Glans inflation morphology and female cloaca copulatory interactions of the male American alligator phallus†

Abstract

The phallic glans of the American alligator (Alligator mississippiensis) is the distal termination of the semen-conducting sulcus spermaticus and during copulation has the closest, most intimate mechanical interactions with the female urodeum, the middle cloacal chamber that contains the opening to the vaginal passages and oviducts. However, the details of this interface leading to insemination and gamete uptake are unclear. Here we: 1) Histologically characterize the underlying tissue types and morphologically quantify the shape changes associated with glans inflation into the copulatory conformation, 2) Digitally reconstruct from MRI the 3D shape of functional tissue compartments, and 3) diceCT image the copulatory fit between male phallus and female cloaca. We discuss these results in relation to tissue type material properties, the transfer on intromittent forces, establishing potential copulatory lock, inflated glans volume scaling with body mass/length, the mechanics of semen targeting and insemination, and potential female cryptic choice impacting multiple clutch paternity. In part, this study further clarifies the phallic morphological variation observed among crocodylians and begins to investigate the role(s) these divergent male forms play during copulation interacting with female cloacal forms to increase reproductive success.

Genital anatomy and copulatory interactions in the broad snouted Caiman (Caiman latirostris)

“…The shaft is anchored to a thick tendon originating on the ischium that acts as a fixed point around which the male phallus rotates when it is everted for copulation via cloacal muscle contraction (Kelly, 2013). Both the sulcus spermaticus and the distal end of the phallus contain spongiform erectile tissue that inflates with blood to close the sulcal groove (Moore & Kelly, 2015) and produce species‐specific glans morphology (Moore et al, 2016; Moore et al 2020,b; Moore et al, 2021). The shaft contains a core of dense, collagenous tissue that does not change shape during vascular inflation (Kelly, 2013; Moore et al, 2021); this tissue maintains a high resistance to bending that is likely to facilitate intromission through the female vent (Kelly, 2016).…”

“…Positions of male and female genital tissues during copulation in crocodylians have only been examined in A. mississippiensis (Moore et al, 2021). In this species, the distal end of the phallus enters the distal portion of the female urodeum during intromission, to the level of the vaginal tracts.…”

“…In this species, the distal end of the phallus enters the distal portion of the female urodeum during intromission, to the level of the vaginal tracts. In all crocodylians, the sulcus spermaticus terminates at the glans tip, the most distal point of the phallus, and may either put semen into close contact with a vaginal opening or, as in A. mississippiensis , insert semen directly into the vaginae (Moore et al, 2021). In ex vivo manipulations, the enlarged male glans cannot pass through the female vent, therefore inflation likely occurs after the phallus is positioned inside the female (Moore et al, 2021).…”