Early-late life trade-offs and the evolution of ageing in the wild

Lemaître, Jean‐François; Berger, Vérane; Bonenfant, Christophe; Douhard, Mathieu; Gamelon, Marlène; Plard, Floriane; Gaillard, Jean‐Michel

doi:10.1098/rspb.2015.0209

Cited by 328 publications

(366 citation statements)

References 98 publications

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“…For example, greater resource allocation to early-life growth or reproduction is expected to come at a cost to late-life performance that can lead to age-related declines in reproduction and survival [i.e., disposable soma theory of aging (35)]. These patterns have been observed in many vertebrates (36), including reptiles (37,38), and could contribute to the reproductive and survival senescence observed here in C. picta.…”

Section: Discussionmentioning

confidence: 89%

Decades of field data reveal that turtles senesce in the wild

Warner

Miller

Bronikowski

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Lifespan and aging rates vary considerably across taxa; thus, understanding the factors that lead to this variation is a primary goal in biology and has ramifications for understanding constraints and flexibility in human aging. Theory predicts that senescence-declining reproduction and increasing mortality with advancing age-evolves when selection against harmful mutations is weaker at old ages relative to young ages or when selection favors pleiotropic alleles with beneficial effects early in life despite late-life costs. However, in many long-lived ectotherms, selection is expected to remain strong at old ages because reproductive output typically increases with age, which may lead to the evolution of slow or even negligible senescence. We show that, contrary to current thinking, both reproduction and survival decline with adult age in the painted turtle, Chrysemys picta, based on data spanning >20 y from a wild population. Older females, despite relatively high reproductive output, produced eggs with reduced hatching success. Additionally, age-specific mark-recapture analyses revealed increasing mortality with advancing adult age. These findings of reproductive and mortality senescence challenge the contention that chelonians do not age and more generally provide evidence of reduced fitness at old ages in nonmammalian species that exhibit long chronological lifespans.aging | lifespan | painted turtle | reproduction | senescence W hy do some organisms show little to no signs of aging as they get older, whereas others exhibit substantial physiological deterioration and reproductive senescence with advancing age (1, 2)? This question has motivated many studies of aging in the wild, ranging from reviews of demographic aging (3, 4) to compilations of mechanistic studies (e.g., ref. 5 and references therein). Senescence should evolve when selection is weaker on deleterious traits expressed at an old age relative to those expressed at a young age (6). Indeed, mutations with senescent effects can persist because of a tradeoff between beneficial effects early in life and pleiotropic detrimental effects late in life (7,8). Importantly, the persistence of age-specific deleterious mutations will therefore be influenced by levels and sources of extrinsic mortality (e.g., predation, resource scarcity, infectious disease) and the particular ages at which extrinsic sources cause death (9, 10). For example, the onset of physiological or reproductive deterioration is expected to occur relatively early in populations exposed to high levels of extrinsic mortality of adults. Accordingly, such organisms are expected to evolve rapid development/growth, high reproductive effort at young ages, and a shortened lifespan. For species or populations that experience low extrinsic mortality rates, physiological and reproductive function are expected to decline more slowly with advancing age or with a delay in the onset of senescent decline (7). Moreover, such age-specific selection dynamics can result in negligible (11) and even negative ...

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Section: Discussionmentioning

confidence: 89%

Decades of field data reveal that turtles senesce in the wild

Warner

Miller

Bronikowski

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Therefore, it would be particularly interesting to compare both males and females in the same study. Moreover, it is noteworthy that males that do not exhibit direct reproductive costs may pay a cost later in life [71], or may suffer from other types of costs, such as intergenerational or cumulative costs of reproduction (see electronic supplementary material, section S1).…”

Section: Tests Of Direct Costs Of Reproduction In Malesmentioning

confidence: 99%

Reproductive costs in terrestrial male vertebrates: insights from bird studies

2016

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Reproduction requires resources that cannot be allocated to other functions resulting in direct reproductive costs (i.e. trade-offs between current reproduction and subsequent survival/reproduction). In wild vertebrates, direct reproductive costs have been widely described in females, but their occurrence in males remains to be explored. To fill this gap, we gathered 53 studies on 48 species testing direct reproductive costs in male vertebrates. We found a trade-off between current reproduction and subsequent performances in 29% of the species and in every clade. As 73% of the studied species are birds, we focused on that clade to investigate whether such trade-offs are associated with (i) levels of paternal care, (ii) polygyny or (iii) pace of life. More precisely for this third question, it is expected that fast species (i.e. short lifespan, early maturity, high fecundity) pay a cost in terms of survival, whereas slow species (with opposite characteristics) do so in terms of fecundity. Our findings tend to support this hypothesis. Finally, we pointed out the potential confounding effects that should be accounted for when investigating reproductive costs in males and strongly encourage the investigation of such costs in more clades to understand to what extent our results are relevant for other vertebrates.

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“…Second, individuals born in poor environmental conditions may suffer from increased costs of reproduction during early adulthood [26]. The disposable soma theory predicts that increased reproductive effort during early adulthood should be accompanied by reductions in late-life performance [32,33]. However, costs of reproduction can only be evident among low-quality individuals that consistently acquire less resources than high-quality individuals [34].…”

Section: Introductionmentioning

confidence: 99%

The influence of weather conditions during gestation on life histories in a wild Arctic ungulate

et al. 2016

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The internal predictive adaptive response (internal PAR) hypothesis predicts that individuals born in poor conditions should start to reproduce earlier if they are likely to have reduced performance in later life. However, whether this is the case remains unexplored in wild populations. Here, we use longitudinal data from a long-term study of Svalbard reindeer to examine age-related changes in adult female life-history responses to environmental conditions experienced in utero as indexed by rain-on-snow (ROS utero ). We show that females experiencing high ROS utero had reduced reproductive success only from 7 years of age, independent of early reproduction. These individuals were able to maintain the same annual reproductive success between 2 and 6 years as phenotypically superior conspecifics that experienced low ROS utero . Young females born after high ROS utero engage in reproductive events at lower body mass (about 2.5 kg less) than those born after low ROS utero . The mean fitness of females that experienced poor environmental conditions in early life was comparable with that of females exposed to good environmental conditions in early life. These results are consistent with the idea of internal PAR and suggest that the life-history responses to early-life conditions can buffer the delayed effects of weather on population dynamics.

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Early-late life trade-offs and the evolution of ageing in the wild

Cited by 328 publications

References 98 publications

Decades of field data reveal that turtles senesce in the wild

Decades of field data reveal that turtles senesce in the wild

Reproductive costs in terrestrial male vertebrates: insights from bird studies

The influence of weather conditions during gestation on life histories in a wild Arctic ungulate

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