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Identifying age-dependent trade-offs between reproductive effort and survival in wild organisms is central for understanding the evolutionary mechanisms of senescence. According to the disposable soma theory, early-life energy investments in reproduction compromise late-life investments in somatic maintenance – leading to senescence. Once thought to only be detectable in captive populations, senescence has recently been documented by several longitudinal studies of wild organisms. However, some reproductive traits that are used to quantify senescence may also be shaped by other age-dependent processes such as mating tactics. For instance, polygamy, which is often positively associated with age, may lead to reduced gamete size due to trade-offs between gamete quantity and quality. Here we investigate how mating behaviour and senescence are associated with reproductive trade-offs of female snowy plovers (Charadrius nivosus). Snowy plovers are long-lived shorebirds (longevity record: 19 years) that produce several nests each year, with females either being polyandrous and sequentially changing partners between breeding attempts or remaining monogamous between attempts. We examined how age, seasonality, and mating tactics affect within-female variation in egg volume using repeated measures collected over a 14-year period. Our results provide clear evidence for senescence in snowy plover females starting at three years of age. Furthermore, females laid smaller eggs in years when they were polyandrous compared to years when they were monogamous, with early- and late-season clutches having the smallest eggs. We suggest that individual female reproductive performance is regulated by flexible mating tactics and age- and season-dependent effects. Our findings highlight the existence of multiple trade-offs for female reproductive investments that likely shape individual variation in lifetime reproductive success. We encourage future research investigating reproductive senescence of wild populations to incorporate age-dependent reproductive investments in light of mating system dynamics.Impact SummaryWhy do organisms senesce at older ages? Life-history theory predicts that early life investments in reproduction compromise future investment opportunities for somatic repair, which leads to senescence. Earlier works assumed that senescence was only observable in captive populations due to the high degree of extrinsic mortality experienced by wild organisms. However, with the expansion of longitudinal studies collecting repeated measures from wild individuals, recent works have identified key insights into the selective processes driving patterns of senescence in nature. Here, we use a 14-year longitudinal mark-recapture dataset of snowy plovers (Charadrius nivosus) breeding in a wild subtropical population in western Mexico to investigate age-dependent trade-offs between female reproductive effort and performance. The snowy plover is a long-lived shorebird characterized by a flexible polyandrous mating system. This rare breeding behaviour represents a unique background for investigating senescence in light of between and within-individual variation in reproductive investment. Our study focused on age-dependent dynamics of egg volume – a convenient measure of a female’s intrinsic reproductive investment, particularly in birds with precocial chicks. We explored age-related correlates of within-female egg volume dynamics while controlling for among-female variation and the confounding effect of trait-dependent (dis)appearance of young (or old) females in the population. Our results show that egg volume expresses an early-life increase followed by a late-life decrease, indicative of reproductive senescence. Furthermore, females tended to lay smaller eggs in years during which they were polyandrous than in years when they were monogamous. Notably, polyandry was not associated with age. As expected, egg volume was highly repeatable within females and clutches. We conclude that age-dependent reproductive effort is an important component driving between- and within-individual variation in reproductive performance of facultatively polygamous species. We encourage future works studying reproductive senescence of wild populations to incorporate age-dependent reproductive investment and mating tactics.

Anisogamy is a central component of sex role evolution, however, the effect of female-female mating competition on egg size variation in polyandrous species is unclear. Moreover, egg size may also be shaped by age-dependent trade-offs between reproductive investments and somatic maintenance that are responsible for senescence. Here we investigate how mating behaviour and senescence are associated with egg size variation in female snowy plovers (Charadrius nivosus). Snowy plovers are long-lived shorebirds (longevity record: 20 years) that often produce several nests each year, with females either sequentially changing partners between breeding attempts or remaining monogamous between attempts. We examined how age, seasonality, body size, and mating behaviour relate to within- and between-female variation in egg volume using repeated measures collected over a 15-year period. We found no evidence of reproductive senescence in egg volume in snowy plover females. Rather, egg volume, polyandry, and re-nesting were strongly linked to breeding phenology: early breeding females had a higher likelihood of being polyandrous or replacing failed clutches, yet these individuals laid smaller eggs likely due to physiological limitations associated with the early season. Older individuals and local recruits secured the earliest breeding opportunities in the season suggesting that prior experience could give an edge in the female-female competition for mates. Larger females laid the largest eggs, as expected, but there was no relationship between body size and lay date - implying that size may not provide an advantage in female-female competition. Our findings highlight the existence of several direct and indirect constraints on female reproductive investment that likely shape individual variation in lifetime reproductive success. Future research investigating reproductive senescence of wild populations should consider mating system dynamics when examining variation in reproductive investment.

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