Trends in Ecology & Evolution
ReviewThe Adaptive Sex in Stressful Environments
Section snippets
Sex–Stress Interaction
Among vertebrates, sex can be determined by environmental sex determination (ESD, see Glossary), genetic sex determination (GSD), or the interaction of both. The phylogenetic distribution of GSD and ESD indicates that transitions between these types of sex determination have occurred many times [1]. Although mammals and birds only have GSD, sex-determining mechanisms have high evolutionary plasticity in fish, reptiles, and amphibians. Nevertheless, the sensitivity of the undifferentiated gonad
Direct Influence of GCs on Sex Determination or Sex Differentiation
In fish, studies conducted to date have tended to show that at suboptimal temperatures (i.e., very high or very low), low pH, continuous lighting, or high density – each of which can be considered to be a stressful condition [2] – more males are produced (Figure 1). In fish, sex determination can occur at different stages of the life cycle: at fertilization or later in development (egg or larval stages). The undifferentiated gonad of fish is extremely labile and sensitive to external factors [1]
Influence of Maternal GCs on Offspring Sex Ratio
Mother-to-offspring GCs transmission is an evolutionarily conserved mechanism found across vertebrate species [18], and is one of the best-studied factors in the maternal effect literature 19, 20. However, studies on the relationship between maternal GCs and sex ratio in fish are, to date, lacking. Three different studies investigated the link between maternal stress and offspring sex of reptile species with different degrees of sex-sensitivity to temperature. Two studies on the common lizard (
Timing of Sex-Ratio Assessment and GC Measurements
The sex ratio can vary in response to stress at several developmental timepoints. Sex-ratio bias can occur at around the time of conception and sexual differentiation (affecting the PSR), or during late stages of development through differential mortality (affecting the SSR) (Box 2). This differential mortality is likely to have higher fitness costs, especially in monotocous species (producing only a single offspring at a time), because it implies loss of offspring after maternal resources have
Adaptive Significance
Some cases discussed above may be adaptive, meaning that the tendency of an animal to develop as a given sex, after experiencing stress directly or indirectly (through maternal influence), is or has been under positive selection. If stress-related changes in the sex ratio are under positive selection, this implies that one sex would have a higher fitness in stressful conditions (Figure 2) or that maternal stress modifies the relative costs of producing male and female offspring. Indeed, in the
Concluding Remarks
The sensitivity of the sex ratio to GC levels appears to be very variable among vertebrates. The effects are more prevalent in fish and birds than in reptiles and mammals. The different mechanisms of sex determination (genetic vs environmental) are not sufficient to explain these results because GSD is found in birds and ESD occurs in many species of reptiles. Stress-related sex-ratio biases are not necessarily more extreme in fish, but the direction of the sex-ratio skew is uniform in
Acknowledgments
We would like to thank Claus Wedekind, Jean-François Lemaître, Ben Parrott, Kristen Navarra, Michael Sheriff, Andrea Stephens, and two anonymous reviewers for constructive comments. We also thank Starrlight Augustine and Bastien Sadoul for their help in collecting dynamic energy budget (DEB) data, and Pierre Lopez for drawing species. We thank Tony Tebby for English correction and suggestions. Finally, we would like to thank Gabriel Geffroy Agudelo and Marin Douhard for the inspiration. B.G. is
Glossary
- Acute stressor
- short-term environmental challenge to the physiology of an animal.
- Chronic stressor
- long-term environmental challenge to the physiology of an animal.
- Cortisol
- the main GC hormone produced by fish and most mammals through the hypothalamic–pituitary–adrenocortical (interrenal for fish) axis, and that is released in response to stressors.
- Corticosterone
- the main GC hormone produced by birds, reptiles, and amphibians, and which is released in response to stressors.
- Environmental sex
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Gamma irradiation-induced offspring masculinization is associated with epigenetic changes in female zebrafish
2024, Ecotoxicology and Environmental SafetyDietary crude oil exposure during sex differentiation skewed adult sex ratio towards males in the zebrafish
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2022, Science of the Total EnvironmentCitation Excerpt :Our results first report that increase in temperature by global warming might be boost heavy metal toxicity associated with cortisol signaling in unbalance of fish population with male bias. Increasing temperature has been emerging as a global big issue in the context of global warming (Geffroy and Douhard, 2019). Temperature is a critical environmental factor that can affect sex ratio of a given population.
Energy as the cornerstone of environmentally driven sex allocation
2022, Trends in Endocrinology and MetabolismHigh-temperature stress will put the thermo-sensitive teleost yellow catfish (Tachysurus fulvidraco) in danger through reducing reproductivity
2022, Ecotoxicology and Environmental SafetyCitation Excerpt :Importantly, the real data of sex reversal force in natural water bodies and reproductivity of sex-reversed individuals have rarely been reported, even though the effects of environmental stress on sex differentiation have been reported in over one hundred fishes (Shen and Wang, 2014, 2018; Ospina-Álvarez and Piferrer, 2008). Many researchers have emphasized the importance of real experimental data for the establishment and verification of mathematical models (Geffroy and Wedekind, 2020; Hurley et al., 2004; Wedekind, 2018; Geffroy and Douhard, 2019). Related studies have been reported in reptiles (Donelson and Munday, 2015; Laloë et al., 2017; Mitchell et al., 2010; Santidrián Tomillo et al., 2015) but not in fish.