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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.

SUBMITTER: Douhard M

PROVIDER: S-EPMC7060686 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Sons accelerate maternal aging in a wild mammal.

Douhard Mathieu M Festa-Bianchet Marco M Pelletier Fanie F

Proceedings of the National Academy of Sciences of the United States of America 20200218 9

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 s ...[more]

PMID: 32071199

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Project description:Intergenerational plasticity or parental effects-when parental environments alter the phenotype of future generations-can influence how organisms cope with environmental change. An intriguing, underexplored possibility is that sex-of both the parent and the offspring-plays an important role in driving the evolution of intergenerational plasticity in both adaptive and non-adaptive ways. Here, we evaluate the potential for sex-specific parental effects in a freshwater population of three-spined sticklebacks Gasterosteus aculeatus by independently and jointly manipulating maternal and paternal experiences and separately evaluating their phenotypic effects in sons versus daughters. We tested the adaptive hypothesis that daughters are more responsive to cues from their mother, whereas sons are more responsive to cues from their father. We exposed mothers, fathers or both parents to visual cues of predation risk and measured offspring antipredator traits and brain gene expression. Predator-exposed fathers produced sons that were more risk-prone, whereas predator-exposed mothers produced more anxious sons and daughters. Furthermore, maternal and paternal effects on offspring survival were non-additive: offspring with a predator-exposed father, but not two predator-exposed parents, had lower survival against live predators. There were also strong sex-specific effects on brain gene expression: exposing mothers versus fathers to predation risk activated different transcriptional profiles in their offspring, and sons and daughters strongly differed in the ways in which their brain gene expression profiles were influenced by parental experience. We found little evidence to support the hypothesis that offspring prioritize their same-sex parent's experience. Parental effects varied with both the sex of the parent and the offspring in complicated and non-additive ways. Failing to account for these sex-specific patterns (e.g. by pooling sons and daughters) would have underestimated the magnitude of parental effects. Altogether, these results draw attention to the potential for sex to influence patterns of intergenerational plasticity and raise new questions about the interface between intergenerational plasticity and sex-specific selective pressures, sexual conflict and sexual selection.

Dataset Information

Sons accelerate maternal aging in a wild mammal.

Publications

Sons accelerate maternal aging in a wild mammal.

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