Anatomical evidence for the epididymis as the prime mover in the evolution of the scrotum

Extensive investigation of the sensitivity of the descended testis to abdominal temperature, and of its thermo-regulation by the scrotum, has so far failed to explain the adaptive significance of the scrotal state. The present viewpoint, derived primarily from comparative anatomical and from experimental studies, suggests a different line of reasoning – that descent into a scrotum has been influenced primarily by the need for migration of the cauda epididymidis to this cooler location; testicular descent is seen as a merely mechanistic event which enables the cauda epididymidis to project from the body, but has no significance for the biological function of the testis as such. The possibility that some advantage derived by the sperm-storage region of the epididymis has been a prime determinant in the evolution of the scrotum is suggested by at least three anatomical features. This is indicated firstly by the relationship of testis and cauda epididymidis to each other in cryptorchid and in scrotal species. In natural cryptorchids (e.g., many insectivores and hystricomorph rodents) which express the transitional stage in testicular descent, the cauda generally precedes the testis within the cremasteric sac, thereby lying closest to the integument. In the scrotum, the disposition of the cauda epididymidis ensures that it occupies the coolest site there also. A second consideration concerns the curious course traced by the Wolffian duct in cryptorchid and scrotal mammals; for its diversionary route along and beyond the border of the testis would seem illogical and unnecessary were descent into a scrotum related solely to the function of the testis. This U-shaped disposition of the duct, which retraces its course from the acute flexure of the cauda, is seen here as a device which permits the cauda epididymidis to occupy a cooler site, whether this be subintegumental or scrotal. Thirdly, although evidenced to different degrees and not in all species, a variety of scrotal features, e.g., a circumscribed hormonally-determined baldness, exaggerated dartos responsitivity and, occasionally, black pigmentation of the peri-caudal surface, as well as the presence of a fat pad between cauda and testis, each appear to favor controlled cooling of the caudal epididymidis. In no animal, by contrast, does the form of the scrotum and the disposition of its content seem designed for preferential cooling of the testis. These considerations do not explain the adaptive significance of the scrotum or the reasons for its variable occurrence among mammals. However, with a few exceptions found particularly amongst marine mammals, a scrotum characterizes polygynous species in which a dominant male achieves all or most of the fertile matings in a large group, and also those known to engage in multiple ejaculatory coitus with one female. Conversely, our limited knowledge of their habits notwithstanding, the frequency of sexual interaction for the males of most ascrotal species would appear to be relatively low. In light of its suggested relationship to the function of the cauda epididymidis, the possibility is raised that the scrotal state may be linked to the sexual capacity of the male, in particular the ability to produce fertile ejaculates repeatedly within a limited period of time.