Variability and asymmetry in the shape of the spiny dogfish vagina revealed by 2D and 3D geometric morphometrics

Abstract

Genital structures are among the most variable in nature and have been suggested to evolve at exceptionally high rates. However, the vast majority of research on genital morphology has been done on male genitalia. We present one of the few studies of female genital shape using geometric morphometrics, and the first of such studies to employ 3D geometric morphometrics, using the spiny dogfish shark, a taxon for which reproductive biology is well‐studied. In a sample of 21 adult females, we found no correlation between body size and reproductive and non‐reproductive trait size, and therefore no general allometric patterns. Furthermore, we found limited evidence for different 2D and 3D vaginal shapes in visibly pregnant and not visibly pregnant sharks, but trends were more obvious in 3D than 2D. We found high congruence between data derived using 2D geometric morphometrics with that derived from 3D methods. We also found exceptionally high asymmetry in the vagina, again more apparent in 3D than in 2D. Visibly pregnant sharks had especially high directional asymmetry (>48% of total variation) likely as a result of an asymmetric distribution of pups in the shark's paired oviducts. Therefore, this asymmetry was functional rather than developmental and presents an important consideration when studying vaginal shape. The lack of significant association between pregnancy and vaginal shape in a species with an extremely long pregnancy suggests that vaginal shape differences may be under additional selective forces such as sexual antagonism during copulation. A combination of 3D geometric morphometric methods along with assessments of asymmetry sheds further light on the growing appreciation that female genitalia is highly variable in shape and may play a substantial role in sexual selection.

How flat can a horse be? Exploring 2D approximations of 3D crania in equids

“…Thus, unlike for instance (Hedrick et al, 2019), who reported important differences in 2D versus 3D results (e.g., in asymmetric changes, as well as group differences, found only in 3D), we reached almost identical conclusions on patterns of ventral cranial variation in equids using either 2D or 3D analyses. This seems paradoxical given the clearly non-negligible differences in the fine details of inter-individual shape variation (the modest matrix correlations, large R 2 s of 2D-3D differences, and the inaccuracies in phenograms, that we mentioned above).…”

“…Indeed, he found that, although repeatability of 2D data was high for the symmetric component of shape, variability in a specimen orientation introduced important differences in patterns of asymmetric variation in basis capituli of three species of ticks. That asymmetric variation, even when large, may be particularly affected by 2D analyses of pictures, was also suggested by a recent study (Hedrick et al, 2019). The authors employed slightly different landmark configurations to capture the shape of dog-fish vaginas both in 2D and 3D.…”

“…Can we, therefore, conclude that TTD is problematic only when measuring small amounts of biological variation? Some of the research summarized in the Introduction suggests potential problems even with macroevolutionary analyses (e.g., (Buser et al, 2018;Hedrick et al, 2019)). In our work too, although TTD improves at supra-specific level, it is still large especially if judged in terms of the not so high correlations between shape matrices (ca.…”

Asymmetric and Spiraled Genitalia Coevolve with Unique Lateralized Mating Behavior

“…To characterize and quantify genital shape and assess the influence of asymmetry on overall genital shape, we used two-dimensional geometric morphometrics (2DGM) and three-dimensional models of male and female harbor porpoise genitalia. Asymmetry has been previously reported in female genitalia in a wide range of taxa, but can be inconspicuous when present [3][4][5]13,24 . Therefore, we examined the pattern of asymmetry in vaginal folds in both 2D and 3D by generating models of the vaginal lumen, in addition to assessing gross morphology.…”

The evolution of female genitalia

“…In these taxa, the lengths of the female common and separate spermathecal ducts are highly divergent among 17 species, and the length of the common spermathecal duct has coevolved with the genital process of males (Kotrba et al, 2014). Several other studies have found similar patterns of female genital diversity and coevolutionary variation between female and male genitalia (Breed, Leigh, & Speight, 2013;Genevcius, Caetano, & Schwertner, 2017;Hedrick, Natanson, Brennan, Antalek-Schrag, & Conith, 2019;Horton & Lewis, 2011;Ilango & Lane, 2000;Ishikawa, 1987;Yoshizawa, Ferreira, Kamimura, & Lienhard, 2014).…”