Oestrogens and temperature-dependent sex determination in reptiles: all is in the gonads

Abstract

In many species of oviparous reptiles, the first steps of gonadal sex differentiation depend on the incubation temperature of the eggs. Feminization of gonads by exogenous oestrogens at a male-producing temperature and masculinization of gonads by antioestrogens and aromatase inhibitors at a female-producing temperature have irrefutably demonstrated the involvement of oestrogens in ovarian differentiation. Nevertheless, several studies performed on the entire gonad/adrenal/ mesonephros complex failed to find differences between male-and female-producing temperatures in oestrogen content, aromatase activity and aromatase gene expression during the thermosensitive period for sex determination. Thus, the key role of aromatase and oestrogens in the first steps of ovarian differentiation has been questioned, and extragonadal organs or tissues, such as adrenal, mesonephros, brain or yolk, were considered as possible targets of temperature and sources of the oestrogens acting on gonadal sex differentiation.In disagreement with this view, experiments and assays carried out on the gonads alone, i.e. separated from the adrenal/mesonephros, provide evidence that the gonads themselves respond to temperature shifts by modifying their sexual differentiation and are the site of aromatase activity and oestrogen synthesis during the thermosensitive period. Oestrogens act locally on both the cortical and the medullary part of the gonad to direct ovarian differentiation. We have concluded that there is no objective reason to search for the implication of other organs in the phenomenon of temperature-dependent sex determination in reptiles. From the comparison with data obtained in other vertebrates, we propose two main directions for future research: to examine how transcription of the aromatase gene is regulated and to identify molecular and cellular targets of oestrogens in gonads during sex differentiation, in species with strict genotypic sex determination and species with temperature-dependent sex determination.

Characterization of early molecular sex differentiation in rainbow trout, Oncorhynchus mykiss

“…Our results suggest an earlier steroidogenic potential in female rainbow trout gonads in comparison with males and also a very specific potential for estrogen synthesis in differentiating ovaries. This is in agreement with the crucial role of estrogens proposed in ovarian differentiation in fish (Guiguen, 2000;Nakamura et al, 2003) and some other lower vertebrates (Pieau and Dorizzi, 2004). Whether estrogens are produced by gonads at these very early stages of ovarian differentiation remains, however, to be demonstrated in fish.…”

Highly conserved linkage homology between birds and turtles: Bird and turtle chromosomes are precise counterparts of each other

“…In contrast to the genotypic (GSD) or chromosomal sex determination (CSD), temperature-dependent sex determination (TSD) is widespread in reptiles (Pieau et al 1999, Pieau & Dorizzi 2004. The mechanisms of sex determination and the primary factors of its complexity in birds and reptiles remain unknown (Sarre et al 2004, Smith & Sinclair 2004.…”

Changes in gonadal gene network by exogenous ligands in temperature-dependent sex determination

“…Previous studies have shown that isolated embryonic gonads had the ability to sense and respond to the ambient temperature in TSD species (Moreno-Mendoza et al 2001, Pieau & Dorizzi 2004, Shoemaker-Daly et al 2010). In the current study, the isolated gonads also exhibited the expression pattern of the candidate sex-determining genes similar to the one observed in ovo when treated with exogenous ligands and steroid hormone antagonists (Figs 6 and 7).…”