Spermatogenesis in nonmammalian vertebrates

Abstract

Spermatogenesis appears to be a fairly conserved process throughout the vertebrate series. Thus, spermatogonia develop into spermatocytes that undergo meiosis to produce spermatids which enter spermiogenesis where they undergo a morphological transformation into spermatozoa. There is, however, variation amongst the vertebrates in how germ cell development and maturation is accomplished. This difference can be broadly divided into two distinct patterns, one present in anamniotes (fish, amphibia) and the other in amniotes (reptiles, birds, mammals). For anamniotes, spermatogenesis occurs in spermatocysts (cysts) which for most species develop within seminiferous lobules. Cysts are produced when a Sertoli cell becomes associated with a primary spermatogonium. Mitotic divisions of the primary spermatogonium produce a cohort of secondary spermatogonia that are enclosed by the Sertoli cell which forms the wall of the cyst. With spermatogenic progression a clone of isogeneic spermatozoa is produced which are released, by rupture of the cyst, into the lumen of the seminiferous lobule. Following spermiation, the Sertoli cell degenerates. For anamniotes, therefore, there is no permanent germinal epithelium since spermatocysts have to be replaced during successive breeding seasons. By contrast, spermatogenesis in amniotes does not occur in cysts but in seminiferous tubules that possess a permanent population of Sertoli cells and spermatogonia which act as a germ cell reservoir for succeeding bouts of spermatogenic activity. There is, in general, a greater variation in the organization of the testis and pattern of spermatogenesis in the anamniotes compared to amniotes. This is primarily due to the fact there is more reproductive diversity in anamniotes ranging from a relatively unspecialized condition where gametes are simply released into the aqueous environment to highly specialized strategies involving internal fertilization. These differences are obviously reflected in the mode of spermatogenesis and this is particularly true of the stage of spermiogenesis where the morphology of the species-specific spermatozoon is determined. Moreover, unlike amniotes, many anamniotes display a spermatogenic wave manifest, depending upon the species, either at the level of the cyst or seminiferous lobule. This variation in the organization of the testis makes certain anamniotes perfect models for investigating germ cell development and maturation. For instance, the presence of a spermatogenic wave provides an opportunity to manually isolate discrete germ cell stages for analysis of specific Sertoli/germ cell interactions. Furthermore, for many anamniotes, germ cells mature in association with a morphologically poorly developed Sertoli cell. This seeming independence of Sertoli cell regulation allows the in vitro culture of isolated germ cells of some species of anamniotes through several developmental stages. Thus, due either to the anatomical organization of the testis, or structural simplicity of the germinal units, nonmammalian vert...

Stage and season effects on cell cycle and apoptotic activities of germ cells and Sertoli cells during spermatogenesis in the spiny dogfish (Squalus acanthias)

“…Within the aborted M-PrM cysts, spermatogonia coalesce to form multinucleate giant cells, a phenomenon probably facilitated by the opening or dissolution of the intercellular bridges between germ cells (Pudney 1995). The multinucleate giant cells are eventually phagocytosed by the Sertoli cells over a period of 10 months after which the ZD cysts are resorbed in the epigonal organ, a lymphomyeloid organ associated with the mature surface of the testis.…”

“…Studies primarily in adult rodents indicate that, of the numerous regulatory mechanisms present within the testis, density-dependent (De Rooij 2001, Tadokoro et al 2002 and hormone-controlled (Meachem et al 1999, Allan et al 2004) mechanisms are two of the major physiological regulators that control these processes in an age-dependent and spermatogonial-stage-dependent manner. In addition, data obtained from organ cultures of immature rodent testes indicate that developing Sertoli cells influence the cellpopulation dynamics of gonocytes, and undifferentiated and differentiated spermatogonia, and their further maturation, depending on the age of the Sertoli cell (Boitani et al 1993, 1995, Zhou et al 1993, De Rooij & Van Dissel-Emiliani 1997, Schlatt et al 1999. Our knowledge of the inter-relationships between the different stages of spermatogonia and the various stages of Sertoli cell development in vivo is incomplete.…”

Differences between male and female growth and sexual maturation in tilapia (oreochromis mossambicus)

“…the stage of development during which an individual becomes capable of reproducing sexually, it is characterized by an activation of the brain-pituitary gonadal (BPG) axis. In vertebrates, including nonmammals, germ cell development and maturation appear in a similar fashion [2]. Spermatogenesis in vertebrates can be divided distinct sequential phases: mitotic stem cell renewal, mitotic proliferation of spermatogonia and supporting cells (e.g., Sertoli and Leydig cells), meiosis (the meiotic division of germ cells), and spermiogenesis (the maturation of germ cells into fully functional spermatozoa) [3,4,5,6].…”

Spermatogenesis in testis primary cell cultures of the tilapia (Oreochromis niloticus)

“…However, there is ample evidence from mammalian and fish spermatogenesis that the Sertoli cells are critically involved in sex determination and the control of spermatogenesis and oogenesis alike (Pudney, 1995;McLaren, 1998). The molecular interactions between the somatic cells and the germ line cells in fish have not been analyzed in detail but the endocrine and paracrine mechanisms controlling spermatogenesis in vertebrates are largely conserved (Nagahama, 1994).…”