No abstract

The rapid divergence of genital morphology is well studied in the context of sexual selection and speciation; however, little is known about the developmental mechanisms underlying divergence in genitalia. Ground beetles in the subgenus Ohomopterus genus Carabus have species‐specific genitalia that show coevolutionary divergence between the sexes. In this study, using X‐ray microcomputed tomography, we examined the morphogenesis of male and female genitalia in two closely related Ohomopterus species with divergent genital morphologies. The morphogenetic processes generating the male and female genitalia at the pupal stage were qualitatively similar in the two species. The male aedeagus and internal sac and female bursa copulatrix were partially formed at pupation and developed gradually thereafter. The species‐specific genital parts, male copulatory piece, and female vaginal appendix differed in the timing and rate of development. The relatively long copulatory piece of Carabus maiyasanus began to develop earlier, but subsequent rates of growth were similar in the two species. The timing of the formation of the vaginal appendix and initial growth rates were similar, but subsequent rapid growth led to a longer vaginal appendix in C. maiyasanus. Thus, substantial interspecific differences in the size of genital parts were mediated by different underlying developmental mechanisms between the sexes (i.e., a shift in the developmental schedule in males and a change in growth rate in females). These results revealed the spatio–temporal dynamics of species‐specific genital structure development, providing a novel platform for evo–devo studies of the diversification of genital morphologies.

Natural selection against maladaptive interspecific reproductive interactions may cause greater divergence in mating traits between sympatric populations than between allopatric populations in a pair of species, known as reproductive character displacement (RCD) which is evidence for the lock-and-key hypothesis of genital evolution. However, the relative importance of various processes contributing to RCD in genital morphology (e.g. reinforcement, reproductive interference, and population filtering or the Templeton effect) is not clear. Here, we examined hypotheses for RCD in genital morphology, with a special focus on the Templeton effect (which predicts that only highly differentiated populations can exist in sympatry). We examined population-level fitness costs in interspecific mating between Carabus maiyasanus and Carabus iwawakianus with RCD in genital morphology. A mating experiment using populations with various degrees of RCD in genital morphology showed no evidence for consistently lower interspecific mating costs in C. maiyasanus populations in contact with displacement in genital morphology than in remote populations, contrary to the predictions of the Templeton effect. Alternatively, interspecific mating costs varied among populations. Observed relationships between the sizes of genital parts concerning isolation and interspecific mating costs across populations suggested that population-level fitness costs do not necessarily decrease during the process leading to RCD. Our results provide insight into ecological and evolutionary processes during secondary contact in closely related species.

1. The timing and frequency of female mating are important determinants of male reproductive success. Elucidating reproductive phenology is crucial to understand the evolution of mating behaviour and mating systems.2. Mate encounter rate is a key variable for understanding the evolutionary consequences of sexual cannibalism. However, remarkably little is known about female mating frequency in wild populations in mantids, charismatic insects that exhibit sexual cannibalism. 3. The authors examined the reproductive phenology of a wild population of the sexually cannibalistic praying mantid Tenodera angustipennis, and paid special attention to female mating frequency. 4. Field surveys throughout two reproductive seasons were combined with survival model analysis to estimate the phenology of eclosion, adult sex ratio, female first mating, and oviposition, allowing quantification of time windows for reproductive maturation and female mating.5. Genetic paternity analysis using newly developed microsatellite markers revealed that females mated with two to six males on average before oviposition in the wild.6. The results provide a comprehensive record of the reproductive phenology and female mating frequency in a wild mantid population, and insight into the evolution of male mating behaviour under sperm competition and sexual cannibalism.

The evolution of exaggerated sexual traits may be possible by the relaxation of various constraints on exaggeration. Functional constraints refer to the reduced performance of exaggerated traits per se or increased survival costs by holding the exaggerated traits. Genetic constraints, such as genetic correlations or pleiotropy, may hinder the independent evolution and exaggeration of traits. Structural constraints, such as competition for space and resources among traits, may require the coordination of the exaggerated trait with surrounding structures. The remarkable diversity of male genital morphology provides an ideal opportunity for examining constraints on sexual trait exaggeration. In this study, we addressed the constraints on the evolution of exaggerated male genital morphology based on a comparative analysis of phenotypic covariation between the genitalia and other body parts using Ohomopterus ground beetles. We found that exaggerated male genitalia were related to a relaxation of functional constraint, as revealed by a steeper allometric slope in the species with exaggerated male genitalia. By contrast, genetic constraint based on a shared genetic basis for the male genitalia and other appendages may have little effect on diversification in male genitalia. Structural constraints were strongest in the species with the most exaggerated male genitalia, suggesting that the observed constraint was a result of exaggeration. These findings improve our understanding of sexual trait exaggeration and underlying constraints.