Female genitalia can evolve more rapidly and divergently than male genitalia.
ABSTRACT: Male genitalia exhibit patterns of divergent evolution driven by sexual selection. In contrast, for many taxonomic groups, female genitalia are relatively uniform and their patterns of evolution remain largely unexplored. Here we quantify variation in the shape of female genitalia across onthophagine dung beetles, and use new comparative methods to contrast their rates of divergence with those of male genitalia. As expected, male genital shape has diverged more rapidly than a naturally selected trait, the foretibia. Remarkably, female genital shape has diverged nearly three times as fast as male genital shape. Our results dispel the notion that female genitalia do not show the same patterns of divergent evolution as male genitalia, and suggest that female genitalia are under sexual selection through their role in female choice.
Project description:The aim of this study rests on three premises: (i) humans are altering ecosystems worldwide, (ii) environmental variation often influences the strength and nature of sexual selection, and (iii) sexual selection is largely responsible for rapid and divergent evolution of male genitalia. While each of these assertions has strong empirical support, no study has yet investigated their logical conclusion that human impacts on the environment might commonly drive rapid diversification of male genital morphology. We tested whether anthropogenic habitat fragmentation has resulted in rapid changes in the size, allometry, shape, and meristics of male genitalia in three native species of livebearing fishes (genus: Gambusia) inhabiting tidal creeks across six Bahamian islands. We found that genital shape and allometry consistently and repeatedly diverged in fragmented systems across all species and islands. Using a model selection framework, we identified three ecological consequences of fragmentation that apparently underlie observed morphological patterns: decreased predatory fish density, increased conspecific density, and reduced salinity. Our results demonstrate that human modifications to the environment can drive rapid and predictable divergence in male genitalia. Given the ubiquity of anthropogenic impacts on the environment, future research should evaluate the generality of our findings and potential consequences for reproductive isolation.
Project description:In contrast to male genitalia that typically exhibit patterns of rapid and divergent evolution among internally fertilizing animals, female genitalia have been less well studied and are generally thought to evolve slowly among closely-related species. As a result, few cases of male-female genital coevolution have been documented. In Drosophila, female copulatory structures have been claimed to be mostly invariant compared to male structures. Here, we re-examined male and female genitalia in the nine species of the D. melanogaster subgroup. We describe several new species-specific female genital structures that appear to coevolve with male genital structures, and provide evidence that the coevolving structures contact each other during copulation. Several female structures might be defensive shields against apparently harmful male structures, such as cercal teeth, phallic hooks and spines. Evidence for male-female morphological coevolution in Drosophila has previously been shown at the post-copulatory level (e.g., sperm length and sperm storage organ size), and our results provide support for male-female coevolution at the copulatory level.
Project description:One of the most striking radiations in brachyuran evolution is the considerable morphological diversification of the external reproductive structures of primary freshwater crabs: the male first gonopod (G1) and the female vulva (FV). However, the lack of quantitative studies, especially the lack of data on female genitalia, has seriously limited our understanding of genital evolution in these lineages. Here we examined 69 species of the large Chinese potamid freshwater crab genus Sinopotamon Bott, 1967 (more than 80% of the described species). We used a landmark-based geometric morphometric approach to analyze variation in the shape of the G1 and FV, and to compare the relative degree of variability of the genitalia with non-reproductive structures (the third maxillipeds). We found rapid divergent evolution of the genitalia among species of Sinopotamon when compared to non-reproductive traits. In addition, the reconstruction of ancestral groundplans, together with plotting analyses, indicated that the FV show the most rapid divergence, and that changes in FV traits correlate with changes in G1 traits. Here we provide new evidence for coevolution between the male and female external genitalia of Sinopotamon that has likely contributed to rapid divergent evolution and an associated burst of speciation in this lineage.
Project description:Insect genitalia exhibit rapid divergent evolution. Truly extraordinary structures have evolved in some groups, presumably as a result of postmating sexual selection. To increase our understanding of this phenomenon, we studied the function of one such structure. The male genitalia of Callosobruchus subinnotatus (Coleoptera: Bruchinae) contain a pair of jaw-like structures with unknown function. Here, we used phenotypic engineering to ablate the teeth on these jaws. We then experimentally assessed the effects of ablation of the genital jaws on mating duration, ejaculate weight, male fertilization success and female fecundity, using a double-mating experimental design. We predicted that copulatory wounding in females should be positively related to male fertilization success; however, we found no significant correlation between genital tract scarring in females and male fertilization success. Male fertilization success was, however, positively related to the amount of ejaculate transferred by males and negatively related to female ejaculate dumping. Ablation of male genital jaws did not affect male relative fertilization success but resulted in a reduction in female egg production. Our results suggest that postmating sexual selection in males indeed favors these genital jaws, not primarily through an elevated relative success in sperm competition but by increasing female egg production.
