Genitalia are morphologically variable across many taxa and in physical contact during intromission, but little is known about how variation in form correlates with function during copulation. Marine mammals offer important insights into the evolutionary forces that act on genital morphology because they have diverse genitalia and are adapted to aquatic living and mating. Cetaceans have a fibroelastic penis and muscular vaginal folds, while pinnipeds have a baculum and lack vaginal folds. We examined copulatory fit in naturally deceased marine mammals to identify anatomical landmarks in contact during copulation and the potential depth of penile penetration into the vagina. Excised penises were artificially inflated to erection with pressurized saline and compared with silicone vaginal endocasts and within excised vaginas in simulated copulation using high-resolution, diffusible iodine-based, contrast-enhanced computed tomography. We found evidence suggestive of both congruent and antagonistic genital coevolution, depending on the species. We suggest that sexual selection influences morphological shape. This study improves our understanding of how mechanical interactions during copulation influence the shape of genitalia and affect fertility, and has broad applications to other taxa and species conservation.
Male genital diversification is likely the result of sexual selection. Female genital diversification may also result from sexual selection, although it is less well studied and understood. Female genitalia are complex among whales, dolphins, and porpoises, especially compared to other vertebrates. The evolutionary factors affecting the diversity of vaginal complexity could include ontogeny, allometry, phylogeny, sexual selection, and natural selection. We quantified shape variation in female genitalia using 2D geometric morphometric analysis, and validated the application of this method to study soft tissues. We explored patterns of variation in the shape of the cervix and vagina of 24 cetacean species (n = 61 specimens), and found that genital shape varies primarily in the relative vaginal length and overall aspect ratio of the reproductive tract. Extensive genital shape variation was partly explained by ontogenetic changes and evolutionary allometry among sexually mature cetaceans, whereas phylogenetic signal, relative testis size, and neonate size were not significantly associated with genital shape. Female genital shape is diverse and evolves rapidly even among closely related species, consistent with predictions of sexual selection models and with findings in invertebrate and vertebrate taxa. Future research exploring genital shape variation in 3D will offer new insights into evolutionary mechanisms because internal vaginal structures are variable and can form complex spirals.
Complex foldings of the vaginal wall are unique to some cetaceans and artiodactyls and are of unknown function(s). The patterns of vaginal length and cumulative vaginal fold length were assessed in relation to body length and to each other in a phylogenetic context to derive insights into functionality. The reproductive tracts of 59 female cetaceans (20 species, 6 families) were dissected. Phylogenetically-controlled reduced major axis regressions were used to establish a scaling trend for the female genitalia of cetaceans. An unparalleled level of vaginal diversity within a mammalian order was found. Vaginal folds varied in number and size across species, and vaginal fold length was positively allometric with body length. Vaginal length was not a significant predictor of vaginal fold length. Functional hypotheses regarding the role of vaginal folds and the potential selection pressures that could lead to evolution of these structures are discussed. Vaginal folds may present physical barriers, which obscure the pathway of seawater and/or sperm travelling through the vagina. This study contributes broad insights to the evolution of reproductive morphology and aquatic adaptations and lays the foundation for future functional morphology analyses.
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