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

Abstract

The study of male genital diversity has long overshadowed evolutionary inquiry of female genitalia, despite its nontrivial diversity. Here, we identify four nonmutually 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/conflict 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.

Correlated divergence of female and male genitalia in replicated lineages with ongoing ecological speciation

“…The genitalia of both sexes exhibited convergent evolution along replicated environmental gradients, and differences in genital morphologies were maintained in laboratory‐raised males and females from one population pair. Overall, our results add to a growing body of work suggesting that divergence in genital traits has the potential to contribute to reproductive isolation at early stages of speciation (Langerhans ; Anderson and Langerhans ). Assessing the importance of mechanical isolation during ecological speciation in the future requires an extension of the pattern‐based approaches employed to date, explicitly identifying the mechanisms driving genital evolution and exploring the functional significance of variation in genital traits for insemination and fertilization in both intra‐ and interpopulation matings.…”

“…; Heinen‐Kay and Langerhans ; Heinen‐Kay et al. ; Anderson and Langerhans ). Ecological sources of selection—like predation—can directly impact genital traits, especially when there are functional trade‐offs that affect other aspects of organismal performance or fitness (Langerhans et al.…”

“…). Few studies have explicitly investigated patterns of genital evolution during early stages of the speciation process (Heinen‐Kay and Langerhans ; Anderson and Langerhans ; Barnard et al. ).…”

“…; Evans et al. ; Anderson and Langerhans ) and among species (Peden ; Langerhans ), has long prompted speculation that genital trait variation might enhance reproductive isolation between lineages of poeciliid fishes via genital incompatibilities (Langerhans ; Anderson and Langerhans ). Nonetheless, only one study (Anderson and Langerhans ) tested for the correlated evolution of female and male genitalia during early stages of speciation.…”

The role of ecology, neutral processes and antagonistic coevolution in an apparent sexual arms race

“…Recent studies have supported a role for ecological variation in population‐level sexually antagonistic evolution in laboratory ( Drosophila melanogaster fruit flies; Arbuthnott et al . ) and field settings (Bahamas mosquitofish, Gambusia hubbsi ; Anderson & Langerhans ). Our results therefore add to a growing body of evidence suggesting the potential for ecological influence of sexual arms races across systems.…”