The sex with the reduced sex chromosome dies earlier: a comparison across the tree of life

Abstract

Many taxa show substantial differences in lifespan between the sexes. However, these differences are not always in the same direction. In mammals, females tend to live longer than males, while in birds, males tend to live longer than females. One possible explanation for these differences in lifespan is the unguarded X hypothesis, which suggests that the reduced or absent chromosome in the heterogametic sex (e.g. the Y chromosome in mammals and the W chromosome in birds) exposes recessive deleterious mutations on the other sex chromosome. While the unguarded X hypothesis is intuitively appealing, it had never been subject to a broad test. We compiled male and female longevity data for 229 species spanning 99 families, 38 orders and eight classes across the tree of life. Consistent with the unguarded X hypothesis, a meta-analysis showed that the homogametic sex, on average, lives 17.6% longer than the heterogametic sex. Surprisingly, we found substantial differences in lifespan dimorphism between female heterogametic species (in which the homogametic sex lives 7.1% longer) and male heterogametic species (in which the homogametic sex lives 20.9% longer). Our findings demonstrate the importance of considering chromosome morphology in addition to sexual selection and environment as potential drivers of sexual dimorphism, and advance our fundamental understanding of the mechanisms that shape an organism's lifespan.

Genetic sex determination and sex-specific lifespan in tetrapods – evidence of a toxic Y effect

“…Previously, Pipoly et al [9] identified female-biased adult sex ratios in taxa with XY systems and male-biased adult sex ratios in taxa with ZW systems. Along the same line, Xirocostas et al [10] recently found that mean/maximum lifespan is shorter in the heterogametic sex across the tree of life, although the latter could be at least partly explained by the effects of phylogenetic signal and/or sexual selection. Our results build on these studies by showing that, in vertebrates, the relationship between sex differences in survival and sex determination system remains after accounting for both phylogenetic signal (which in our sample explained ∼33% of the variance in the sex gap in lifespan) and sexual size dimorphism (a proxy for sexual selection).…”

“…The most commonly cited hypothesis to explain broad patterns of sex-specific lifespan across taxa is the UXh hypothesis put forward by Trivers [21]. Recent work reporting a link between sex determination systems and different proxies for sex-specific lifespan have been interpreted as supporting this hypothesis [9, 10]. Here, we specifically tested for the UXh by asking whether there is a correlation between the sex-gap in survival and the relative size of the sex chromosomes (X/Z relative to Y/W and autosomes; Figure 1).…”

“…Despite its long history and intuitive appeal, our results suggest that the UXh may in fact not be a fundamental driver of sex-specific mortality. Since it was first formulated, more than three decades ago, support for the UXh has been scant and indirect [1, 9, 10, 12] and, while this may be due to the inherent difficulties in testing this hypothesis, there are also frequently overlooked reasons to doubt it plays a major role in explaining sex-specific lifespans. For example, the fact that there is likely to be strong selection against big effect X-linked recessive mutations in nature [22], meaning that any mutations that do accumulate on the recombining chromosome should have relatively minor effects.…”

“…There are at least two reasons why sex chromosomes should directly contribute to the evolution of different female and male lifespans [9, 10]. First, the unguarded X hypothesis (UXh) predicts increased mortality of the heterogametic sex due to the expression of deleterious recessive mutations that accumulate in the non-recombining parts of the X (or Z) chromosome [10]. Because these mutations are masked in the homogametic sex, males are predicted to live longer than females in ZW systems (where males are the homogametic sex), and females longer than males in XY systems (where females are the homogametic sex).…”

“…This idea has received indirect support in the finding that adult sex-ratios are typically female-biased in tetrapods with XY systems, but male-biased in taxa with ZW systems, as expected if biased adult sex ratios result from sex-specific mortality [8]. A recent study further shows that the heterogametic sex tends to exhibit higher mean/maximum lifespan across a wide taxonomic range, but phylogenetic signal and sexual selection could contribute to explain this relationship [10]. In addition, recent experimental evidence shows that “unguarding” the X chromosome in females erases the sex gap in lifespan in Drosophila melanogaster [11, 12] but see [13].…”