The Adaptive Sex in Stressful Environments

doi:10.1016/j.tree.2019.02.012

Trends in Ecology & Evolution

Volume 34, Issue 7, July 2019, Pages 628-640

https://doi.org/10.1016/j.tree.2019.02.012 Get rights and content

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.

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.

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

References (112)

R. van den Hurk et al.
Effects of natural androgens and corticosteroids on gonad differentiation in the rainbow trout, Salmo gairdneri
Gen. Comp. Endocrinol.
(1985)
R.S. Telemeco et al.
Temperature has species-specific effects on corticosterone in alligator lizards
Gen. Comp. Endocrinol.
(2014)
T.A. Mousseau et al.
The adaptive significance of maternal effects
Trends Ecol. Evol.
(1998)
T.W. Pike et al.
Maternal body condition and plasma hormones affect offspring sex ratio in peafowl
Anim. Behav.
(2005)
R.J. Chason
Preconception stress and the secondary sex ratio: a prospective cohort study
Fertil. Steril.
(2012)
N.C. Pratt et al.
Dexamethasone can prevent stress-related litter deficits in the golden hamster
Behav. Neural Biol.
(1990)
M. Mahmoodkhani
Pre-pregnancy stress suppressed the reproductive systems in parents and changed sex ratio in offspring
J. Appl. Biomed.
(2018)
J. Bae
Preconception stress and the secondary sex ratio in a population-based preconception cohort
Fertil. Steril.
(2017)
R. Monclús
Older mothers follow conservative strategies under predator pressure: the adaptive role of maternal glucocorticoids in yellow-bellied marmots
Horm. Behav.
(2011)
S. Helle
Female field voles with high testosterone and glucose levels produce male-biased litters
Anim. Behav.
(2008)

M. Mendl

Maternal social status and birth sex ratio in domestic pigs: an analysis of mechanisms

Anim. Behav.

(1995)

R. Rosenthal

The file drawer problem and tolerance for null results

Psychol. Bull.

(1979)

S.A. Frank et al.

Sex ratio under conditional sex expression

J. Theor. Biol.

(1988)

D. Pauly

Female fish grow bigger – let’s deal with it

Trends Ecol. Evol.

(2019)

L.J.G. Barcellos

The effects of fasting on cortisol, blood glucose and liver and muscle glycogen in adult jundiá Rhamdia quelen

Aquaculture

(2010)

N. Greenberg

Social status, gonadal state, and the adrenal stress response in the lizard, Anolis carolinensis

Horm. Behav.

(1984)

D.H. Abbott

Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates

Horm. Behav.

(2003)

S. Creel

Social dominance and stress hormones

Trends Ecol. Evol.

(2001)

A.M. Edwards et al.

Forgotten fathers: paternal influences on mammalian sex allocation

Trends Ecol. Evol.

(2014)

V. Ronget

The ‘evo-demo’ implications of condition-dependent mortality

Trends Ecol. Evol.

(2017)

J.P. Brunelli

Deep divergence and apparent sex-biased dispersal revealed by a Y-linked marker in rainbow trout

Mol. Phylogenet. Evol.

(2010)

P.J. Greenwood

Mating systems, philopatry and dispersal in birds and mammals

Anim. Behav.

(1980)

L.M. Romero

Physiological stress in ecology: lessons from biomedical research

Trends Ecol. Evol.

(2004)

A.M. Dettmer

Population density-dependent hair cortisol concentrations in rhesus monkeys (Macaca mulatta)

Psychoneuroendocrinology

(2014)

S. Messina

Physiological and immunological responses of birds and mammals to forest degradation: a meta-analysis

Biol. Conserv.

(2018)

E.G. Wessling

The costs of living at the edge: seasonal stress in wild savanna-dwelling chimpanzees

J. Hum. Evol.

(2018)

B. Geffroy

How nature-based tourism might increase prey vulnerability to predators

Trends Ecol. Evol.

(2015)

L.S. Hayward et al.

Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype

Gen. Comp. Endocrinol.

(2004)

B. Capel

Vertebrate sex determination: evolutionary plasticity of a fundamental switch

Nat. Rev. Genet.

(2017)

C.B. Schreck

Biology of Stress in Fish

(2016)

Y. Hayashi

High temperature causes masculinization of genetically female medaka by elevation of cortisol

Mol. Reprod. Dev.

(2010)

R.S. Hattori

Cortisol-induced masculinization: does thermal stress affect gonadal fate in pejerrey, a teleost fish with temperature-dependent sex determination?

PLoS One

(2009)

T. Yamaguchi

Cortisol is involved in temperature-dependent sex determination in the Japanese flounder

Endocrinology

(2010)

G.A. Corona-Herrera

Experimental evidence of masculinization by continuous illumination in a temperature sex determination teleost (Atherinopsidae) model: is oxidative stress involved?

