Abstract
Males and females frequently differ in their rates of ageing, but the origins of these differences are poorly understood. Sex differences in senescence have been hypothesized to arise, because investment in intra-sexual reproductive competition entails costs to somatic maintenance, leaving the sex that experiences stronger reproductive competition showing higher rates of senescence. However, evidence that sex differences in senescence are attributable to downstream effects of the intensity of intra-sexual reproductive competition experienced during the lifetime remains elusive. Here, we show using a 35 year study of wild European badgers (Meles meles), that (i) males show higher body mass senescence rates than females and (ii) this sex difference is largely attributable to sex-specific downstream effects of the intensity of intra-sexual competition experienced during early adulthood. Our findings provide rare support for the view that somatic maintenance costs arising from intra-sexual competition can cause both individual variation and sex differences in senescence.
Highlights
Senescence, defined as within-individual physiological deterioration with age, has been detected in a wide variety of natural populations, but the causes of the often marked individual variation in senescence rates remain poorly understood [1]
The sex that experiences stronger intra-sexual reproductive competition often shows higher mean mortality rates, which may thereby differentially weaken the force of selection against deleterious mutations or antagonistically pleiotropic genes acting in late life in that sex [12], leading to the evolution of faster senescence rates and shorter lifespans [10]
As overt intra-sexual reproductive competition appears to be more intense among male European badgers than females, the observed sex difference in late-life body mass dynamics is consistent with a role for intra-sexual reproductive competition in generating sex differences in senescence rates, and echoes previous reports of higher senescence rates among males in polygynous species [3,5,16]
Summary
Senescence, defined as within-individual physiological deterioration with age, has been detected in a wide variety of natural populations, but the causes of the often marked individual variation in senescence rates remain poorly understood [1]. It has been hypothesized that individuals may suffer resource allocation trade-offs between the expression of competitive morphologies and behaviour and their simultaneous allocation to somatic maintenance, which might thereby lead to steeper senescent declines later in life in the sex that experiences stronger intrasexual competition [11,14] This perspective highlights the potential limitations of focusing solely on the implications of mortality rates, and predicts instead a direct effect of the intensity of intra-sexual competition experienced during early adulthood on both individual variation in senescence rates and the extent of any sex difference observed in senescence rates [1]. We test two key predictions: if somatic maintenance costs arising from intra-sexual reproductive competition play a key role in generating sex differences in senescence rates: (i) male European badgers should show a faster rate of late-life decline in body mass than females and (ii) this sex 2 difference in senescence rate should be attributable in part to downstream effects of the intensity of intra-sexual reproductive competition experienced in early adulthood. We apply a linear mixed-model approach throughout, which allows us to examine changes in body mass with chronological age while controlling for selective disappearance and terminal effects that might otherwise obscure or exaggerate patterns of senescence [32]
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