Observations on the anterior testicular ducts in snakes with emphasis on sea snakes and ultrastructure in the yellow‐bellied sea snake, Pelamis platurus

Abstract

The anterior testicular ducts of squamates transport sperm from the seminiferous tubules to the ductus deferens. These ducts consist of the rete testis, ductuli efferentes, and ductus epididymis. Many histological and a few ultrastructural studies of the squamate reproductive tract exist, but none concern the Hydrophiidae, the sea snakes and sea kraits. In this study, we describe the anterior testicular ducts of six species of hydrophiid snakes as well as representatives from the Elapidae, Homolapsidae, Leptotyphlopidae, and Uropeltidae. In addition, we examine the ultrastructure of these ducts in the yellow-bellied Sea Snake, Pelamis platurus, only the third such study on snakes. The anterior testicular ducts are similar in histology in all species examined. The rete testis is simple squamous or cuboidal epithelium and transports sperm from the seminiferous tubules to the ductuli efferentes in the extratesticular epididymal sheath. The ductuli efferentes are branched, convoluted tubules composed of simple cuboidal, ciliated epithelium, and many species possess periodic acid-Schiff+ granules in the cytoplasm. The ductus epididymis at the light microscopy level appears composed of pseudostratified columnar epithelium. At the ultrastructural level, the rete testis and ductuli efferentes of P. platurus possess numerous small coated vesicles and lack secretory vacuoles. Apocrine blebs in the ductuli efferentes, however, indicate secretory activity, possibly by a constitutive pathway. Ultrastructure reveals three types of cells in the ductus epididymis of P. platurus: columnar principal cells, squamous basal cells, and mitochondria-rich apical cells. This is the first report of apical cells in a snake. In addition, occasional principal cells possess a single cilium, which has not been reported in reptiles previously but is known in some birds. Finally, the ductus epididymis of P. platurus differs from other snakes that have been studied in possession of apical, biphasic secretory vacuoles. All of the proximal ducts are characterized by widening of adjacent plasma membranes into wide intercellular spaces, especially between the principal cells of the ductus epididymis. Our results contribute to a larger, collaborative study of the evolution of the squamate reproductive tract and to the potential for utilizing cellular characters in future phylogenetic inferences.

Ductuli efferentes of the male Golden Syrian hamster reproductive tract

“…Consistent with this physiological activity, the basolateral plasma membranes show extensive interdigitations and often dilated intercellular spaces in the proximal ductules of some species (Goyal & Williams, 1988; Holmes & Gist, 2004; Ilio & Hess, 1992; Jones & Jurd, 1987; Pudney & Fawcett, 1984; Ramos & Dym, 1977; Sever & Freeborn, 2012). …”

“…He described the tubules as being very thin and “coiled individually from side to side”. Since then, efferent ductules have been described in more than 20 different mammalian (Hess, 2002; Ilio & Hess, 1994) and numerous nonmammalian vertebrate species (Guerrero et al ., 2004; Hernandez-Franyutti & Uribe, 2012; Hess et al ., 1976; Holmes & Gist, 2004; Rheubert et al ., 2010; Sever & Freeborn, 2012). Efferent ductules transport spermatozoa from rete testis to the epididymis.…”

Observations on variation in the ultrastructure of the proximal testicular ducts of the ground skink, scincella lateralis (reptilia: Squamata)

“…The accuracy of staining was shown by simultaneously staining portions of the kidney in which the sexual segment was PAS+ and BB+ and the proximal convoluted tubules AB+ as reported by Sever and Hopkins (2005). Squamates examined in previous studies have all shown a reaction, especially in the ductus epididymis, to neutral carbohydrates and/or proteins, often stronger for one product than the other (Dufaure and Saint Girons, 1984; Sever and Freeborn, 2012).…”

“…Ultrastructural descriptions of the testicular ducts of lizards are limited to Calotes versicolor (Meeran et al, 2001) and Sitana ponticeriana (Akbarsha et al, 2006a, b, 2007) of the Agamidae, Lacerta (= Zootoca) vivipara (Mesure et al, 1991) and Podarcis sicula (Desantis et al, 2002) of the Lacertidae, Tropidurus itambere (Ferreira et al, 2009) of the Tropiduridae, and Hemidactylus turcicus (Rheubert et al, 2010) of the Gekkonidae. For snakes, ultrastructure of the testicular ducts has been described for Seminatrix pygaea of the Natricidae (Sever, 2004, 2010), Agkistrodon piscivorus of the Viperidae (Siegel et al, 2009; Trauth and Sever, 2011), Pantherophis obsoletus of the Colubridae (Trauth and Sever, 2011), and Pelamis platurus of the Elapidae (Sever and Freeborn, 2012).…”

Observations on the Sexual Segment of the Kidney of Snakes with Emphasis on Ultrastructure in the Yellow‐Bellied Sea Snake, Pelamis platurus

“…In this article, we use a sample of snakes similar to that used in a recent study on histology and ultrastructure of the anterior testicular ducts of snakes (Sever and Freeborn, 2012). We include eight species from the Elapidae, a cosmopolitan group of some 350 venomous species with fixed front fangs and which includes terrestrial and marine forms (Burbrink and Crother, 2011).…”