A possible highway system for the rapid delivery of sperm from the testis to the penis in the naked mole-rat, Heterocephalus glaber

Gerhard van der Horst, Sanet Kotzè, Mannus Justin O’Riain, Nolan Muller, Liana Maree

Department of Medical, Biosciences, University of the Western Cape, Bellville, South Africa; Division of Clinical Anatomy, Department of
Biomedical Sciences, Stellenbosch University, Cape Town, South Africa; Ross University School of Veterinary Medicine, Basseterre, St. Kitts, West Indies; Department of Zoology, University of Cape Town, Cape Town, South Africa; National Health Laboratory Services,
Anatomical Pathology, Tygerberg Hospital, Parow, South Africa

Abstract: Gametogenesis is suppressed in most members of the eusocial naked mole-rat (NMR) colony, while the queen selects mainly one breeding male during her life span. Recently, it was reported that the NMR testicular organization seems to produce spermatozoa on demand after suppression of spermatogenesis during most of gestation. A Sertoli cell “pump” is then used to flush the spermatozoa into short tubuli recti and simplified rete testis to reach the excurrent duct system. We hypothesize that the components of this duct system are adapted for rapid delivery of spermatozoa to the penis and for numerous copulations with the queen. Therefore, the aim was to study the ultrastructure of the male NMR reproductive duct system using light microscopy and transmission electron microscopy. The NMR rete testis gives rise to six to eight efferent tubules joining the caput epididymis. The caput epididymis resembles that of other rodents but with less distinction in terms of histological zoning. The remainder of the epididymis is considerably reduced in length compared to other rodents. In contrast, the vas deferens epithelium is highly specialized in that a vast range of vesicles, often closely associated with the spermatozoa, were visible. The large ampulla is a factory for merocrine and apocrine secretions, producing even more diverse vesicles. The transitional epithelial cells of the bladder appear to secrete abundant mucous and the penis as well as its baculum is relatively small. We speculate that these modifications strongly suggest that the excurrent duct system has been simplified and adjusted to compensate for the absence of long maturation and storage of spermatozoa. We propose that these adaptations to the NMR reproductive tract are associated with a state of degenerative orthogenesis that was selected for due to the absence of sperm competition and apparently rapid delivery of spermatozoa from the testis.

Journal of Morphology. 2021;1–21. – DOI: 10.1002/jmor.21399
Received: 12 March 2021 / Revised: 8 July 2021 / Accepted: 17 July 2021 / Published: 23 July 2021