Social Status and Gene Regulation: Conservation and Context Dependence in Primates

Simons, Noah D.; Tung, Jenny

doi:10.1016/j.tics.2019.06.003

Cited by 15 publications

(11 citation statements)

References 12 publications

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“…Together, these results argue that social status/dominance rank effects should not be interpreted as a universal phenomenon. Instead, the manner through which social status is achieved and maintained is likely to be key to understanding its consequences for physiology, health, and fitness 71 . Specifically, we predict that high status will be most likely to accelerate the aging process, including epigenetic age, in species-sex combinations where high status increases reproductive success or fecundity, and achieving status is energetically costly (e.g., male red deer, mandrills, and geladas; female meerkats [72][73][74] ).…”

Section: Discussionmentioning

confidence: 99%

High social status males experience accelerated epigenetic aging in wild baboons

Anderson

Johnston

Lea

et al. 2021

eLife

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Aging, for virtually all life, is inescapable. However, within populations, biological aging rates vary. Understanding sources of variation in this process is central to understanding the biodemography of natural populations. We constructed a DNA methylation-based age predictor for an intensively studied wild baboon population in Kenya. Consistent with findings in humans, the resulting 'epigenetic clock' closely tracks chronological age, but individuals are predicted to be somewhat older or younger than their known ages. Surprisingly, these deviations are not explained by the strongest predictors of lifespan in this population, early adversity and social integration. Instead, they are best predicted by male dominance rank: high-ranking males are predicted to be older than their true ages, and epigenetic age tracks changes in rank over time. Our results argue that achieving high rank for male baboons—the best predictor of reproductive success—imposes costs consistent with a 'live fast, die young' life history strategy.

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Section: Discussionmentioning

confidence: 99%

High social status males experience accelerated epigenetic aging in wild baboons

Anderson

Johnston

Lea

et al. 2021

eLife

Self Cite

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“…These and other components of social adversity are thought to accelerate ageing through altered hypothalamic–pituitary–adrenal (HPA) axis function, particularly gradual desensitization of the glucocorticoid receptor response, leading to chronic activation of downstream pro-inflammatory cascades [68]. Indeed, various forms of social adversity are associated with elevated expression of pro-inflammatory genes and decreased expression of genes related to innate immune responses in humans [69] and rhesus macaques [70]. Low macaque dominance rank, for instance, has been causally linked to altered glucocorticoid and immune regulation and polarization of some immune pathways towards a pro-inflammatory response [71–74].…”

Section: Outlook and Challengesmentioning

confidence: 99%

Rhesus macaques as a tractable physiological model of human ageing

Chiou

Montague

Goldman

et al. 2020

Phil. Trans. R. Soc. B

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Research in the basic biology of ageing is increasingly identifying mechanisms and modifiers of ageing in short-lived organisms such as worms and mice. The ultimate goal of such work is to improve human health, particularly in the growing segment of the population surviving into old age. Thus far, few interventions have robustly transcended species boundaries in the laboratory, suggesting that changes in approach are needed to avoid costly failures in translational human research. In this review, we discuss both well-established and alternative model organisms for ageing research and outline how research in nonhuman primates is sorely needed, first, to translate findings from short-lived organisms to humans, and second, to understand key aspects of ageing that are unique to primate biology. We focus on rhesus macaques as a particularly promising model organism for ageing research owing to their social and physiological similarity to humans as well as the existence of key resources that have been developed for this species. As a case study, we compare gene regulatory signatures of ageing in the peripheral immune system between humans and rhesus macaques from a free-ranging study population in Cayo Santiago. We show that both mRNA expression and DNA methylation signatures of immune ageing are broadly shared between macaques and humans, indicating strong conservation of the trajectory of ageing in the immune system. We conclude with a review of key issues in the biology of ageing for which macaques and other nonhuman primates may uniquely contribute valuable insights, including the effects of social gradients on health and ageing. We anticipate that continuing research in rhesus macaques and other nonhuman primates will play a critical role in conjunction with the model organism and human biodemographic research in ultimately improving translational outcomes and extending health and longevity in our ageing population. This article is part of the theme issue ‘Evolution of the primate ageing process’.

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“…These and other components of social adversity are thought to accelerate ageing through altered hypothalamic-pituitary-adrenal (HPA) axis function, particularly a gradual desensitisation of the glucocorticoid receptor response, leading to chronic activation of downstream proinflammatory cascades [68]. Indeed, various forms of social adversity are associated with elevated expression of proinflammatory genes and decreased expression of genes related to innate immune responses in humans [69] and rhesus macaques [70]. Low macaque dominance rank, for instance, has been causally linked to altered glucocorticoid and immune regulation and a polarisation of some immune pathways towards a proinflammatory response [71][72][73][74].…”

Section: Ageing Across the Bodymentioning

confidence: 99%

Rhesus macaques as a tractable physiological model of human ageing

Chiou

Montague

Goldman

et al. 2020

Preprint

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Research in the basic biology of ageing is increasingly identifying mechanisms and modifiers of ageing in short-lived organisms such as worms and mice. The ultimate goal of such work is to improve human health, particularly in the growing segment of the population surviving into old age. Thus far, few interventions have robustly transcended species boundaries in the laboratory, suggesting that changes in approach are needed to avoid costly failures in translational human research. In this review, we discuss both well-established and alternative model organisms for ageing research and outline how research in nonhuman primates is sorely needed, first, to translate findings from shorter-lived organisms to humans, and second, to understand key aspects of ageing that are unique to primate biology. We focus on rhesus macaques as a particularly promising model organism for ageing research due to their social and physiological similarity to humans as well as the existence of key resources that have been developed for this species. As a case study, we compare gene regulatory signatures of ageing in the peripheral immune system between humans and rhesus macaques from a free-ranging study population in Cayo Santiago. We show that both mRNA expression and DNA methylation signatures of immune ageing are broadly shared between macaques and humans, indicating strong conservation of the trajectory of ageing in the immune system. We conclude with a review of key issues in the biology of ageing for which macaques and other nonhuman primates may uniquely contribute valuable insights, including the effects of social gradients on health and ageing. We anticipate that continuing research in rhesus macaques and other nonhuman primates will play a critical role in conjunction with model organism and human biodemographic research in ultimately improving translational outcomes and extending health and longevity in our ageing population.

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Social Status and Gene Regulation: Conservation and Context Dependence in Primates

Cited by 15 publications

References 12 publications

High social status males experience accelerated epigenetic aging in wild baboons

High social status males experience accelerated epigenetic aging in wild baboons

Rhesus macaques as a tractable physiological model of human ageing

Rhesus macaques as a tractable physiological model of human ageing

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