J. Fish Biol.

(2018)

J.L. Mankiewicz

Masculinizing effect of background color and cortisol in a flatfish with environmental sex-determination

Integr. Comp. Biol.

(2013)

L. Ribas

Appropriate rearing density in domesticated zebrafish to avoid masculinization: links with the stress response

J. Exp. Biol.

(2017)

R. Nozu et al.

Cortisol administration induces sex change from ovary to testis in the protogynous wrasse, Halichoeres trimaculatus

Sex Dev.

(2015)

S. Miyagawa

Environmental control of sex determination and differentiation in reptiles

I.W. Deveson

Differential intron retention in Jumonji chromatin modifier genes is implicated in reptile temperature-dependent sex determination

Sci. Adv.

(2017)

C. Ge

The histone demethylase KDM6 B regulates temperature-dependent sex determination in a turtle species

Science

(2018)

D.A. Warner

Corticosterone exposure during embryonic development affects offspring growth and sex ratios in opposing directions in two lizard species with environmental sex determination

Physiol. Biochem. Zool.

(2009)

T. Uller

Sex-specific developmental plasticity in response to yolk corticosterone in an oviparous lizard

J. Exp. Biol.

(2009)

J.L. Iungman

Are stress-related hormones involved in the temperature-dependent sex determination of the broad-snouted caiman?

South Am. J. Herpetol.

(2015)

Z.M. Thayer

Impact of prenatal stress on offspring glucocorticoid levels: a phylogenetic meta-analysis across 14 vertebrate species

Sci. Rep.

(2018)

M.J. Sheriff et al.

Determining the adaptive potential of maternal stress

Ecol. Lett.

(2013)

D.A.S. Owen

Sex-dependent effects of maternal stress: stressed moms invest less in sons than daughters

J. Exp. Zool. Part Ecol. Integr. Physiol.

(2018)

T. Uller

Is sexual dimorphism affected by the combined action of prenatal stress and sex ratio?

J. Exp. Zoolog. A Comp. Exp. Biol.

(2005)

D.A. Warner

Maternal nutrition affects reproductive output and sex allocation in a lizard with environmental sex determination

Proc. R. Soc. Lond. B Biol. Sci.

(2007)

T.W. Pike et al.

Experimental evidence that corticosterone affects offspring sex ratios in quail

Proc. R. Soc. B Biol. Sci.

(2006)

F. Bonier

Maternal corticosteroids influence primary offspring sex ratio in a free-ranging passerine bird

Behav. Ecol.

(2007)

Cited by (53)

