Early and Adult Social Environments Shape Sex-Specific Actuarial Senescence Patterns in a Cooperative Breeder

Berger, Vérane; Lemaître, Jean‐François; Allainé, Dominique; Gaillard, Jean‐Michel; Cohas, Aurélie

doi:10.1086/699513

Cited by 39 publications

(40 citation statements)

References 78 publications

(104 reference statements)

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“…Incumbent dominants can maintain long tenures sheltered from extrinsic mortality in large groups with dedicated sentinels (Cram et al, 2018), and this buffering effect of group living might be enough to prevent age-dependent increases in mortality risk in dominants irrespective of individual declines in condition. Alternatively, the presence and intensity of survival senescence might vary over time as environmental and demographic conditions modify the likelihood of different forms of intrinsic and extrinsic mortality (Berger, Lemaître, Allainé, Gaillard, & Cohas, 2018;Hämäläinen et al, 2014;Ronget, Garratt, Lemaître, & Gaillard, 2017), and might go undetected when these sources of variation are not accounted for in survival analyses. A failure to detect survival senescence could also reflect sampling effort when longitudinal studies have not been run for long enough to capture its onset (Péron, Gimenez, Charmantier, Gaillard, & Crochet, 2010).…”

Section: Discussionmentioning

confidence: 99%

Sex‐independent senescence in a cooperatively breeding mammal

Thorley

Duncan

Sharp

et al. 2020

Journal of Animal Ecology

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Researchers studying mammals have frequently interpreted earlier or faster rates of ageing in males as resulting from polygyny and the associated higher costs of reproductive competition. Yet, few studies conducted on wild populations have compared sex‐specific senescence trajectories outside of polygynous species, making it difficult to make generalized inferences on the role of reproductive competition in driving senescence, particularly when other differences between males and females might also contribute to sex‐specific changes in performance across lifespan. Here, we examine age‐related variation in body mass, reproductive output and survival in dominant male and female meerkats, Suricata suricatta. Meerkats are socially monogamous cooperative breeders where a single dominant pair virtually monopolizes reproduction in each group and subordinate group members help to rear offspring produced by breeders. In contrast to many polygynous societies, we find that neither the onset nor the rate of senescence in body mass or reproductive output shows clear differences between males and females. Both sexes also display similar patterns of age‐related survival across lifespan, but unlike most wild vertebrates, survival senescence (increases in annual mortality with rising age) was absent in dominants of both sexes, and as a result, the fitness costs of senescence were entirely attributable to declines in reproductive output from mid‐ to late‐life. We suggest that the potential for intrasexual competition to increase rates of senescence in females—who are hormonally masculinized and frequently aggressive—is offset by their ability to maintain longer tenures of dominance than males, and that these processes when combined lead to similar patterns of senescence in both sexes. Our results stress the need to consider the form and intensity of sexual competition as well as other sex‐specific features of life history when investigating the operation of senescence in wild populations.

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Section: Discussionmentioning

confidence: 99%

Sex‐independent senescence in a cooperatively breeding mammal

Thorley

Duncan

Sharp

et al. 2020

Journal of Animal Ecology

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“…For example, mating alone (either with a fertile or a sterilized male) can substantially increase the life span of queens of the ant Cardiocondyla obscurior; queens that received viable sperm also have increased fecundity (Schrempf, Heinze, & Cremer, 2005). As when having two or more helpers at birth (Berger et al, 2018).…”

Section: The Effect Of Social and Sexual Interactionsmentioning

confidence: 99%

Are trade‐offs really the key drivers of ageing and life span?

