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

Lemaître, Jean‐François; Ronget, Victor; Gaillard, Jean‐Michel

doi:10.1016/j.mad.2020.111377

Cited by 40 publications

(64 citation statements)

References 120 publications

(137 reference statements)

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“…For example, long‐lived painted turtles, considered to lack senescence, were revealed to senesce in the wild, though the onset of senescence was postponed compared to animals that cease growing soon after sexual maturation (Warner et al., 2016). Limited knowledge of reproductive senescence in some organisms, including model organisms, prevents a solid understanding of the mechanisms related to decline in this key fitness component (Lemaitre et al., 2020).…”

Section: Discussionmentioning

confidence: 99%

Reproductive senescence in a short‐lived fish

Žák

Reichard

2020

Journal of Animal Ecology

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Reproductive senescence is an age‐associated decline in reproductive performance, which often arises as a trade‐off between current and future reproduction. Given that mortality is inevitable, increased allocation into current reproduction is favoured despite costs paid later in life. This assumption is violated in organisms with post‐maturity growth whose reproductive output increases long after maturity. While reproductive senescence is frequently studied in animals with determinate growth at maturity, such as insects or mammals, we have very limited understanding of reproductive senescence in organisms with an extensive post‐maturity growth period. The fact that many post‐maturity growers experience strong adult mortality leads to conflicting expectations for reproductive senescence. The aim of this study was to investigate how co‐occurrence of rapid life history and post‐maturity growth mould reproductive senescence in a short‐lived killifish, Nothobranchius furzeri, using longitudinal data on laboratory and wild‐type populations. We followed the individual fecundity, fertility and fertilization of 132 singly housed fish from the perspectives of chronological and biological age. At the onset of senescence, the sex‐specific contribution to decrease in fertilization capacity was investigated. Allocation trade‐offs were estimated through the association between reproductive parameters and life span, and between early‐life and late‐life fecundity. We demonstrate that female fecundity increased steadily after maturity and reproductive senescence occurred long after the growth asymptote. The prime age for fecundity coincided with 50% female survival and consequent decline in fecundity implies an association with somatic deterioration. Reproductive senescence in fertilization rate was stronger in females than in males. Females with high early fecundity experienced a long life span and high late‐life fecundity, discounting the role of allocation trade‐offs in reproductive senescence. The present study reports a clear case of reproductive senescence in a fish with a long post‐maturation growth period, unusually rapid development and short life span. The onset of reproductive senescence was postponed compared to animals that cease growing at sexual maturity. Fish and other animals with post‐maturity growth have long been considered insusceptible to ageing but this conclusion may be related to the previous lack of longitudinal data rather than to the absence of reproductive senescence in such organisms.

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Section: Discussionmentioning

confidence: 99%

Reproductive senescence in a short‐lived fish

Žák

Reichard

2020

Journal of Animal Ecology

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“…due to extra-pair offspring often produced by males; [27]) and has been reported in a much higher number of vertebrate species, we focus on the reproductive ageing of females in both birds and mammals. Reproductive senescence parameters of 101 wild or semi-captive mammal species were taken from [28]. This data set includes the presence/absence of reproductive senescence and, for species with evidence of senescence, the age at onset and the rate of reproductive senescence.…”

Section: Methodsmentioning

confidence: 99%

“…number of female offspring alive at birth that are produced by a female of age x, tabulated as m x in a life table) extracted from published life tables or graphs using WebPlotDigitizer (https://automeris.io/WebPlotDigitizer/). The acquisition of age-specific reproductive data for mammals is fully detailed in [28]. In cooperatively breeding mammals, age-specific reproductive data were collected for dominant females (e.g.…”

Section: Methodsmentioning

confidence: 99%

“…We included those studies in our analyses and controlled for the effect of standardization (yes/no). When reproductive data were reported for multiple populations of the same species, we only included the study with the largest sample size, as done in mammals [28]. To estimate senescence parameters, we accounted for differences in the age-specific sample sizes, as done in mammals [28].…”

Section: Methodsmentioning

confidence: 99%

“…When reproductive data were reported for multiple populations of the same species, we only included the study with the largest sample size, as done in mammals [28]. To estimate senescence parameters, we accounted for differences in the age-specific sample sizes, as done in mammals [28]. We used the original age-specific sample size when reported in the original studies, and we calculated the number of females expected to be alive at age x from the observed age distribution of females when sample sizes were not reported.…”

Section: Methodsmentioning

confidence: 99%

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Is degree of sociality associated with reproductive senescence? A comparative analysis across birds and mammals

Vágási

Vincze

Lemaître

et al. 2020

Preprint

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Our understanding on how widespread reproductive senescence is in the wild and how the onset and rate of reproductive senescence vary among species in relation to life histories and lifestyles is currently limited. More specifically, whether the species-specific degree of sociality is linked to the occurrence, onset and rate of reproductive senescence remains unknown. Here, we investigate these questions using phylogenetic comparative analyses across 36 bird and 101 mammal species encompassing a wide array of life histories, lifestyles and social traits. We found that female reproductive senescence (1) is widespread and occurs with similar frequency (about two thirds) in birds and mammals; (2) occurs later in life and is slower in birds than in similar-sized mammals; (3) occurs later in life and is slower with an increasingly slower pace of life in both vertebrate classes; and (4) is only weakly associated, if any, with the degree of sociality in both classes after accounting for the effect of body size and pace of life. However, when allowing for species differences in pace of life, a higher degree of sociality was associated with later and weaker reproductive senescence in females, which suggests that degree of sociality is indirectly related to reproductive senescence via the pace of life.Subject Areasecology, evolution

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Influence of environmental conditions on population growth and age‐specific vital rates of a long‐lived primate species in two contrasted habitats

et al. 2023

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As wildlife is increasingly affected by environmental change, identifying how vital rates vary with ecological factors is essential to predict the consequences of environmental perturbations on wild population dynamics. We explored the effects of habitat constraints on the demographic and life history patterns of two Barbary macaque (Macaca sylvanus) populations living in two contrasted habitats in Algeria. Using 11 years of field data, we estimated age‐specific survival rates of females and of infants of both sexes, as well as female reproduction rates. We investigated how these vital rates were influenced by both intra‐ and inter‐habitat environmental variations. We parameterized age‐structured female‐only transition matrices and conducted a prospective analysis to estimate the contribution of each vital rate to the populations' asymptotic growth rates (λ). A retrospective analysis (LTRE, Life Table Response Experiment) was also conducted to determine how each vital rate contributed to the observed differences in λ between populations. The macaques exhibited common patterns of survival and reproduction (low rates at young ages, and then high and stable until a decrease at old ages), with first evidence of both actuarial and reproductive senescence. Both populations were growing. In both populations, adult and immature survival had the highest elasticities, and remained stable in changing environmental conditions. By contrast, infant survival and female reproduction had low elasticities, and varied more with environmental variations. As Barbary macaque habitats are increasingly degrading, we provide robust estimates of their vital rates with conservation implications, in particular to predict population responses to anthropogenic perturbations.

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

Cited by 40 publications

References 120 publications

Reproductive senescence in a short‐lived fish

Reproductive senescence in a short‐lived fish

Is degree of sociality associated with reproductive senescence? A comparative analysis across birds and mammals

Influence of environmental conditions on population growth and age‐specific vital rates of a long‐lived primate species in two contrasted habitats

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