Gamma irradiation-induced offspring masculinization is associated with epigenetic changes in female zebrafish
2024, Ecotoxicology and Environmental Safety
Sex ratio variation is a key topic in ecology, because of its direct effects on population dynamics and thus, on animal conservation strategies. Among factors affecting sex ratio, types of sex determination systems have a central role, since some species could have a sex determined by genetic factors, environmental factors or a mix of those two. Yet, most studies on the factors affecting sex determination have focused on temperature or endocrine-disrupting chemicals (EDCs), and much less is known regarding other factors. Exposure to gamma irradiation was found to trigger offspring masculinization in zebrafish. Here we aimed at deciphering the potential mechanisms involved, by focusing on stress (i.e. cortisol) and epigenetic regulation of key genes involved in sex differentiation in fish. Cortisol levels in exposed and control (F0) zebrafish females’ gonads were similar. However, irradiation increased the DNA methylation level of foxl2a and cyp19a1a in females of the F0 and F1 generation, respectively, while no effects were detected in testis. Overall, our results suggest that parental exposure could alter offspring sex ratio, at least in part by inducing methylation changes in ovaries.
Dietary crude oil exposure during sex differentiation skewed adult sex ratio towards males in the zebrafish
2023, Science of the Total Environment
Dietary crude oil exposure has detrimental morpho-physiological effects in fishes, including endocrine disruption. However, little is known about how it influences sex differentiation and its potential for skewing sex ratios of populations. Appropriate sex ratio is important for maintaining effective population size and structure. Deviations of these ratios can compromise population growth and maintenance and may induce changes in a species' evolutionary trajectory. We assessed the potential of dietary exposure to crude oil (6.5, 11.4, and 17.5 mg/kg food) to alter sex differentiation in the zebrafish (Danio rerio) (20–35 days post fertilization (dpf)) and subsequently skew the adult (90 dpf) sex ratio. Multiple health- and fitness-related phenotypic traits (i.e., body mass and length, condition factor, heart rate, oxygen consumption, and their capacity to cope with hypoxia) were also assessed to better understand the effects of dietary crude oil exposure. We showed that dietary exposure to crude oil during the process of sex differentiation skewed sex ratio towards males (up to 0.34:1 female to male ratio in the highest oil concentration). Remarkably, this effect occurred independently of affecting physiological variables and female gonad characteristics, thus highlighting just how subtle the effects of dietary crude oil exposure can be. Our results suggest that, although fish were in an apparently healthy state during experimentation, sex ratio was still impacted, potentially compromising the resilience of the population. Therefore, considering how complex chemical mixtures affect organisms at several levels (molecular-individual) in experimental designs is warranted to better understand the implications of the exposures and the hazards that populations face in the wild.
Spermatozoa selection in the female reproductive tract: The initiation of the battle of the sexes
2023, Principles of Gender-Specific Medicine: Sex and Gender-Specific Biology in the Postgenomic Era
Historically, the sex ratio of offspring in mammals has been regarded as solely dependent on whether an X or Y chromosome-bearing spermatozoon fertilizes the oocyte. Recently, however, data from ingenious experiments showing that X and Y chromosome-bearing spermatozoa elicit differential genomic transcription by oviductal cells and presence or absence of key receptors have suggested that the female reproductive tract has an active role in selecting which spermatozoa reach the oocyte. These findings, which probably extend to other genomic differences, also suggest that the female reproductive tract has a role in controlling sperm selection prior to fertilization. Additionally, via processes involving the differential survival of early embryos, the oviduct may also be able to influence the next generation even after fertilization has occurred.
Environmental co-exposure of high temperature and Cu induce hormonal disturbance of cortisol signaling and altered responses of cellular defense genes in zebrafish
2022, Science of the Total Environment
Citation 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.
Global warming is causing a continuous increase in environmental temperatures, which simultaneously activates toxic environmental stresses, such as heavy metal exposure, in aquatic ecosystems. The present study aimed at evaluating the effects of Cu toxicity along with increased temperature during zebrafish embryogenesis. Decreased survival rates were observed following combined exposure to high temperature and Cu. Heart rates of zebrafish embryos were significantly increased only during heat stress. An abnormal morphology with curved body shape was induced by exposure to a combination of Cu and heat stress. Furthermore, heat stress also triggered Cu-induced intracellular reactive oxygen species (ROS) production, with upregulation of superoxide dismutase (SOD) and glutathione s-transferase (GST) expression, and cell death with modified expression of p53 and B-cell lymphoma-2 (Bcl-2) in zebrafish embryos. Finally, increased cortisol levels and altered expression of cortisol-signaling genes were observed following exposure to Cu and high temperatures. These results highlight that realistic exposure to combined stressors induces developmental disturbances via stress-induced responses involving oxidative stress and cell death as well as transcriptional alterations leading to cortisol signaling in fish.
Energy as the cornerstone of environmentally driven sex allocation
2022, Trends in Endocrinology and Metabolism
In recent years, observations of distinct organisms have linked the quality of the environment experienced by a given individual and the sex it will develop. In most described cases, facing relatively harsh conditions resulted in masculinization, while thriving in favorable conditions promoted the development of an ovary. This was shown indistinctively in some species presenting a genetic sex determination (GSD), which were able to sex-reverse, and in species with an environmental sex determination (ESD) system. However, this pattern strongly depends on evolutionary constrains and is detected only when females need more energy for reproduction. Here, I describe the mechanisms involved in this environmentally driven sex allocation (EDSA), which involves two main energy pathways, lipid and carbohydrate metabolism. These pathways act through various enzymes and are not necessarily independent of the previously known transducers of environmental signals in species with ESD: calcium–redox, epigenetic, and stress regulation pathways. Overall, there is evidence of a link between energy level and the sexual fate of individuals of various species, including reptiles, fish, amphibians, insects, and nematodes. As energy pathways are evolutionarily conserved, this knowledge opens new avenues to advance our understanding of the mechanisms that allow animals to adapt their sex according to the local environment.
High-temperature stress will put the thermo-sensitive teleost yellow catfish (Tachysurus fulvidraco) in danger through reducing reproductivity
2022, Ecotoxicology and Environmental Safety
Citation 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.
Recently, concerns for species that sex differentiation is influenced by temperature in the context of global warming have increased because disrupted operational sex ratios could threaten population maintenance. In contrast, little attention has been given to the reproductive ability of populations that experienced elevated temperatures. In this study, we demonstrated that high temperature (HT) would decrease population size via three different aspects of reproductive ability for the first time. We show that, in a thermo-sensitive teleost yellow catfish, a short period of HT (+3 °C) exposure during the critical period of sex differentiation leads to a different percentage of masculinization of XX genotypic females (1–23%) in wet-lab and natural water bodies. Combining the results of gonadal appearance, histology, sperm parameters, and fertilization rate, we found that XX pseudo-males induced by HT display significantly discounted fertility and reproductive performance compared to XY normal males. We demonstrate that the survival of the XY genotype is lower than XX genotype under environmental stress, including HT, hypoxia, and parasite infection, and the differential survival seems unrelated to male-biased sexual size dimorphism. The mathematical model predicts that the phenotypic female percent will be stabilized at 50% and the population will be sustainably maintained when masculinizing force is less than 0.5, while HT will put the population in danger when the masculinizing force exceeds 0.5. However, when we combine the real-world data of reproductive ability and mathematic model, our results suggest the population size decreases and the long-term survival of the studied species are threatened under the projected pace of increasing temperature. These findings will be useful for understanding the long-term effects of increasing temperature on sex ratio, reproduction and population maintenance in teleost.

