Ultrastructural and histochemical study of previtellogenic oogenesis in the desert lizard Scincus mitranus (Squamata, Sauropsida)

Abstract

The structure of the granulosa in reptilian sauropsids varies between groups. We investigated the follicle development in the desert lizard Scincus mitranus. In the germinal bed, oogonia, and primary oocytes were identified and found to be interspersed between the epithelial cells. Previtellogenesis was divided into three stages: early, transitional, and late previtellogenic stages. During the early previtellogenic stage (diplotene), the oocyte is invested by small epithelia cells that formed a complete single layer, which may be considered as a young follicle. The transitional previtellogenic stage was marked by proliferation and differentiation of the granulosa layer from a homogenous layer consisting of only small cells to a heterogeneous layer containing three cell types: small, intermediate, and large cells. The late previtellogenic stage was marked by high‐synthetic activity of large cells and the initiation of cytoplasmic bridges between large granulosa cells and the oocyte. Small cells were the only type of granulosa cells that underwent division. Thus, these cells may be stem cells for the granulosa cell population and may develop into intermediate and subsequently large cells. The intermediate cells may be precursors of large cells, as suggested by their ultrastructure. The ultrastructure of the large granulosa was indicative of their high synthetic activity. Histochemical analysis indicated the presence of cholesterol and phospholipids in the cytoplasm of large cells, the zona pellucida, among the microvilli, in the bridges region, and in the cortical region of the oocyte cytoplasm. These materials may be transferred from large cells into the oocyte through cytoplasmic bridges and provide nutritive function to large cells rather than functioning in steroidogenesis or vitellogenesis.

Sex Determination and Ovarian Development in Reptiles and Amphibians: From Genetic Pathways to Environmental Influences

“…Vitellogenesis proceeds as the follicles fill with yolk platelets prior to ovulation and await fertilization. Several papers have described these events in detail for specific species in each taxon: Crocodilia [Uribe and Guillette, 2000;Calderón et al, 2004;Moore et al, 2008Moore et al, , 2010a, Testudines [Callebaut et al, 1997;Hei et al, 2010;Pérez-Bermúdez et al, 2012], Squamata [Doddamani, 1994;Hernández-Franyutti et al, 2005;Vieira et al, 2010;Aldokhi et al, 2019;Delssin et al, 2019], Anura [Dumont, 1972;Ogielska and Kotusz, 2004;Piprek et al, 2017], andCaudata [Chardard andDournon, 1999;Chardard et al, 2003;Mendoza-Cruz et al, 2017]. For the purposes of this review, the remainder of this section will focus primarily on the major differences that exist across groups and important gaps that must be addressed to gain a comprehensive understanding of ovarian development in reptiles and amphibians.…”

“…While the presence of germinal nests in the cortex is ubiquitous across groups, the number of nests varies substantially. Crocodilians, turtles, and frogs generally have several [Callebaut et al, 1997;Uribe and Guillette, 2000;Ogielska and Kotusz, 2004;Moore et al, 2008;Pérez-Bermúdez et al, 2012], while most squamates have 1 or 2, but as many as 6 nests [Jones et al, 1982;Aldokhi et al, 2019]. It has been hypothesized that germinal nest number is related to clutch size and frequency of reproduction [Guraya, 1989].…”

“…The ovarian medulla in crocodilians and turtles develops a system of large lacunae that continually increase in size during ovarian maturation [Callebaut et al, 1997;Uribe and Guillette, 2000;Moore et al, 2010c;Pérez-Bermúdez et al, 2012]. Anurans and caudates also develop a similar central cavity within each ovarian sac, termed a lumen [Uribe, 2003;Ogielska and Kotusz, 2004], while squamates lack such a structure [Aldokhi et al, 2019;Delssin et al, 2019]. Ovarian lacunae are also evident in birds, although their size and number vary both within and across taxonomic groups [Uribe and Guillette, 2000;Hei et al, 2010;Pérez-Bermúdez et al, 2012].…”

“…Other intriguing, histological differences also exist during later stage follicular maturation. For example, in crocodilians [Uribe and Guillette, 2000;Moore et al, 2008], testudines [Callebaut et al, 1997;Hei et al, 2010;Pérez-Bermúdez et al, 2012], anurans [Dumont, 1972], and caudates [Uribe, 2009] a single or few layers of homogenous granulosa cells surround the oocyte and remain relatively unchanged throughout, whereas lizards [Delssin et al, 2019;Aldokhi et al, 2019] and snakes [Tumkiratiwong et al, 2012] begin with a single layer of cells termed small cells that develop into pyriform cells, with an intermediate cell stage, giving the appearance of 3 layers that eventually regress back to a single layer. In squamates, intercellular bridges between small cells and the growing oocyte have been observed that are believed to play a nutritive role in nourishing the oocyte [Andreuiccetti, 1992].…”

“…Unlike mammals, in which all oogonia enter meiosis early in life, in most reptiles and amphibians, the adult ovary retains nests of mitotic oogonia which can serve as an active supply of new oocytes. This includes crocodilians, turtles, squamates, and caudates [Callebaut et al, 1997;Uribe and Guillette, 2000;Uribe, 2009;Hei et al, 2010;Aldokhi et al, 2019]. This unique feature opens interesting questions about reproductive senescence in these groups, since it appears the oocyte pool has the potential to evade depletion.…”