Temperature‐dependent sex determination in reptiles: Proximate mechanisms, ultimate outcomes, and practical applications

Abstract

In many egg-laying reptiles, the incubation temperature of the egg determines the sex of the offspring, a process known as temperature-dependent sex determination (TSD). In TSD sex determination is an "all or none" process and intersexes are rarely formed. How is the external signal of temperature transduced into a genetic signal that determines gonadal sex and channels sexual development? Studies with the red-eared slider turtle have focused on the physiological, biochemical, and molecular cascades initiated by the temperature signal. Both male and female development are active processes--rather than the organized/default system characteristic of vertebrates with genotypic sex determination--that require simultaneous activation and suppression of testis- and ovary-determining cascades for normal sex determination. It appears that temperature accomplishes this end by acting on genes encoding for steroidogenic enzymes and steroid hormone receptors and modifying the endocrine microenvironment in the embryo. The temperature experienced in development also has long-term functional outcomes in addition to sex determination. Research with the leopard gecko indicates that incubation temperature as well as steroid hormones serve as organizers in shaping the adult phenotype, with temperature modulating sex hormone action in sexual differentiation. Finally, practical applications of this research have emerged for the conservation and restoration of endangered egg-laying reptiles as well as the embryonic development of reptiles as biomarkers to monitor the estrogenic effects of common environmental contaminants.

Expression of Sox9, Mis, and Dmrt1 in the gonad of a species with temperature‐dependent sex determination

“…Cooler incubation temperatures (25-27°C) produce all male hatchlings and warmer temperatures (31-35°C) result in all female hatchlings, with varying sex ratios produced by temperatures in between (Wibbels et al, 1991). Shifting eggs during the TSP from one end of the temperature spectrum to the other redirects gonadal development, resulting in 100% sex reversal (Crews et al, 1994).…”

The ends of a continuum: genetic and temperature‐dependent sex determination in reptiles

“…(17) The conventional view, which emerged from the early work on sex determination in reptiles, is that these two mechanisms are mutually exclusive (18,19) and can therefore be viewed as discrete and fundamentally different. (20,21) Implicit in this perspective is that differences in the mechanisms between the two modes are complex, (22) that they constitute a discrete dichotomous process, and that through appropriate experimental approaches, one can be demonstrated to the exclusion of the other. (21) Pieau, (23) reflecting that proposed for insects, (24) offered an alternative view by suggesting that a common underlying sex-differentiation pathway implied that there were no clear boundaries between TSD and GSD and empirical evidence (25) and a broader taxonomic perspective led Wilkins (26)(27)(28) to suggest that it is probable that all sexdetermining systems have some genetic component.…”

“…(37) There is general consensus that temperature exerts its influence in species with TSD by acting upon the genetic mechanisms that govern steroidogenic enzymes or steroid hormone receptors, thus altering the hormone environment of the sexually indifferent embryo and directing development in either a male or a female direction. (22,38) Administration of exogenous oestrogen in turtles will override the effect of a male-producing temperature to yield female hatchlings (39,40) and the period of sensitivity to exogenous oestrogen coincides with the thermosensitive period. (41) In reptiles, synthesis of oestrogens depends on the aromatization of testosterone and androstenedione to the oestrogens estrone and estradiol-17b.…”

Mapping phenotypic plasticity and genotype–environment interactions affecting life-history traits in Caenorhabditis elegans

“…It is a widespread phenomenon and occurs throughout several kingdoms. Some well-known examples are temperaturedependent sex determination in reptiles (Crews et al, 1994), seasonal polyphenism in various species of butterflies in response to temperature and/or humidity Brakefield, 1996, 1999), or 'shade-avoidance' developmental response in several types of plants (Pigliucci, 1996). Plasticity can be visualized by plotting measurements for the same trait in different environments for a given genotype, also called the norm of reaction.…”