Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons

Lea, Amanda J.; Akinyi, Mercy; Nyakundi, Ruth; Mareri, Peter; Nyundo, Fred; Kariuki, Thomas; Alberts, Susan C.; Archie, Elizabeth A.; Tung, Jenny

doi:10.1073/pnas.1811967115

Cited by 59 publications

(124 citation statements)

References 60 publications

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“…In support of this interpretation, a model that includes rank-for-age as an additional covariate recapitulates the significant effect of ordinal male rank (p=0.045), but finds no effect of rank-for-age (p=0.819; Table S4). In contrast, we observed no evidence for rank effects on Δ age in females, consistent with overall sex differences in patterns of aging in primates and other mammals [15] and marked sex differences in the effects of rank on other molecular phenotypes in the Amboseli baboons specifically [11, 28].…”

Section: Resultssupporting

confidence: 77%

“…Elevated or chronic inflammation is thought to be one of the hallmarks of aging, and, in human populations, is one of the strongest predictors of mortality risk [29–31]. Consistent with these observations, CpG sites in the epigenetic clock that increase in DNA methylation with age (N = 459 sites) are enriched in or near genes that are up-regulated in the Amboseli baboons in response to the bacterial endotoxin lipopolysaccharide (LPS), which is a strong driver of inflammation (Figure S3; Fisher’s exact test: log 2 (odds ratio) = 1.88, p = 0.001; gene expression data from [28]). In contrast, clock sites that decrease in DNA methylation with age (N = 134) are significantly enriched in or near genes that are down-regulated after LPS exposure (Fisher’s exact test: log 2 (OR) = 3.28, p = 0.002).…”

Section: Resultsmentioning

confidence: 86%

“…Previous work has shown that high-ranking male baboons, but not high-ranking female baboons, up-regulate gene expression in inflammation-related and immune response pathways [28]. Elevated or chronic inflammation is thought to be one of the hallmarks of aging, and, in human populations, is one of the strongest predictors of mortality risk [29–31].…”

Section: Resultsmentioning

confidence: 99%

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The costs of competition: high social status males experience accelerated epigenetic aging in wild baboons

Anderson

Johnston

Lea

et al. 2020

Preprint

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25Aging, for virtually all life, is inescapable. However, within species and populations, 26 rates of biological aging (i.e., physical decline with age) vary across individuals. 27Understanding sources of variation in biological aging is therefore central to understanding 28 the biodemography of natural populations. Here, we constructed a DNA methylation-based 29 predictor of chronological age for a population of wild baboons in which behavioral, 30 ecological, and life history data have been collected for almost 50 years (N = 277 blood 31 samples from 245 individuals, including 30 who were longitudinally sampled). Consistent 32 with findings in humans and model organisms [1][2][3][4], DNA methylation patterns exhibit a 33 strong, clock-like association with chronological age, but individuals are often predicted to 34 be somewhat older or younger than their known age. However, the two most robust 35 predictors of lifespan described for this population-cumulative early adversity and social 36bond strength-do not explain this deviation. Instead, the single most predictive factor is 37 male dominance rank: high-ranking males are predicted to be biologically older than their 38 true chronological age, such that alpha males appear to be nearly a year older than their 39 known age. Longitudinal sampling indicates that males who climb the social hierarchy 40 subsequently look epigenetically "older," likely reflecting the high energetic costs of rank 41 attainment and maintenance in male baboons. Together, our results indicate that 42 environmental effects on survival and epigenetic age can be disjunct, and that achieving 43high rank for male baboons-the best predictor of reproductive success-imposes 44 physiological costs consistent with a "live fast, die young" life history strategy. 45 46

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Section: Resultssupporting

confidence: 77%

Section: Resultsmentioning

confidence: 86%

Section: Resultsmentioning

confidence: 99%

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The costs of competition: high social status males experience accelerated epigenetic aging in wild baboons

Anderson

Johnston

Lea

et al. 2020

Preprint

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“…Convergent evidence from humans, wild animal populations, and experimental animal models indicates that social interactions are reflected in the regulation and activity of the immune system (6,7,11,(26)(27)(28)48). Our findings join those of others to suggest that social adversity is particularly relevant to the inflammatory response, one of the first lines of defense in the innate immune system (49).…”

