Sons accelerate maternal aging in a wild mammal

Abstract

Aging, or senescence, is a progressive deterioration of physiological function with age. It leads to age-related declines in reproduction (reproductive senescence) and survival (actuarial senescence) in most organisms. However, senescence patterns can be highly variable across species, populations, and individuals, and the reasons for such variations remain poorly understood. Evolutionary theories predict that increases in reproductive effort in early life should be associated with accelerated senescence, but empirical tests have yielded mixed results. Although in sexually size-dimorphic species offspring of the larger sex (typically males) commonly require more parental resources, these sex differences are not currently incorporated into evolutionary theories of aging. Here, we show that female reproductive senescence varies with both the number and sex ratio of offspring weaned during early life, using data from a long-term study of bighorn sheep. For a given number of offspring, females that weaned more sons than daughters when aged between 2 and 7 y experienced faster senescence in offspring survival in old age. By contrast, analyses of actuarial senescence showed no cost of early-life reproduction. Our results unite two important topics in evolutionary biology: life history and sex allocation. Offspring sex ratio may help explain among-individual variation in senescence rates in other species, including humans.

Late-life costs of raising sons in bighorn sheep

“…The detection of costs in reproduction rather than survival aligns with findings in other long-lived vertebrates, where the variance in reproduction tends to be greater than that in survival, at least in prime-age individuals, making it easier to detect such costs (12). Further investigation revealed that the higher cost of raising males in early life arose through reductions in the survival of offspring produced in later life (7). The authors find no evidence that the frequency of breeding or offspring survival over the summer months was impacted by the sex ratio of lambs in early life.…”

“…1). In their study, Douhard et al (7) test these predictions and find that bighorn females who successfully weaned more offspring between 2 y and 7 y of age suffered more-rapid declines in reproductive success in later life. Importantly, for a given number of offspring weaned in early life, females that weaned more sons showed faster reproductive senescence.…”

“…Such individual heterogeneity may mask trade-offs at the population level (14), making age-related declines difficult to detect (15). Douhard et al (7) find that females with higher average reproductive success in later life also tend to live longer. Using statistical tools to control for this "selective disappearance" of poorer breeders enabled them to better capture senescence among the survivors.…”

Female reproductive senescence across mammals: A high diversity of patterns modulated by life history and mating traits

“…However, whether the quality and quantity of resources available in the environment mitigate the reproductive ageing cost of these functional declines remains to be investigated. Moreover, following a resource-based allocation trade-off, a high reproductive effort during early life can be paid in terms of increased reproductive senescence (Douhard et al, 2020;Lemaître et al, 2015;Nussey et al, 2006). For instance, it has been suggested that the early onset of reproductive senescence reported in domestic mammals might be due to the strong artificial selection for a high reproductive effort during early life in domestic animals (Mysterud et al, 2002for sheep, Grange et al 2009 for horses, Equus caballus).…”

Understanding Reproductive Aging in Wildlife to Improve Animal Conservation and Human Reproductive Health

“…In bighorn sheep ( Ovis canadensis ), there is no consequence of early life reproduction; however, for a given number of offspring, females that weaned more sons than daughters experience earlier senescence ( Douhard et al, 2020 ). Offspring sex ratio could help explain among-individual variation in senescence rates, perhaps in other species, including humans.…”