Cohen

Coste

et al. 2019

Functional Ecology

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1. Current thinking in life-history theory and the biology of ageing suggests that ageing rates, and consequently life spans, evolve largely as a function of trade-offs with reproduction. While various evolutionary constraints are generally acknowledged to exist, their potential role in determining ageing rates is rarely considered.2. This review integrates three types of information to assess the relative importance of constraints and trade-offs in shaping ageing rates: (a) empirical work on the presence of intraspecific trade-offs; (b) theoretical work on factors limiting the force of trade-offs; and (c) consideration of the biological mechanisms of ageing, as currently understood. 3. At the empirical level, evidence for intraspecific trade-offs is mixed, including some surprising failures to observe a trade-off in model organisms. At the theoretical level, the presence of multiple currencies and nonlinearity can weaken the strength and/or generality of trade-offs. Additionally, trade-offs among lowerlevel functions, such as between sources of mortality, can create constraints at higher organizational levels, for example such that reductions in reproduction are unable to produce decreases in ageing rate. In terms of ageing mechanisms, some mechanisms, such as the regulation of IGF-1 and related pathways, seem to agree quite well with trade-offs as a driving force; however, other mechanisms, such as dysregulation of the vertebrate stress response and stem cell exhaustion, seem more likely to impose constraints than to mediate trade-offs. 4. Taken together, these findings suggest that trade-offs alone are insufficient to understand how ageing rates evolve; instead, both trade-offs and constraints likely play important roles in shaping evolutionary patterns, with their relative importance varying across taxa. Accordingly, it is time to revisit the broad assumption that survival-reproduction trade-offs are the key force structuring much of lifehistory variation and the evolution of ageing rates. K E Y W O R D S ageing, constraint, cost of reproduction, disposable soma, life history, physiology, senescence, trade-off 154 | Functional Ecology COHEN Et al. | 155Functional Ecology COHEN Et al. | 157Functional Ecology COHEN Et al.

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“…Events early in life can have profound consequences for an animal's life history, health, and fitness (Berens, Jensen, & Nelson, ; Chaby, ; Lindström, ). An emerging body of work suggests that early life effects may also shape or be mediated by animal microbiomes (Berger, Lemaître, Allainé, Gaillard, & Cohas, ; Clarke, ; Laforest‐Lapointe & Arrieta, ; Martínez et al, ). The suitability of primate systems for understanding these processes stems from primatology's traditional focus on individual‐based research, and its long history of studying early life effects–especially maternal effects (e.g., Altmann & Alberts, ; Bailey, Lubach, & Coe, ; Bernstein, Setchell, Verrier, & Knapp, ).…”

Section: Key Areas Of Microbiome Science Where Primate Studies Can Comentioning

confidence: 99%

Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research

Björk

Dasari

Grieneisen

et al. 2019

American J Primatol

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To date, most insights into the processes shaping vertebrate gut microbiomes have emerged from studies with cross-sectional designs. While this approach has been valuable, emerging time series analyses on vertebrate gut microbiomes show that gut microbial composition can change rapidly from 1 day to the next, with consequences for host physical functioning, health, and fitness. Hence, the next frontier of microbiome research will require longitudinal perspectives. Here we argue that primatologists, with their traditional focus on tracking the lives of individual animals and familiarity with longitudinal fecal sampling, are well positioned to conduct research at the forefront of gut microbiome dynamics. We begin by reviewing some of the most important ecological processes governing microbiome change over time, and briefly summarizing statistical challenges and approaches to microbiome time series analysis. We then introduce five questions of general interest to microbiome science where we think fieldbased primate studies are especially well positioned to fill major gaps: (a) Do early life events shape gut microbiome composition in adulthood? (b) Do shifting social landscapes cause gut microbial change? (c) Are gut microbiome phenotypes heritable across variable environments? (d) Does the gut microbiome show signs of host aging? And (e) do gut microbiome composition and dynamics predict host health and fitness?For all of these questions, we highlight areas where primatologists are uniquely positioned to make substantial contributions. We review preliminary evidence, discuss possible study designs, and suggest future directions. Research Highlights• To date nearly all insights into the processes shaping vertebrate gut microbiomes have emerged from studies that have cross-sectional designs, but emerging time series analyses show that gut microbiomes can change rapidly from 1 day to the next.• Field-based primate studies, owing to their focus on the lives of individual animals, and the relative ease of collecting longitudinal fecal samples from known animals, are better positioned to collect these data than studies of humans or other species.• We propose five questions of general interest to microbiome science where fieldbased primate studies are especially well positioned to fill major gaps. We review preliminary evidence, discuss possible study designs, and suggest future directions.Am J Primatol. 2019;81:e22970.wileyonlinelibrary.com/journal/ajp

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Early and Adult Social Environments Shape Sex-Specific Actuarial Senescence Patterns in a Cooperative Breeder

Cited by 39 publications

References 78 publications

Sex‐independent senescence in a cooperatively breeding mammal

Sex‐independent senescence in a cooperatively breeding mammal

Are trade‐offs really the key drivers of ageing and life span?

Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research

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