Climate change, sex reversal and lability of sex‐determining systems

Abstract

Sex reversal at high temperatures during embryonic development (e.g., ZZ females) provides the opportunity for new genotypic crosses (e.g., ZZ male × ZZ female). This raises the alarming possibility that climatic warming could lead to the loss of an entire chromosome—one member of the sex chromosome pair (the Y or W)—and the transition of populations to environmental sex determination (ESD). Here we examine the evolutionary dynamics of sex‐determining systems exposed to climatic warming using theoretical models. We found that the loss of sex chromosomes is not an inevitable consequence of sex reversal. A large frequency of ZZ sex reversal (50% reversal from male to female) typically divides the outcome between loss of the ZW genotype and the stable persistence of ZZ males, ZW females and ZZ females. The amount of warming associated with sex chromosome loss depended on several features of wild populations—environmental fluctuation, immigration, heritable variation in temperature sensitivity and differential fecundity of sex‐reversed individuals. Chromosome loss was partially or completely buffered when sex‐reversed individuals suffered a reproductive fitness cost, when immigration occurred or when heritable variation for temperature sensitivity existed. Thus, under certain circumstances, sex chromosomes may persist cryptically in systems where the environment is the predominant influence on sex.

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

“…On the other hand, we also need theoretical studies on how further factors affect our predictions. For example, in species where the temperature reaction norm is non-linear, climate warming may lead to ZZ feminization and ultimately the loss of W chromosome [15]. In bearded dragons (Pogona vitticeps), for instance, ZZ individuals develop into females at high temperatures, and surprisingly, these sex-reversed females enjoy a fecundity advantage over normal females [16].…”

“…tparalell reaction norms). We followed Grossen and colleagues [13] in assuming that male signal increases monotonically with temperature, based on the empirical observations of masculinising effects of high temperatures and feminising effects of low temperatures in several amphibians and fish [4,27], although we note that counter-examples exist and nonlinear temperature reaction norms are also possible [14,15].…”

“…We did not allow new mutations to occur on the thr locus or the sex-determinant locus, because in the realistically small simulated populations (starting with 200 adults) appearance of a new mutant allele is unlikely over the relatively short evolutionary time simulated here due to rapid climate warming. Note, however, that evolution is still possible due to standing variation in temperature sensitivity [15], which was allowed in our simulations by changes in relative frequencies of the thr alleles.…”

“…We set εB = 0.01 based on the standard deviation of temperature anomalies observed in the Northern Hemisphere between 1970 and 2000 [39]. We set εW = 0.05, a value five times higher than εB, which is realistic based on empirical data for reptiles [15]. These settings ensure that, before the start of climate warming, a stable genetic sex-determination system (either XX/XY or ZW/ZZ) persists, with only occasional events of sex reversal in individuals experiencing unusually high temperature (resulting in ca.…”

“…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].…”