The Adaptive Sex in Stressful Environments

Abstract

The impact of early stress on juvenile development has intrigued scientists for decades, but the adaptive significance of such effects remains an ongoing debate. This debate has largely ignored some characteristics of the offspring, such as their sex, despite strong evolutionary and demographic implications of sex-ratio variation. We review recent studies that examine associations between glucocorticoids (GCs), the main class of stress hormones, and offspring sex. Whereas exposure to GCs at around the time of sex determination in fish consistently produces males, the extent and direction of sex-ratio bias in response to stress vary in reptiles, birds, and mammals. We propose proximate and ultimate explanations for most of these trends. Highlights ► Offspring sex ratios have been shown to correlate with environmental stressors and maternal stress in many vertebrate species. ► There is an adaptive advantage for parents to produce the sex that is more likely to survive and reproduce in a future hazardous environment. ► In the fastest life histories, there is more likely to be a close good match between the environment around sex determination and the future environment of the offspring. ► GCs are key messengers of environmental contexts that likely influence the sex-determination processes of various species. ► A combination of field and laboratory studies will be necessary to understand the extent to which stress influences offspring sex from conception to birth.

RADSex: a computational workflow to study sex determination using Restriction Site-Associated DNA Sequencing data

“…Although Y chromosome population differences have rarely been explored, at least in fish species, the results from our re-analysis of a medaka population suggest that such polymorphism may be more frequent than expected. In addition, female-to-male sex-reversal could be a consequence of intensive rearing aquaculture conditions leading to stress induced sex-reversal (Geffroy & Douhard, 2019) , which has been observed in other fish species reared in laboratory or aquaculture facilities .…”

Cellular calcium and redox regulation: the mediator of vertebrate environmental sex determination?

“…The hypothalamic–pituitary–adrenal (HPA) axis in reptiles, birds and mammals or inter‐renal (HPI) axis in fish and amphibians has a role in sex determination in a range of taxa [see reviews in Goikoetxea, Todd & Gemmell () and Geffroy & Douhard ()]. Among gonochoristic (single‐sex) fish, cortisol‐mediated sex determination in response to temperature is well supported by experimental application of cortisol (Hattori et al ., ; Hayashi et al ., ; Castañeda Cortés et al ., ; Miller et al ., ).…”

Effects of global warming on sex ratios in fishes

“…The link between environmental variables (particularly high temperature and fish density) and the stress axis (through the production of cortisol) has been established as an important factor influencing sex determination in various fish species, typically resulting in masculinization (Geffroy & Douhard, 2019). Incubating O. mykiss eggs in cortisol leads to the development of testes (van den Hurk & van Oordt, 1985), and cortisol administration induces masculinization in three‐spotted wrasse Halichoeres trimaculatus (Quoy & Gaimard 1834) (Nozu & Nakamura, 2015) and orange‐spotted grouper Epinephelus coioides (Hamilton 1822) (Chen et al ., 2020).…”

“…It therefore seems that male bias at high temperature is a rule in fishes. This suggests that producing males may often be adaptive in harsh conditions (Geffroy & Douhard, 2019). Different hypotheses have been proposed in this context, including higher migration propensity and quicker maturation, leading to a greater relative fitness for males than females in unpredictable environments (Geffroy & Douhard, 2019).…”

“…This suggests that producing males may often be adaptive in harsh conditions (Geffroy & Douhard, 2019). Different hypotheses have been proposed in this context, including higher migration propensity and quicker maturation, leading to a greater relative fitness for males than females in unpredictable environments (Geffroy & Douhard, 2019). However, female bias at high temperatures is common in other taxa ( e.g ., Janzen 1994) and there are at least two examples of temperature‐related female bias in fishes, in O. nerka (Craig et al ., 1996) and channel catfish Ictalurus punctatus (Rafinesque 1818) (Patiño et al ., 1996).…”