Sex differences in adult lifespan and aging rates of mortality across wild mammals

Lemaître, Jean François; Ronget, Victor; Tidière, Morgane; Allainé, Dominique; Berger, Vérane; Cohas, Aurélie; Colchero, Fernando; Conde, Dalia Amor; Garratt, Michael; Liker, András; Marais, Gabriel; Scheuerlein, Alexander; Székely, Tamás; Gaillard, Jean Michel

doi:10.1073/pnas.1911999117

Cited by 221 publications

(232 citation statements)

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“…Alike humans or laboratory rodents, there is compelling evidence that mammalian males in the wild display shorter lives than females (Lemaître et al 2020c), as predicted by several (and non-mutually exclusive) evolutionary theories (e.g. heterogametic sex hypothesis, mother's curse hypothesis, sex differences in life history strategies, see Austad and Fischer 2016;Marais et al 2018 for reviews).…”

Section: Discussionmentioning

confidence: 99%

“…telomere dynamics in Seychelle warblers, Acrocephalus sechellensis, Hammers et al, 2019). In addition, while mammalian females generally live longer than males in the wild (Lemaître et al 2020c), as commonly observed in humans or laboratory rodents (Austad and Fischer 2016;Zarulli et al 2018), the exact mechanisms modulating these sex differences in survival are yet to be deciphered (Tower 2017;Marais et al 2018). In that context, the focus on wild populations can be particularly relevant as the magnitude of sex differences in lifespan is likely modulated by environmental conditions, in interaction with the sex differences in genetic background (Lemaître et al 2020c;Tidière et al 2020).…”

Section: Introductionmentioning

confidence: 99%

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Epigenetic clock and DNA methylation studies of roe deer in the wild

Lemaître¹,

Rey²,

Gaillard³

et al. 2020

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DNA methylation-based biomarkers of aging (epigenetic clocks) promise to lead to new insights in the evolutionary biology of ageing. Relatively little is known about how the natural environment affects epigenetic aging effects in wild species. In this study, we took advantage of a unique long-term (>40 years) longitudinal monitoring of individual roe deer (Capreolus capreolus) living in two wild populations (Chize and Trois Fontaines, France) facing different ecological contexts to investigate the relationship between chronological age and levels of DNA methylation (DNAm). We generated novel DNA methylation data from n=90 blood samples using a custom methylation array (HorvathMammalMethylChip40). We present several three DNA methylation-based estimators of age (DNAm or epigenetic age), which were trained in males, females, and both sexes combined. We investigated how sex differences influenced the relationship between DNAm age and chronological age through the use of sex-specific epigenetic clocks. Our results highlight that both populations and sex influence the epigenetic age, with the bias toward a stronger male average age acceleration (i.e. differences between epigenetic age and chronological ages) particularly pronounced in the population facing harsh environmental conditions. Further, we identify the main sites of epigenetic alteration that have distinct aging patterns across the two sexes. These findings open the door to promising avenues of research at the crossroad of evolutionary biology and biogerontology.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Epigenetic clock and DNA methylation studies of roe deer in the wild

Lemaître¹,

Rey²,

Gaillard³

et al. 2020

Preprint

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“…Earlier works assumed that senescence was only observable in captive populations due to the high degree of extrinsic mortality experienced by pre-senescent individuals in the wild through predation, disease, or resource shortages (Kirkwood & Rose, 1991;Bronikowski & Promislow, 2005). 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 (e.g., Bowen et al, 2006;Nussey et al, 2006Nussey et al, , 2008Bouwhuis et al, 2009;Schroeder et al, 2012;Zhang et al, 2015;Warner et al, 2016;Dingemanse et al, 2020;Lemaître et al, 2020). A key issue for studying senescence in wild populations is that stochastic extrinsic mortality reduces the frequency of observable individuals in older age classes, hence making it challenging to disentangle among-vs. within-individual age-dependent variation -a phenomenon known as "selective disappearance" (Nussey et al, 2008;van de Pol & Wright, 2009).…”

Section: Impact Summary (297 Words)mentioning

confidence: 99%

“…Malemale competition through combat can lead to increased somatic deterioration or damage (Bonduriansky et al, 2008). Hence, in polygynous species, strong sexual selection and intrasexual competition are thought to accelerate senescence and may lead to high mortality rates in males (Clutton-Brock & Isvaran, 2007;Bonduriansky et al, 2008;Maklakov & Lummaa, 2013;Greiner et al, 2014;Beirne et al, 2015;Tidière et al, 2015; but see Lemaître et al, 2020). Conversely, in monogamous species where sexual selection is not as intense, senescence acts similarly on both males and females (Clutton-Brock & Isvaran, 2007) or shows only moderate biases towards either sex (e.g., Lecomte et al, 2010;Froy et al, 2017;Tompkins & Anderson, 2019).…”

Section: Impact Summary (297 Words)mentioning

confidence: 99%

Egg size variation in the context of polyandry: a case study using long-term field data from snowy plovers

Eberhart‐Hertel¹,

Rodrigues²,

Krietsch³

et al. 2020

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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.

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“…The physiological hypothesis emphasises that the interactions between sex hormones and the immune system render one sex more susceptible to infection and disease [28]. For example, in mammals, males have consistently weaker immune competence than females, and this correlates with male-biased disease prevalence, mortality, and female-biased adult sex ratio [29,30]. On the other hand, the behavioural hypothesis posits that sexual differences in behaviour may cause sex-specific exposure to pathogens [31].…”

Section: Introductionmentioning

confidence: 99%

How do biases in sex ratio and disease characteristics affect the spread of sexually transmitted infections?

Halimubieke

Pirrie

Székely

et al. 2020

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AbstractThe epidemiology of sexually transmitted infections (STIs) is inherently linked to host mating dynamics. Studies across many taxa show that adult sex ratio, a major determinant of host mating dynamics, is often skewed – sometimes strongly – toward males or females. However, few predictions exist for the effects of skewed sex ratio on STI epidemiology, and none when coupled with sex biased disease characteristics. Here we use mathematical modelling to examine how interactions between sex ratio and disease characteristics affect STI prevalence in males and females. Notably, we find that while overall disease prevalence peaks at equal sex ratios, prevalence per sex peaks at skewed sex ratios. Furthermore, disease characteristics, sex-biased or not, drive predictable differences in male and female STI prevalence as sex ratio varies, with higher transmission and lower virulence generally increasing differences between the sexes for a given sex ratio. These findings may be due to a balance between increased per-capita mating in the less common sex, and a reduction in mating rate – hence disease prevalence – at the population level. Our work reveals new insights into how STI prevalence in males and females depends on a complex interaction between host population demography and disease characteristics.

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Sex differences in adult lifespan and aging rates of mortality across wild mammals

Cited by 221 publications

References 70 publications

Epigenetic clock and DNA methylation studies of roe deer in the wild

Epigenetic clock and DNA methylation studies of roe deer in the wild

Egg size variation in the context of polyandry: a case study using long-term field data from snowy plovers

How do biases in sex ratio and disease characteristics affect the spread of sexually transmitted infections?

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