Climate-driven shifts in adult sex ratios via sex reversals: the type of sex determination matters

Abstract

Sex reversals whereby individuals of one genetic sex develop the phenotype of the opposite sex occur in ectothermic vertebrates with genetic sex-determination systems that are sensitive to extreme temperatures during sexual differentiation. Recent rises in global temperatures have led researchers to predict that sex reversals will become more common, resulting in the distortion of many populations' sex ratios. However, it is unclear whether susceptibility to climate-driven sex-ratio shifts depends on the type of sex determination that varies across species. First, we show here using individual-based theoretical models that XX/XY (male-heterogametic) and ZZ/ZW (female-heterogametic) sex-determination systems can respond differentially to temperature-induced sex reversals. Interestingly, the impacts of climate warming on adult sex ratio (ASR) depend on the effects of both genotypic and phenotypic sex on survival and reproduction. Second, we analyse the temporal changes of ASR in natural amphibian populations using data from the literature, and find that ASR shifted towards males in ZZ/ZW species over the past 60 years, but did not change significantly in XX/XY species. Our results highlight the fact that we need a better understanding of the interactions between genetic and environmental sex-determining mechanisms to predict the responses of ectotherms to climate change and the associated extinction risks.This article is part of the themed issue 'Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies'.

Adult sex ratios and reproductive strategies: a critical re-examination of sex differences in human and animal societies

“…He argues that environmentally driven feminization could be more common than currently thought, although the frequency of these phenotype-genotype mismatched individuals may significantly affect population dynamics. Bó kony et al [62] examine the effects of climate-driven sex changes on ASRs in ectotherms with either temperature-dependent sex determination or temperature-sensitive genetic sex determination systems. Globally rising temperatures and environmental contaminants threaten to distort population sex ratios, which, in turn, may disrupt evolved mating strategies and potentially lead to population decline or even extinction.…”

Evolutionary and demographic consequences of temperature-induced masculinization under climate warming: the effects of mate choice

“…We assumed that sex-reversed males (XX, ZW or WW) are as viable and fecund as normal males, following previous models and empirical data [27,33,34]. Note that our previous model predicted that 25% decrease in reproductive success of masculinized individuals had little effect on adult sex ratios and sex chromosome frequencies, whereas their sterility lead to the ZW system behaving exactly like the XY system [11]. Further, we assumed that the WW genotype (aa in ZW/ZZ system) is phenotypically equivalent to normal females (i.e.…”

“…We aimed to build a relatively realistic model where a number of parameters affect the life history and demography of iteroparous animals including the age of maturation, annual survival rates differing across life stages, fertility, environmental carrying capacity, and limited number of mating events for each individual per breeding season. We set these parameters to be representative for amphibians using empirical data from the literature, mostly following our previous model [11], although similar parameter settings may be representative for other temperature-sensitive taxa such as fish or reptiles. Every year, the population produces N offspring calculated using equation 3:…”

“…Exposure to unusually high temperature can cause masculinization in some species and feminization in others, as observed among urodelans and lizards, whereas masculinization seems to be the typical response to high temperatures in anurans and fish [3,4,8,10]. In natural populations of such species, global climate change may potentially distort the sex ratios and, with significant temperature rise, may lead to population extinction [11]. Furthermore, theoretical models suggest that climate change may cause, via temperature-induced sex reversals, drastic changes in the population's genetic constitution, including novel genotypes, sex-chromosome extinction, and turnovers of the sex-determination system e.g.…”

“…Furthermore, theoretical models suggest that climate change may cause, via temperature-induced sex reversals, drastic changes in the population's genetic constitution, including novel genotypes, sex-chromosome extinction, and turnovers of the sex-determination system e.g. from genetic to temperaturedependent sex determination as well as from female-heterogametic (ZW/ZZ system; ZW females, ZZ males) to male-heterogametic (XX/XY system; XX females, XY males) sexchromosome systems [11][12][13][14][15].…”