Data from: 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 stronger postmating female choice/choice when predators are present, but greater premating female choice in their absence. Our results additionally supported the lock-and-key hypothesis, uncovering a pattern of reproductive character displacement for genital shape. We found no support for the sexual conflict or female choice hypotheses. Our results demonstrate a strong role for ecology in generating female genital diversity, and suggest that lock-and-key may provide a viable cause of female genital diversification.

长期以来，针对雄性生殖器多样性的研究掩盖了雌性生殖器演化研究的关注度，尽管雌性生殖器本身具有不容忽视的多样性。本研究明确了四种非互斥的机制，这些机制可驱动雌性生殖器分化，并可能催生雌雄生殖器协同演化的模式：1. 生态变异改变性选择的作用情境，即生态假说（ecology hypothesis）；2. 性拮抗选择，即性冲突假说（sexual-conflict hypothesis）；3. 由雌性生殖器性状介导的对雄性生殖器的雌性偏好，即雌性选择假说（female-choice hypothesis）；4. 针对种群间交配的选择压力，即锁钥假说（lock-and-key hypothesis）。本研究以栖息于捕食风险各异的蓝洞中的巴哈马食蚊鱼为模式系统，对上述四种假说开展了实证检验。研究结果明确支持生态假说：在存在肉食性鱼类的蓝洞中，雌性个体的生殖器开口更小。这与以下情形相符：当捕食者存在时，雌性的交配后选择作用更强；而在捕食者缺失时，雌性的交配前选择作用更强。此外，本研究结果还支持锁钥假说，揭示了生殖器形状存在生殖特征替代（reproductive character displacement）的模式。本研究未发现支持性冲突假说与雌性选择假说的证据。本研究结果证实了生态因子在塑造雌性生殖器多样性中发挥的重要作用，并表明锁钥假说或许可成为雌性生殖器多样化的合理解释。