Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals

Tidière, Morgane; Gaillard, Jean‐Michel; Berger, Vérane; Müller, Dennis; Lackey, Laurie Bingaman; Giménez, Olivier; Clauss, Marcus; Lemaître, Jean‐François

doi:10.1038/srep36361

Cited by 152 publications

(174 citation statements)

References 35 publications

Supporting

Mentioning

154

Contrasting

Unclassified

Order By: Relevance

“…The primary aim of our study is to apply a systematic meta‐analytical approach to evaluate the evidence for the occurrence of immunosenescence in wild vertebrates (amniotes). We include free‐living and captive populations for comparison to gain insight into what extent environmental variation can explain variation in immunosenescence (for example, actuarial senescence patterns differ between wild and captive (zoo) populations; Tidière et al ). Senescence is the result of an increase in susceptibility to environmental and physiological challenges with age (Medawar ), including infections and disease, which can be difficult to simulate in captivity (Pedersen & Babayan ).…”

Section: Introductionmentioning

confidence: 99%

Immunosenescence in wild animals: meta‐analysis and outlook

et al. 2019

View full text Add to dashboard Cite

Immunosenescence, the decline in immune defense with age, is an important mortality source in elderly humans but little is known of immunosenescence in wild animals. We systematically reviewed and meta‐analysed evidence for age‐related changes in immunity in captive and free‐living populations of wild species (321 effect sizes in 62 studies across 44 species of mammals, birds and reptiles). As in humans, senescence was more evident in adaptive (acquired) than innate immune functions. Declines were evident for cell function (antibody response), the relative abundance of naïve immune cells and an in vivo measure of overall immune responsiveness (local response to phytohaemagglutinin injection). Inflammatory markers increased with age, similar to chronic inflammation associated with human immunosenescence. Comparisons across taxa and captive vs free‐living animals were difficult due to lack of overlap in parameters and species measured. Most studies are cross‐sectional, which yields biased estimates of age‐effects when immune function co‐varies with survival. We therefore suggest longitudinal sampling approaches, and highlight techniques from human cohort studies that can be incorporated into ecological research. We also identify avenues to address predictions from evolutionary theory and the contribution of immunosenescence to age‐related increases in disease susceptibility and mortality.

show abstract

Section: Introductionmentioning

confidence: 99%

Immunosenescence in wild animals: meta‐analysis and outlook

et al. 2019

View full text Add to dashboard Cite

show abstract

“…First, actuarial senescence is a nearly ubiquitous process in the living world (Nussey, Froy, Lemaitre, Gaillard, & Austad, ; Shefferson, Jones, & Salguero‐Gómez, ). Second, patterns of senescence can be highly variable among species (Colchero et al, ; Jones et al, ; Tidière et al, ). Comparative analyses have shown that senescence patterns across multicellular organisms can be predicted by ecological traits, lifestyles and covariation among life‐history traits (Gaillard et al, ; Péron, Gimenez, Charmantier, Gaillard, & Crochet, ; Ricklefs, ; Salguero‐Gómez & Jones, ).…”

Section: Introductionmentioning

confidence: 99%

Population position along the fast–slow life‐history continuum predicts intraspecific variation in actuarial senescence

Cayuela

Lemaître

Bonnaire

et al. 2020

Journal of Animal Ecology

View full text Add to dashboard Cite

Patterns of actuarial senescence can be highly variable among species. Previous comparative analyses revealed that both age at the onset of senescence and rates of senescence are linked to position of a species along the fast–slow life‐history continuum. As there are few long‐term datasets of wild populations with known‐age individuals, intraspecific (i.e. between‐population) variation in senescence is understudied and limited to comparisons of wild and captive populations of the same species, mostly birds and mammals. In this paper, we examined how population position along the fast–slow life‐history continuum affects intraspecific variation in senescence in an amphibian, Bombina variegata. We used capture–recapture data collected in four populations with contrasting life‐history strategies. Senescence trajectories were analysed using Bayesian capture–recapture models. We show that in populations with fast life histories the onset of actuarial senescence was earlier and individuals aged at a faster rate than individuals in populations with slow life histories. Our study provides one of the few empirical examples of among‐population variation in actuarial senescence patterns in the wild and confirms that the fast–slow life‐history gradient is associated with both macroevolutionary and microevolutionary patterns of actuarial senescence.

show abstract

“…A recent meta‐analysis of laboratory studies found no effect of early diet on life span (English & Uller, ), but the simplified environments of laboratory or captive studies may produce results different from those observed in the wild (Briga & Verhulst, ; Kawasaki, Brassil, Brooks, & Bonduriansky, ; Tidière et al., ). In addition, not all species are suitable for laboratory study.…”

Section: Introductionmentioning

confidence: 99%

Trophy hunting mediates sex‐specific associations between early‐life environmental conditions and adult mortality in bighorn sheep

Douhard

Festa‐Bianchet

Landes

et al. 2019

Journal of Animal Ecology

View full text Add to dashboard Cite

Environmental conditions during early development, from conception to sexual maturity, can have lasting consequences on fitness components. Although adult life span often accounts for much of the variation in fitness in long‐lived animals, we know little about how early environment affects adult life span in the wild, and even less about whether these effects differ between the sexes. Using data collected over 45 years from wild bighorn sheep (Ovis canadensis), we investigated the effects of early environment on adult mortality in both sexes, distinguishing between natural and anthropogenic sources of mortality. We used the average body mass of yearlings (at about 15 months of age) as a yearly index of environmental quality. We first examined sex differences in natural mortality responses to early environment by censoring harvested males in the year they were shot. We then investigated sex differences in the effects of early environment on overall mortality (natural and hunting mortality combined). Finally, we used path analysis to separate the direct influence of early environment from indirect influences, mediated by age at first reproduction, adult mass and horn length. As early environmental conditions improved, natural adult mortality decreased in both sexes, although for males the effect was not statistically supported. Sex differences in the effects of early environment on adult mortality were detected only when natural and hunting mortality were pooled. Males that experienced favourable early environment had longer horns as adults and died earlier because of trophy hunting, which does not mimic natural mortality. Females that experienced favourable early environment started to reproduce earlier and early primiparity was associated with reduced mortality, suggesting a silver‐spoon effect. Our results show that early conditions affect males and females differently because of trophy hunting. These findings highlight the importance of considering natural and anthropogenic environmental factors across different life stages to understand sex differences in mortality.

show abstract

Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals

Cited by 152 publications

References 35 publications

Immunosenescence in wild animals: meta‐analysis and outlook

Immunosenescence in wild animals: meta‐analysis and outlook

Population position along the fast–slow life‐history continuum predicts intraspecific variation in actuarial senescence

Trophy hunting mediates sex‐specific associations between early‐life environmental conditions and adult mortality in bighorn sheep

Contact Info

Product

Resources

About