This is consistent with stron...