Sex‐related differences in aging rate are associated with sex chromosome system in amphibians

Abstract

Sex‐related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture–recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex‐specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the “unguarded X/Z effect”) or repeat‐rich Y/W chromosome (the “toxic Y/W effect”) could accelerate aging in the heterogametic sex in some vertebrate clades.

Sex‐specific aging in animals: Perspective and future directions

“…An analysis focused on tetrapods suggested that the sex‐determination system (XY vs. ZW) explained ¼ to ⅓ of the differences in the adult sex ratio (a proxy of sex differences in adult mortality) observed between species, depending on the heterogametic sex (Pipoly et al, 2015 ). A similar result was obtained in a study focused on amphibians (Cayuela et al, 2021 ). Data from the four core genotypes in mouse (animals with either XX or XY sex chromosome complement and either ovaries or testes generated by exploiting a translocation of the SRY gene to an autosome) shows that the presence of two X chromosomes improves lifespan, irrespective of the gonads (Davis et al, 2019 ).…”

How much does the unguarded X contribute to sex differences in life span?

“…Two additional observations imply that the unguarded X is unlikely to provide a general explanation for sex differences in longevity. First, extensive sex differences for ageing and life span are observed in species with largely homomorphic sex chromosomes, including higher mortality rates in the heterogametic sex (Cayuela et al 2022), which cannot be explained by unguarded X effects. Second, although birds are predicted (by unguarded X theory) to exhibit stronger sex differences in life span than mammals, data support the opposite pattern (the sex difference in life span in birds is roughly half the average difference observed in mammals; Lemaître et al 2020;Xirocostas et al 2020).…”

“…2020; Cayuela et al. 2022). Estimates of adult sex ratios are typically skewed toward the homogametic sex (i.e., females in species with X chromosomes; males in species with a Z; Pipoly et al.…”

Asymmetrical sex reversal: Does the type of heterogamety predict propensity for sex reversal?

“…Heterogamety is a fundamental aspect of organismal biology that, according to recent research, has far‐ranging consequences on life histories and population dynamics, including sex ratios, sex‐specific aging rates, and life spans. [ 82–84 ] Here we have highlighted that heterogamety may further influence the fate of ectothermic vertebrates by affecting their propensity to undergo environmental sex reversal. By considering “asymmetrical sex reversal,” a relaxed interpretation of Witschi's rule, we can generate testable predictions regarding the differences in sex‐reversal propensity between populations with different sex‐chromosome systems induced by different environmental conditions.…”

“…Heterogamety is a fundamental aspect of organismal biology that, according to recent research, has far-ranging consequences on life histories and population dynamics, including sex ratios, sex-specific aging rates, and life spans. [82][83][84] Here we have highlighted that heterogamety may further influence the fate of ectothermic vertebrates by affecting their propensity to undergo environmental sex reversal.…”