Project description:The evolution of asymmetry in male genitalia is a pervasive and recurrent phenomenon across almost the entire animal kingdom. Although in some taxa the asymmetry may be a response to the evolution of one-sided, male-above copulation from a more ancestral female-above condition, in other taxa, such as Mammalia and Coleoptera, this explanation appears insufficient. We carried out an informal assessment of genital asymmetry across the Coleoptera and found that male genital asymmetry is present in 43% of all beetle families, and at all within-family taxonomic levels. In the most diverse group, Cucujiformia, however, genital asymmetry is comparatively rare. We also reconstructed the phylogeny of the leiodid tribe Cholevini, and mapped aspects of genital asymmetry on the tree, revealing that endophallus sclerites, endophallus, median lobe and parameres are, in a nested fashion, increasingly unlikely to have evolved asymmetry. We interpret these results in the light of cryptic female choice versus sexually antagonistic coevolution and advocate further ways in which the phenomenon may be better understood.This article is part of the themed issue 'Provocative questions in left-right asymmetry'.
Project description:The diversity of genital morphology among closely related animals with internal fertilization is well known, but the genetic backgrounds are unclear. Here, we show that, in Carabus (Ohomopterus) beetles showing correlated evolution of male and female genital parts, only a few major quantitative trait loci (QTLs) determine differences in genital dimensions between sister species, and sequence divergence is pronounced in the genomic regions containing genital QTLs. The major QTLs for male and female genital dimensions reside in different locations within the same linkage group, implying that coevolution between the sexes is only loosely constrained and can respond to sexually antagonistic selection. The same genomic regions containing the major QTLs show elevated divergence between three pairs of parapatric species with marked differences in genital parts. Our study demonstrates that species diversification can follow coevolution of genitalia between the sexes, even without tight linkage of loci affecting male and female genital dimensions.
Project description:Male genitals are highly divergent in animals with internal fertilization. Most studies attempting to explain this diversity have focused on testing the major hypotheses of genital evolution (the lock-and-key, pleiotropy, and sexual selection hypotheses), and quantifying the form of selection targeting male genitals has played an important role in this endeavor. However, we currently know far less about selection targeting female genitals or how male and female genitals interact during mating. Here, we use formal selection analysis to show that genital size and shape is subject to strong multivariate stabilizing sexual selection in both sexes of the red flour beetle, Tribolium castaneum. Moreover, we show significant sexual selection on the covariance between the sexes for specific aspects of genital shape suggesting that male and female genitalia also interact to determine the successful transfer of a spermatophore during mating. Our work therefore highlights the important role that both male and female genital morphologies play in determining mating success and that these effects can occur independently, as well as through their interaction. Moreover, it cautions against the overly simplistic view that the sexual selection targeting genital morphology will always be directional in form and restricted primarily to males.
Project description:For most arthropod species, male genital size is relatively implastic in response to variation in developmental nutrition, such that the genitals in large well-fed males are similar in size to those in small poorly-fed males. In Drosophila melanogaster, reduced nutritional plasticity of the male genitalia is a consequence of low insulin sensitivity through a tissue-specific reduction in the expression of FOXO, a negative growth regulator . Despite an understanding of the proximate developmental mechanisms regulating organ size, the ultimate evolutionary mechanisms that may have led to reduced FOXO expression in the genitalia have not been fully elucidated. Here we show that restoring FOXO activity in the developing genitalia reduces the male genital size and decreases various aspects of male reproductive success. These data support the hypothesis that sexual selection has acted on the male genitalia to limit their nutritional plasticity through a reduction in FOXO expression, linking proximate with ultimate mechanisms of genital evolution.
Project description:The diversity, variability, and apparent rapid evolution of animal genitalia are a vivid focus of research in evolutionary biology, and studies exploring genitalia have dramatically increased over the past decade. These studies, however, exhibit a strong male bias, which has worsened since 2000, despite the fact that this bias has been explicitly pointed out in the past. Early critics argued that previous investigators too often considered only males and their genitalia, while overlooking female genitalia or physiology. Our analysis of the literature shows that overall this male bias has worsened with time. The degree of bias is not consistent between subdisciplines: studies of the lock-and-key hypothesis have been the most male focused, while studies of cryptic female choice usually consider both sexes. The degree of bias also differed across taxonomic groups, but did not associate with the ease of study of male and female genital characteristics. We argue that the persisting male bias in this field cannot solely be explained by anatomical sex differences influencing accessibility. Rather the bias reflects enduring assumptions about the dominant role of males in sex, and invariant female genitalia. New research highlights how rapidly female genital traits can evolve, and how complex coevolutionary dynamics between males and females can shape genital structures. We argue that understanding genital evolution is hampered by an outdated single-sex bias.
Project description:Male genital organs are among the fastest evolving morphological structures. However, large parts of the male's genitalia are often hidden inside the female during mating. In several bushcricket species, males bear a pair of sclerotized genital appendices called titillators. By employing synchrotron-based in vivo X-ray cineradiography on mating couples, we were able to visualize titillator movement and spermatophore attachment inside the female. Titillators are inserted and retracted rhythmically. During insertion the titillator processes tap the soft and sensillae-covered dorsal side of the female's flap-like genital fold, which covers the opening of the female's genitalia, without tissue penetration. Titillators thus appear to be initially used for stimulation; later they may apply pressure that forces the female's genital fold to stay open, thereby aiding mechanically in spermatophore transfer.