Testicular Histology Reveals a Novel Type of Spermatogenesis in Pseudobranchus axanthus (Caudata: Sirenidae)
We examined the testicular histology of 32 adult male
Pseudobranchus axanthus
collected at Rainey Slough (Glades County), Florida, during 1974–76. The process of spermatogenesis was evident throughout all regions of the testes and appeared to occur year-round. The testes contain numerous, spherical-to-oblong testicular lobules that vary greatly in size. Unlike all other salamanders, which exhibit cystic spermatogenesis along with a caudo-cephalic wave of maturing cell types (leading to spatial and temporal segregation of germ cells), spermatogenesis in
P. axanthus
lacks testicular cysts. Instead, the testicular lobules possess an assortment of different spermatogenic cell stages, all arising from primary spermatogonia through mitotic and meiotic divisions, thus creating a germ cell/Sertoli cell syncytium along the lobular epithelium. Secondary spermatocytes then detach from the lobular epithelium and from their accompanying Sertoli cells and undergo spermiogenesis within the lumen. We propose naming this new type of germ cell development non-cystic lobular spermatogenesis. Upon maturation, sperm travel from the lobular lumen into a longitudinal testicular canal via an intratesticular duct. The testicular canal conveys sperm to about 15 vasa efferentia, which then connect to genital renal capsules. Sperm move through the renal tubules and eventually reach the Wollfian duct. This duct transports sperm to the cloaca.
Body morphology and testicular anatomy of adult male Pseudobranchus axanthus. (A) Left lateral view of dissected adult male (USNM 289387; 86 mm SVL) collected 8 February 1976. (B) Ventral view of male in A revealing position of testes in lower pleuroperitoneal cavity. (C) Longitudinal section of testes of adult male (USNM 289202; 91 mm SVL; collected 26 July 1975) showing histology, including numerous oval lobules scattered throughout. Lt, left testis; Pc, precava; Rt, right testis.
Testis/genital kidney complex in Pseudobranchus axanthus. (A) Transverse section revealing basic anatomical structures, including genital convoluted tubule (Gct), genital nephron (Gn), genital neck segment (Gns), genital renal corpuscle (Grc), postcava (Pc), testicular canal (Tc), testicular lobule (Tl), vas efferens (Ve), and Wolffian duct (Wd). (B) Longitudinal section through the complex showing various structures in A, including dorsal aorta (Da) and glomerulus (Gl). Scale bar in A the same for B.
Longitudinal sections of representative testes of four adult Pseudobranchus axanthus collected on 4 November 1974 (A, USNM 289106), 28 March 1975 (B, USNM 289173), 26 July 1975 (C, USNM 289193), and 20 September 1975 (D, USNM 289261).
Transverse sections of progressive spermatogenic stages from representative testes of four adult Pseudobranchus axanthus collected on 20 September 1975 (A–D, USNM 289226), 2 January 1975 (E and G, USNM 289147), 26 July 1975 (F, USNM 289202), and 28 March 1975 (H, USNM 289173). (A) Black arrowheads point to bed of primary spermatogonia within the testicular stroma. Black arrows point to Sertoli cells. Scale bar in A is the same from B–D and F–H. (B) Black arrowhead points to group of mitotically dividing primary spermatogonia within an expanding testicular lobule. (C) Black arrows point to Sertoli cell nuclei lying within a luminal cell ring interior to basally positioned secondary spermatogonia (black arrowheads; to the right is an advanced lobule containing germ cells undergoing spermiogenesis). (D) Testicular lobule exhibiting primary spermatocytes (white arrowhead), secondary spermatocytes (white arrow) and some spermiogenic sperm. Detachment from the basement membrane can be seen in some of the cells. (E) Ring of secondary spermatocytes (white arrows) completely detached from the basement membrane. (F) Three advanced testicular lobules undergoing spermiogenesis. One lobule (lower left) is releasing sperm and cellular debris into an intratesticular duct (gray arrowhead). (G) Gray arrows points to mature sperm within lobule exhibiting late stage spermiation. (H) Exhausted lobules with cellular debris. A few cells (presumably Sertoli cells) lie along the basement membrane (black arrows).
Consecutive transverse sections (10-micron thick sections) of the testis/genital kidney complex of an adult Pseudobranchus axanthus (USNM 289124) collected 17 December 1974. Scale bar in A the same for B–F. The testicular canal (Tc) connects with a vas efferens (Ve; follow Tc from A to F). The Ve empties into a genital kidney renal corpuscle (Grc; follow Ve from F to A). At the point where the Ve merges with the Grc, a genital kidney neck segment (Gns) branches from the Ve (follow Gns from F to B). Intratesticular ducts (It) can be seen merging with the Tc following It from C to F.
Contributor Notes
Associate Editor: M. J. Lannoo.