Stress and sex: does cortisol mediate sex change in fish?

Abstract

Cortisol is the main glucocorticoid (GC) in fish and the hormone most directly associated with stress. Recent research suggests that this hormone may act as a key factor linking social environmental stimuli and the onset of sex change by initiating a shift in steroidogenesis from estrogens to androgens. For many teleost fish, sex change occurs as a usual part of the life cycle. Changing sex is known to enhance the lifetime reproductive success of these fish and the modifications involved (behavioral, gonadal and morphological) are well studied. However, the exact mechanism behind the transduction of the environmental signals into the molecular cascade that underlies this singular process remains largely unknown. We here synthesize current knowledge regarding the role of cortisol in teleost sex change with a focus on two well-described transformations: temperature-induced masculinization and socially regulated sex change. Three non-mutually exclusive pathways are considered when describing the potential role of cortisol in mediating teleost sex change: cross-talk between GC and androgen pathways, inhibition of aromatase expression and upregulation of amh (the gene encoding anti-Müllerian hormone). We anticipate that understanding the role of cortisol in the initial stages of sex change will further improve our understanding of sex determination and differentiation across vertebrates, and may lead to new tools to control fish sex ratios in aquaculture.Reproduction (2017) 154 R149-R160

Stress, novel sex genes and epigenetic reprogramming orchestrate socially-controlled sex change

“…Cortisol can then initiate gonadal sex change, and our data implicate pathways that promote stress-induced masculinization of genetic females in artificial settings ( Fig. 7): 1) suppression of aromatase expression via glucocorticoid response elements in the cyp19a1a promoter, 2) upregulation of amh expression to induce germ cell apoptosis and promote maleness, and 3) cross-talk with the androgenesis pathway via increased cyp11c1 and hsd11b2 expression (dual roles in 11-KT synthesis and cortisol metabolism) (36,60). Our finding of opposing expression patterns for genes encoding glucocorticoid and mineralocorticoid receptors (nr3c1 and nr3c2) and the enzymes that control cortisol production (cyp11c1 and hsd11b1la) and inactivation (hsd11b2), implies highest cortisol production in early sex change (stage 2) ( Fig.…”

“…The stress response in sex-changing females is expected to elicit rapid signaling changes of brain neurotransmitters, such as arginine vasotocin (AVT), gonadotropinreleasing hormone (GnRH), and norepinephrine (NE), which have been suggested to control behavioral sex change in social wrasses (36,51,52). We observed no significant early expression changes in genes encoding these neuropeptides or their precursors in the brain, but this may be because the sex-specific signal is subtle (53,54) or highly localized (55).…”

“…Cortisol, a glucocorticoid that controls stress-induced responses in all vertebrates, may be an important mediator of environmental sex determination (36). We therefore determined if cortisol-pathway genes show altered expression during early sex change stages.…”

Measuring cortisol, the major stress hormone in fishes

“…Nonetheless, it has been successfully applied by a variety of scientists, from physiologists (Auperin et al, ) to behavioural ecologists (Colson et al, ), in controlled environments and also in the wild (Geffroy et al, ; Love et al, ), to assess levels of stress in fishes. In addition, relation between the stress axis and neurogenesis (Sadoul et al, ; Sørensen et al, ), growth (Sadoul & Vijayan, ) and sex determination or sex‐change (Geffroy & Bardonnet, ; Goikoetxea et al, ; Olivotto & Geffroy, ) are now well described, highlighting the central role of cortisol in fish physiology and behaviour. It is also an important tool in characterising coping abilities of fishes and investigating how the environment can disturb this.…”

Anin vitroovarian explant culture system to examine sex change in a hermaphroditic fish

“…It was hypothesised that CORT treatment would promote oocyte degeneration, following evidence that CORT may mediate sex change in fish by inhibiting aromatase transcription and promoting androgen production (14,15). However, no significant differences were observed in the proportion of non-atretic PVO between the controls and ovaries treated with 1 and 10 ng/mL of CORT (43.3 ± 7.7 % and 42.9 ± 6.2 %, respectively) (Figure 2C).…”