Exposure to female olfactory cues hastens reproductive ageing and increases mortality when mating in male mice.

Theories of ageing predict that investment in reproduction will trade-off against survival and later-life reproduction. Recent evidence from invertebrates suggests that just perceiving cues of a potential mate's presence can reduce lifespan, particularly in males, and that activation of neuroendocrine reward pathways associated with mating can alleviate these effects. Whether similar effects occur in vertebrates remains untested. We tested whether exposure to olfactory cues from the opposite sex would influence mortality and reproductive senescence in male mice. We observed that males exposed to female olfactory cues from middle- to old age (from 10 to 24 months of age) showed reduced late-life fertility, irrespective of whether they had also been allowed to mate with females earlier in life. Males that were exposed to female odours in conjunction with mating also showed an increased mortality rate across the exposure period, indicating that olfactory cues from females can increase male mortality in some environments. Our results show that exposure to female odours can influence reproductive ageing and mortality in male mice, highlighting that sensory perception of mates may be an important driver of life-history trade-offs in mammals.

Access to females and early life castration individually extend maximal but not median lifespan in male mice.

Investment in reproduction is predicted to accelerate ageing, but the link between reproductive investment and lifespan can be sex- and context-specific. In mammals, female reproductive costs are linked to pregnancy and lactation, but in males substantial reproductive allocation is required for a range of pre- and post-copulatory reproductive traits. Such traits include male-specific increased body size, olfactory signalling and territory defence-traits often expressed under androgen-dependent control. In this experimental study, we explored how reproduction influences lifespan in male mice, contrasting this to the established lifespan costs of reproduction in females. In a 2 × 2 factorial design, we gave either castrated or intact males (factor 1) access to a female or a male cage-mate across their entire life (factor 2). Neither castration nor access to females influenced median lifespan in male mice, but maximal lifespan was increased by either castration or reproduction when compared to intact males housed in male groups (standard male housing conditions). In females, mating significantly reduced lifespan, and while both sexes had similar lifespans in non-reproductive environments, males had a much longer lifespan when allowed mating. This data highlights the sex-specific nature of social environments and reproduction on lifespan, and the role of these conditions in promoting sexual dimorphism in ageing.

Mating in the absence of fertilization promotes a growth-reproduction versus lifespan trade-off in female mice.

Trade-offs between growth, reproduction, and lifespan constrain animal life histories, leading to evolutionary diversification of life history cycles in different environments. In female mammals, gestation and lactation are expected to impose the major costs of reproduction, driving reproductive trade-offs, although mating also requires interactions with males that could themselves influence life history. Here we show that a male's presence by itself leads to lifelong alterations in life history in female mice. Housing C57BL/6J female mice with sterilized males early in life led to an increase in body weight, an effect that persisted across life even when females were later allowed to produce pups. We found that those females previously housed with sterile males also showed enhanced late-life offspring production when allowed to reproduce, indicating that earlier mating can influence subsequent fecundity. This effect was the opposite to that seen in females previously housed with intact males, which showed the expected trade-off between early-life and late-life reproduction. However, housing with a sterile male early in life came at a cost to lifespan, which was observed in the absence of females ever undergoing fertilization. Endocrinologically, mating also permanently reduced the concentration of circulating prolactin, a pituitary hormone influencing maternal care. Changes in hormone axes that influence reproduction could therefore help alter life history allocation in response to opposite-sex stimuli. Our results demonstrate that mating itself can increase growth and subsequent fecundity in mammals, and that responses to sexual stimuli could account for some lifespan trade-offs normally attributed to pregnancy and lactation.