High social status males experience accelerated epigenetic aging in wild baboons.

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.

For most animals, age is one of the strongest predictors of health and survival, but not all individuals age at the same rate. In fact, animals of the same species can have different 'biological ages' even when they have lived the same number of years. In humans and other mammals this variation in aging shows up in chemical modifications known as DNA methylation marks. Some researchers call these marks 'epigenetic', which literally means 'upon the genes'. And some DNA methylation marks change with age, so their combined pattern of change is often called the 'epigenetic clock'. Environmental stressors, such as smoking or lack of physical activity, can make the epigenetic clock 'tick' faster, making the DNA of some individuals appear older than expected based on their actual age in years. These 'biologically older' individuals may also experience a higher risk of age-related disease. Studies in humans have revealed some of the reasons behind this fast biological aging, but it is unclear whether these results apply in the wild. It is possible that early life events trigger changes in the epigenetic clock, affecting health in adulthood. In primates, for example, adversity in early life has known effects on fertility and survival. Low social status also has a negative effect on health. To find out whether early experiences and the social environment affect the epigenetic clock, Anderson, Johnston et al. tracked DNA methylation marks in baboons. This revealed that epigenetic clocks are strong predictors of age in wild primates, but neither early adversity nor the strength of social bonds affected the rate at which the clocks ticked. In fact, it was competition for social status that had the most dramatic effect on the clock's speed. Samples of males taken at different times during their lives showed that their epigenetic clocks sped up or slowed down as they moved up or down the social ladder, reflecting recent social experiences, rather than events early in their lives. On average, epigenetic clock measurements overestimated the age in years of alpha males by almost a year, showing that fighting to be on top comes at a cost. This study highlights one way in which the social environment can influence aging. The next step is to understand how health is affected by the ways that animals attain social status. This could help researchers who study evolution understand how social interactions and environmental conditions affect survival and reproduction. It could also provide insight into the effects of social status on human health and aging.

Social bonds, social status and survival in wild baboons: a tale of two sexes.

People who are more socially integrated or have higher socio-economic status live longer. Recent studies in non-human primates show striking convergences with this human pattern: female primates with more social partners, stronger social bonds or higher dominance rank all lead longer lives. However, it remains unclear whether social environments also predict survival in male non-human primates, as it does in men. This gap persists because, in most primates, males disperse among social groups, resulting in many males who disappear with unknown fate and have unknown dates of birth. We present a Bayesian model to estimate the effects of time-varying social covariates on age-specific adult mortality in both sexes of wild baboons. We compare how the survival trajectories of both sexes are linked to social bonds and social status over the life. We find that, parallel to females, male baboons who are more strongly bonded to females have longer lifespans. However, males with higher dominance rank for their age appear to have shorter lifespans. This finding brings new understanding to the adaptive significance of heterosexual social bonds for male baboons: in addition to protecting the male's offspring from infanticide, these bonds may have direct benefits to males themselves. This article is part of the theme issue 'Evolution of the primate ageing process'.

Life at the top: rank and stress in wild male baboons.

In social hierarchies, dominant individuals experience reproductive and health benefits, but the costs of social dominance remain a topic of debate. Prevailing hypotheses predict that higher-ranking males experience higher testosterone and glucocorticoid (stress hormone) levels than lower-ranking males when hierarchies are unstable but not otherwise. In this long-term study of rank-related stress in a natural population of savannah baboons (Papio cynocephalus), high-ranking males had higher testosterone and lower glucocorticoid levels than other males, regardless of hierarchy stability. The singular exception was for the highest-ranking (alpha) males, who exhibited both high testosterone and high glucocorticoid levels. In particular, alpha males exhibited much higher stress hormone levels than second-ranking (beta) males, suggesting that being at the very top may be more costly than previously thought.

Floating limb behaviors and self-biting are associated in laboratory monkeys.

Early descriptions of floating limb behaviors in monkeys were associated with isolation rearing, a practice that ended more than two decades ago. The present authors named various forms of behaviors in which a leg is elevated for no apparent reason: "Floating Limb Suite" (FLS). Floating limb behaviors, identified in laboratory monkeys at the Washington National Primate Research Center (WaNPRC), consist of two subcategories distinguished by whether monkeys seem to react to the elevated leg or ignore it. Given the past association of isolation rearing with both self-biting (SB) and floating limb, the investigators predicted that SB and FLS would be associated in monkeys not reared in isolation. The investigators tracked, over a period of 3 years, the presence of FLS and SB in macaques (Macaca nemestrina, M. fascicularis, M. mulatta) and Papio cynocephalus at WaNPRC. SB and both subcategories of FLS occurred in mother-reared and surrogate-peer-nursery-reared monkeys. We analyzed presence of FLS, the two subcategories of FLS, and SB in 1,117 macaques monitored for up to 3 years, and 781 macaques observed for 8 min of structured data collection. The Papio sample size was insufficient for statistical analysis. Both sampling methodologies found FLS and FLS subcategories to be associated with SB. Nearly half the monkeys only engaging in seemingly harmless nonreactive forms of FLS also performed the potentially injurious behavior of self-biting. The positive association between FLS and SB suggests that monkeys exhibiting one of these behaviors are at a heightened risk for developing the other. One impediment to studying floating limb behaviors is lack of consensus on definitions. This study defined seven forms of apparently functionless elevated limb behaviors. Continued research on factors associated with floating limb behaviors across demographic groups and settings may provide insights into the etiology and treatment of self-biting.