Does sexual selection shape sex differences in longevity and senescence patterns across vertebrates? A review and new insights from captive ruminants

Abstract

In most mammals, both sexes display different survival patterns, often involving faster senescence in males. Being under intense sexual competition to secure mating opportunities, males of polygynous species allocate resources to costly behaviors and conspicuous sexual traits, which might explain these observed differences in longevity and senescence patterns. However, comparative studies performed to date have led to conflicting results. We aimed to resolve this problem by first reviewing case studies of the relationship between the strength of sexual selection and age-specific survival metrics. Then, we performed a comprehensive comparative analysis to test whether such relationships exist among species of captive ruminants. We found that the strength of sexual selection negatively influenced the onset of actuarial senescence in males, with males senescing earlier in polygynous than in monogamous species, which led to reduced male longevity in polygynous species. Moreover, males of territorial species senesced earlier but slower, and have a shorter longevity than males of species displaying other mating tactics. We detected little influence of the strength of sexual selection on the rate of actuarial senescence. Our findings demonstrate that the onset of actuarial senescence, rather than its rate, is a side effect of physiological mechanisms linked to sexual selection, and potentially accounts for observed differences in longevity.

Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals

“…In addition, we show that both males and females respond similarly to captive conditions. Such a discovery provides indirect evidence that the genuine sex differences in survival patterns in mammalian species subjected to high sexual selection23 involve physiological mechanisms and cannot only be explained by higher susceptibility of males to environmental conditions.…”

The Williams' legacy: A critical reappraisal of his nine predictions about the evolution of senescence

“…; Tidière et al. ). The study of these differences is a timely topic in both biogerontology and evolutionary biology, probably because it provides a better understanding of the fitness costs inherent to the sex‐specific reproductive tactics (Bonduriansky et al.…”

“…; Clutton‐Brock and Isvaran ; Austad ; Tidière et al. ), especially when environmental conditions are harsh (Toïgo and Gaillard ). This bias is generally considered to be a direct consequence of the male involvement into intra‐ and/or intersexual competition (Bonduriansky et al.…”

“…The critical role of the sex‐differences in the physiological system is reinforced by the fact that sex‐differences in mortality are also observed in captive populations, even if zoological gardens generally prevent aggressive contests between conspecific males (Tidière et al. ).…”

Reproductive costs in terrestrial male vertebrates: insights from bird studies

“…effort in wild males than females [7]. Also, while it has become an accepted notion that reproduction is costly for males as well [8][9][10], studies dealing with costs of reproduction in males are often rooted in the theory of sexual selection and therefore refer to the cost of producing or maintaining sexual traits on future survival [8] (see [11] for a recent review on the relationship between strength of sexual selection and age-specific survival patterns across vertebrates). Investigating reproductive costs in males specifically through the covariations between life-history traits (also called direct fitness traits sensu Roff [4], i.e.…”