Sperm of Galeorhinus galeus (Elasmobranchii, Triakidae) Traverse an Excurrent Duct System Characterized by Pronounced Regionalization: A Scanning Electron and Light Microscopy Study

Abstract

The transport and subsequent maturation of spermatozoa in the vertebrate excurrent duct require the creation of a series of biochemically defined luminal milieus along the length of the duct. Such specialization is accomplished, among others, by changes in the epididymal histoarchitecture. Here we show that the intratesticular and extratesticular genital ducts of mating Galeorhinus galeus exhibit pronounced regionalization both in terms of epithelial histology and lumen diameter size. Findings also reveal distinct differences in the manner in which the spermatozoa were found in each segment of the duct. Novel scanning electron microscopy evidence is presented showing that the wide lumen ductuli epididymides, which ultimately convey the spermatozoa to the proximal epididymis, show functional specialization as well. The wall of the former consisted of cuboidal ciliated and nonciliated cells whose spatial arrangement in the duct wall resulted in a luminal surface showing lengthy rows of cilia-free areas, with each row bordered on both sides by a single row of cilia. The proximal epididymis comprised several subregions whose epithelial histology varied widely. The distal epididymis and ampulla of the epididymis possessed many fingerlike projections and transverse septa, respectively. As the main storage site for spermatozoa, the ampulla completed the bundling of spermatozoa into spermatozeugmata. These were circular sperm masses in which the heads of the spermatozoa were aligned side by side and embedded in a seminal matrix, while their tails extended outward. These findings of pronounced regionalization differ greatly from the rather uniform epididymal histology seen in some rays.

Development and Application of Techniques for the Control of Captive Breeding in Elasmobranchs

“…Similar aggregations of spermatozoa, when spermatozoa connected without surrounding matrix (unencapsulated), were observed in different Elasmobranchii species and called spermatozeugmata (Girard et al, 2000;Jones and Hamlett, 2002;Del Mar Pedreros-Sierra, 2015;McClusky, 2015). Clumped spermatozoa were also observed surrounded by additional structures (matrix), thus being embedded inside capsules, so-called spermatophores, and observed in several other Elasmobranchii species (Wyffels et al, 2019;Pratt and Tanaka, 1994).…”

A Comparative Study of Intratesticular Ductules in the Spermatogenically Active Testes of Shortfin Mako and Thresher Sharks

“…Interestingly, the epithelial linings and lumina of thresher shark sperm‐carrying ductules filled with sperm (as deduced from their hallmark corkscrew‐shaped heads) were both completely devoid of leukocytes (unpublished observations). This is in stark contrast to the numerous luminal leukocytes observed among leftover spermatozoa in the epididymis of the Atlantic stingray (Piercy et al, ) and soupfin shark (McClusky, ) captured in the period of reproductive inactivity. It is further worth mentioning that wandering granule‐filled leukocytes were likewise occasionally observed in the lumina of sperm passageways located immediately adjacent to meiosis‐arrested, degenerate cysts in the sexually immature Greenland shark (McClusky, Christiansen, and Nielsen, unpublished observations).…”

Andrology of shortnose guitarfish Zapteryx brevirostris (Müller & Henle, 1841) (Chondrichthyes, Trygonorrhinidae)

“…Sperm bundles are observed in the semen of many elasmobranch species (Pratt Jr & Tanaka, 1994;Wyfels et al, 2021) and may serve to minimize sperm loss during copulation, increase sperm storage efficiency in the male and female reproductive systems or preserve sperm longevity and motility during storage (Pratt Jr & Tanaka, 1994). The spermatozeugmata of Z. brevirostris are similar to the circular, matrix-containing aggregations of spermatozoa found in Heterodontus portusjacksoni (Meyer, 1793), Raja eglanteria (Bosc, 1802) and Galeorhinus galeus (Linnaeus, 1758) (Jones & Hamlett, 2006;Jones & Jones, 1982;McClusky, 2015) and markedly different from the laterally aligned sperm bundles observed in Squalus acanthias (Linneaus, 1758) and Hydrolagus colliei (Lay & Bennett, 1839) (Pratt Jr & Tanaka, 1994), or the complete envelopment of sperm by the luminal matrix to form spermatophores, as observed in Cetorhinus maximus (Gunnerus, 1765) (Matthews, 1950), Callorhynchus mili (Bory de Saint-Vincent, 1823) (Hamlett et al, 2002) and C. taurus (Wyffels et al, 2020).…”