Demographic and genetic consequences of disturbed sex determination

Abstract

During sex determination, genetic and/or environmental factors determine the cascade of processes of gonad development. Many organisms, therefore, have a developmental window in which their sex determination can be sensitive to, for example, unusual temperatures or chemical pollutants. Disturbed environments can distort population sex ratios and may even cause sex reversal in species with genetic sex determination. The resulting genotype-phenotype mismatches can have long-lasting effects on population demography and genetics. I review the theoretical and empirical work in this context and explore in a simple population model the role of the fitness v_yy of chromosomally aberrant YY genotypes that are a consequence of environmentally induced feminization. Low v_yy is mostly beneficial for population growth. During feminization, low v_yy reduces the proportion of genetic males and hence accelerates population growth, especially at low rates of feminization and at high fitness costs of the feminization itself (i.e. when feminization would otherwise not affect population dynamics much). When sex reversal ceases, low v_yy mitigates the negative effects of feminization and can even prevent population extinction. Little is known about v_yy in natural populations. The available models now need to be parametrized in order to better predict the long-term consequences of disturbed sex determination.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'.

Keywords: climate change; endocrine-disrupting chemicals; environmental sex reversal; extinction; population growth; sex determination.

Figure 1.

Illustrating the continuum of genetic and environmental sex determination. Examples of possible effects of environmental factors (e.g. temperature or concentration of endocrine-disrupting micropollutants) on sex determination in (a) a hypothetical population with genetic sex determination and the female genotype being susceptible to environmental factors that masculinize (i.e. turning some XX or ZW individuals into males) and (b) a population with genetic sex-determining factors and the male genotype being susceptible to environmental factors that feminize (i.e. turning some XY or ZZ individuals into females). The shaded area indicates the within-population variance that could be due to additive genetic variance in the reaction norms or due to random effects at the start of the sex determination cascade. The hatched line gives the population sex ratio (proportion of males) if all clutches experience the same environmental conditions. This population sex ratio will equal adult sex ratio (ASR) if there is no sex-specific mortality.

Figure 2.

The effects of environmental feminization and various types of fitness reduction on population size and genetics. Low fitness of YY genotypes (v_YY) can significantly mitigate the negative long-term effects of feminization when sex reversal ceases. Low v_YY can also produce positive effects on population growth during feminization, especially at low rates and high costs of feminization. The figure shows the population census sizes N_c (non-hatched lines) and the genetically effective population sizes N_e (hatched lines) when sex reversal (here only feminization, i.e. q = 0) causes no fitness reduction (v_ESR = 1; panels a,b) or fitness reductions of v_ESR = 0.75 (panels c and d) or v_ESR = 0.5 (panels e,f). Feminization is either weak (p = 0.25; panels a,c,e) or strong (p = 0.75; panels b,d,f) during the first 10 generations (q always = 0). Feminization ceases from generation 10 on (p = 0). The aberrant YY karyotype either causes no additional fitness reduction (v_YY = 1; thick black lines) or a fitness of v_YY = 0.5 (thin black lines) or v_YY = 0 (thin grey lines). See box 1 for the settings of the model.

Figure 3.

The effects of environmental feminization and various types of fitness reduction on phenotypic and genetic sex ratio. Feminization reduces the proportion of phenotypic males while it increases the proportion of genetic males. Both effects are dependent on the fitness of YY genotypes (v_YY). Low v_YY can significantly reduce the proportion of genetic males, especially so at high rates of feminization. The figure shows the phenotypic population sex ratio (proportion of males; non-hatched lines) and the genetic sex ratio, i.e. the rate of individuals with Y-chromosomes (hatched lines). The parameter setting are as in figure 2, i.e. the fitness effect of sex reversal is either v_ESR = 1 (panels a,b), v_ESR = 0.75 (panels c,d), or v_ESR = 0.5 (panels e,f), feminization is either weak (p = 0.25; panels a,c,e) or strong (p = 0.75; panels b,d,f) during the first 10 generations, feminization ceases from generation 10 on (p = 0), and the aberrant YY karyotype has a fitness of either v_YY = 1 (thick black lines), v_YY = 0.5 (thin black lines), or v_YY = 0 (thin grey lines).