View all citing articles on Scopus

View full text

Trends in Ecology & Evolution

ReviewThe Adaptive Sex in Stressful Environments

Highlights

Section snippets

Sex–Stress Interaction

Direct Influence of GCs on Sex Determination or Sex Differentiation

Influence of Maternal GCs on Offspring Sex Ratio

Timing of Sex-Ratio Assessment and GC Measurements

Adaptive Significance

Concluding Remarks

Acknowledgments

Glossary

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Trends Ecol. Evol.

Anim. Behav.

Fertil. Steril.

Behav. Neural Biol.

J. Appl. Biomed.

Fertil. Steril.

Horm. Behav.

Anim. Behav.

Anim. Behav.

Psychol. Bull.

J. Theor. Biol.

Trends Ecol. Evol.

Aquaculture

Horm. Behav.

Horm. Behav.

Trends Ecol. Evol.

Trends Ecol. Evol.

Trends Ecol. Evol.

Mol. Phylogenet. Evol.

Anim. Behav.

Trends Ecol. Evol.

Psychoneuroendocrinology

Biol. Conserv.

J. Hum. Evol.

Trends Ecol. Evol.

Gen. Comp. Endocrinol.

Vertebrate sex determination: evolutionary plasticity of a fundamental switch

Nat. Rev. Genet.

Biology of Stress in Fish

High temperature causes masculinization of genetically female medaka by elevation of cortisol

Mol. Reprod. Dev.

Cortisol-induced masculinization: does thermal stress affect gonadal fate in pejerrey, a teleost fish with temperature-dependent sex determination?

PLoS One

Cortisol is involved in temperature-dependent sex determination in the Japanese flounder

Endocrinology

Experimental evidence of masculinization by continuous illumination in a temperature sex determination teleost (Atherinopsidae) model: is oxidative stress involved?

J. Fish Biol.

Masculinizing effect of background color and cortisol in a flatfish with environmental sex-determination

Integr. Comp. Biol.

Appropriate rearing density in domesticated zebrafish to avoid masculinization: links with the stress response

J. Exp. Biol.

Cortisol administration induces sex change from ovary to testis in the protogynous wrasse, Halichoeres trimaculatus

Sex Dev.

Environmental control of sex determination and differentiation in reptiles

Differential intron retention in Jumonji chromatin modifier genes is implicated in reptile temperature-dependent sex determination

Sci. Adv.

The histone demethylase KDM6 B regulates temperature-dependent sex determination in a turtle species

Science

Corticosterone exposure during embryonic development affects offspring growth and sex ratios in opposing directions in two lizard species with environmental sex determination

Physiol. Biochem. Zool.

Sex-specific developmental plasticity in response to yolk corticosterone in an oviparous lizard

J. Exp. Biol.

Are stress-related hormones involved in the temperature-dependent sex determination of the broad-snouted caiman?

South Am. J. Herpetol.

Impact of prenatal stress on offspring glucocorticoid levels: a phylogenetic meta-analysis across 14 vertebrate species

Sci. Rep.

Determining the adaptive potential of maternal stress

Ecol. Lett.

Sex-dependent effects of maternal stress: stressed moms invest less in sons than daughters

J. Exp. Zool. Part Ecol. Integr. Physiol.

Is sexual dimorphism affected by the combined action of prenatal stress and sex ratio?

J. Exp. Zoolog. A Comp. Exp. Biol.

Maternal nutrition affects reproductive output and sex allocation in a lizard with environmental sex determination

Proc. R. Soc. Lond. B Biol. Sci.

Experimental evidence that corticosterone affects offspring sex ratios in quail

Proc. R. Soc. B Biol. Sci.

Review
The Adaptive Sex in Stressful Environments