Testing hypotheses of bat baculum function with 3D models derived from microCT

Abstract

The baculum (os penis) has been extensively studied as a taxon-specific character in bats and other mammals but its mechanical function is still unclear. There is a wide consensus in the literature that the baculum is probably a sexually selected character. Using a novel approach combining postmortem manipulation and threedimensional (3D) imaging, we tested two functional hypotheses in the common noctule bat Nyctalus noctula, the common pipistrelle Pipistrellus pipistrellus, and Nathusius' pipistrelle Pipistrellus nathusii: (i) whether the baculum can protect the distal urethra and urethral opening from compression during erection and copulation; and (ii) whether the baculum and corpora cavernosa form a functional unit to support both the penile shaft and the more distal glans tip. In freshly dead or frozen and thawed bats, we compared flaccid penises with artificially 'erect' penises that were inflated with 10% formalin. Penises were stained with alcoholic iodine and imaged with a lab-based high-resolution x-ray microtomography system. Analysis of the 3D images enabled us to compare the changes in relative positions of the baculum, corpora cavernosa, urethra, and corpus spongiosum with one another between flaccid and 'erect' penises. Our results support both functional hypotheses, indicating that the baculum probably performs two different roles during erection. Our approach should prove valuable for comparing and testing the functions of different baculum morphologies in bats and other mammals. Moreover, we have validated an essential component of the groundwork necessary to extend this approach with finite element analysis for quantitative 3D biomechanical modeling of penis function.

The baubellum is more developmentally and evolutionarily labile than the baculum

“…There is even some speculation that engorgement of the clitoris alters access to the female's reproductive tract, and without it copulation cannot occur (Lönnberg, 1902; Steel, 1885). In males, engorgement of the penis can lead to changes in the orientation of the baculum, probably the result of hydrostatic pressure in the corpora cavernosa pressing against the baculum (Herdina et al., 2015; Kelly, 2000). The stiffening of the corpus cavernosa in the clitoris might have similar effects on the baubellum, which again might shed light on its potential role during copulation.…”

Postcopulatory sexual selection influences baculum evolution in primates and carnivores

“…Ensuring that the urethra is unrestricted and there is as little distance as possible for sperm to travel is a way of increasing the amount of sperm transported to the cervical canal. The baculum serves as a supportive structure during prolonged intromission, both protecting the urethra and preventing it from being constricted [14]. …”

Diffusible iodine‐based contrast‐enhanced computed tomography (diceCT): an emerging tool for rapid, high‐resolution, 3‐D imaging of metazoan soft tissues

“…; Cox & Faulkes, ; Herdina et al. ,b). Nonetheless, specimen treatments, including freezing prior to fixation, choice of fixation agent, and fixation process, can significantly affect staining outcomes (see details in ‘Reporting standards’ below).…”

“…; Gignac & Kley, ; Tsai & Holliday ; Herdina et al. ), and 4% paraformaldehyde (Metscher, ; Degenhardt et al. ; Wong et al.…”

“…; Cox & Faulkes, ; Herdina et al. ,b; Li & Clarke, in press). Exemplar images and 3‐D renderings demonstrating the impressive taxonomic range and anatomical detail captured through use of this approach are illustrated in Figs and .…”