Section: Discussionsupporting

confidence: 73%

“…This relationship is thought to arise in part through changes in gene regulation, which mediate the genomic response to physiological signals of social stress (e.g., glucocorticoids, adrenaline, noradrenaline; (6,7)). Gene expression signatures of social status and social adversity have now been reported in multiple studies, encompassing clinical and population-based samples in humans, and studies of both experimental and natural populations in other social animals (6,(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)) (see also (20)(21)(22)(23)(24)(25) for evidence in social insects and other social vertebrates). Because this work has concentrated most extensively on peripheral white blood cells, it provides a direct window into how social experiences are reflected in the regulation of the immune system (26)(27)(28).…”

Section: Introductionmentioning

confidence: 99%

Social history and exposure to pathogen signals modulate social status effects on gene regulation in rhesus macaques

Sanz

Maurizio²,

Snyder‐Mackler

et al. 2019

Preprint

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Social experiences are an important predictor of disease susceptibility and survival in humans and other social mammals. Chronic social stress is thought to generate a proinflammatory state characterized by elevated antibacterial defenses and reduced investment in antiviral defense. Here, we manipulated long-term social status in female rhesus macaques to show that social subordination alters the gene expression response to ex vivo bacterial and viral challenge. As predicted by current models, bacterial lipopolysaccharide polarizes the immune response such that low status corresponds to higher expression of genes in NF-κBdependent pro-inflammatory pathways and lower expression of genes involved in the antiviral response and type I interferon (IFN) signaling. Counter to predictions, however, low status drives more exaggerated expression of both NF-κB and IFN-associated genes after cells are exposed to the viral mimic Gardiquimod. Status-driven gene expression patterns are not only linked to social status at the time of sampling, but also to social history (i.e., past social status), especially in unstimulated cells. However, for a subset of genes, we observed interaction effects in which females who fell in rank were more strongly affected by current social status than those who climbed the social hierarchy. Together, our results indicate that the effects of social status on immune cell gene expression depend on pathogen exposure, pathogen type, and social history -in support of social experience-mediated biological embedding in adulthood, even in the conventionally memory-less innate immune system.

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Sex differences in the impact of social status on hair cortisol concentrations in rhesus monkeys (Macaca mulatta)

Vandeleest

Winkler

Beisner

et al. 2019

American J Primatol

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Social status impacts stress in primates, but the direction of the effect differs depending on species, social style, and group stability. This complicates our ability to identify broadly applicable principles for understanding of how social status impacts health and fitness. One reason for this is the fact that social status is often measured as linear dominance rank, yet social status is more complex than simply high or low rank. Additionally, most research on social status and health ignores the effects of sex and sex-specific relationships, despite known differences in disease risk, coping strategies, and opposite-sex dominance interactions between males and females in many species. We examine the influence of social status, sex, and opposite-sex interactions on hair cortisol concentrations in a well-studied species, rhesus macaques, where the literature predicts low ranking individuals would experience more chronic stress. Animals in three captive, seminaturalistic social groups (N = 252, 71 male) were observed for 6 weeks to obtain metrics of social status (rank and dominance certainty (DC)). DC is a measure of one's fit within the hierarchy. Hair samples were collected from each subject and analyzed for hair cortisol concentrations (HCC). Generalized linear mixed models were used to examine 1) whether rank, DC, or sex predicted HCC, 2) whether same-or opposite-sex dominance relationships differentially impacted HCC, and 3) whether aggressive interactions initiated or received could explain any observed relationships. Results indicated that DC, not rank, predicted HCC in a sex-specific manner. For males, high HCC were predicted by receiving aggression from or having high DC with other males as well as having low DC with females. For females, only high DC with males predicted high HCC. These results likely relate to sex-specific life history pattern differences in inherited versus earned rank that are tied to female philopatry and male immigration.

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Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons

Cited by 59 publications

References 60 publications

The costs of competition: high social status males experience accelerated epigenetic aging in wild baboons

The costs of competition: high social status males experience accelerated epigenetic aging in wild baboons

Social history and exposure to pathogen signals modulate social status effects on gene regulation in rhesus macaques

Sex differences in the impact of social status on hair cortisol concentrations in rhesus monkeys (Macaca mulatta)

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