Abstract

BackgroundGonadal fate in many reptiles, fish, and amphibians is modulated by the temperature experienced during a critical period early in life (temperature-dependent sex determination; TSD). Several molecular processes involved in TSD have been described but how the animals “sense” environmental temperature remains unknown. We examined whether the stress-related hormone cortisol mediates between temperature and sex differentiation of pejerrey, a gonochoristic teleost fish with marked TSD, and the possibility that it involves glucocorticoid receptor- and/or steroid biosynthesis-modulation.Methodology/Principal FindingsLarvae maintained during the period of gonadal sex differentiation at a masculinizing temperature (29°C; 100% males) consistently had higher cortisol, 11-ketotestoterone (11-KT), and testosterone (T) titres than those at a feminizing temperature (17°C; 100% females). Cortisol-treated animals had elevated 11-KT and T, and showed a typical molecular signature of masculinization including amh upregulation, cyp19a1a downregulation, and higher incidence of gonadal apoptosis during sex differentiation. Administration of cortisol and a non-metabolizable glucocorticoid receptor (GR) agonist (Dexamethasone) to larvae at a “sexually neutral” temperature (24°C) caused significant increases in the proportion of males.Conclusions/SignificanceOur results suggest a role of cortisol in the masculinization of pejerrey and provide a possible link between stress and testicular differentiation in this gonochoristic TSD species. Cortisol role or roles during TSD of pejerrey seem(s) to involve both androgen biosynthesis- and GR-mediated processes. These findings and recent reports of cortisol effects on sex determination of sequential hermaphroditic fishes, TSD reptiles, and birds provide support to the notion that stress responses might be involved in various forms of environmental sex determination.

Highlights

  • In many reptiles, fish, and amphibians, the fate of the differentiating gonad is influenced by a combination of genetic and environmental cues early during development [1,2,3]

  • Strong environmental effects on sex determination characterize environmental sex determination (ESD) as opposed to the strict genetic control of this process which occurs in genotypic sex determination (GSD)

  • In temperature-dependent sex determination (TSD), the most extensively studied form of ESD, for example, many molecular and biochemical pathways involved in sex differentiation have been identified, but studies often yield results that suggest the presence of other endogenous modulator(s) of the differentiation process which remain unknown [4,5,6,7,8,9]

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Summary

Introduction

Fish, and amphibians, the fate of the differentiating gonad is influenced by a combination of genetic and environmental cues (e.g. pH, relative density, social factors or temperature) early during development [1,2,3]. Experiments were performed to measure the cortisol, 11-ketotestosterone (11-KT) and testosterone (T) concentrations in larvae reared at masculinizing- (MPT), feminizing(FPT), and mixed-sex-producing temperatures (MixPT), the effects of cortisol and a non-metabolizable glucocorticoid receptor agonist (Dexamethasone) on sex ratio, and of cortisol administration on the sex differentiation molecular cascade.

Results
Conclusion
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