High social status males experience accelerated epigenetic aging in wild baboons

  1. Jordan A Anderson
  2. Rachel A Johnston
  3. Amanda J Lea
  4. Fernando A Campos
  5. Tawni N Voyles
  6. Mercy Y Akinyi
  7. Susan C Alberts
  8. Elizabeth A Archie
  9. Jenny Tung

  • Curated by eLife

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    Evaluation Summary:

    In this paper, the authors collect epigenomic data from a well-studied wild baboon community, which they use to construct an epigenetic clock, a method of measuring "biological age" that is increasingly used as a tool in human aging research. The authors find that deviations between biological and chronological age can in part be explained by social phenomena. In particular, for male baboons, maintaining social dominance may play an important role in accelerating the dimension of aging indexed by this measure. This is a foundational study for social-biological-health research.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

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Abstract

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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  1. Version published to 10.7554/elife.66128 on eLife
  2. eLife

    Evaluation Summary:

    In this paper, the authors collect epigenomic data from a well-studied wild baboon community, which they use to construct an epigenetic clock, a method of measuring "biological age" that is increasingly used as a tool in human aging research. The authors find that deviations between biological and chronological age can in part be explained by social phenomena. In particular, for male baboons, maintaining social dominance may play an important role in accelerating the dimension of aging indexed by this measure. This is a foundational study for social-biological-health research.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

  3. eLife

    Reviewer #1 (Public Review):

    This is an interesting manuscript which does a lot - both building and validating an epigenetic clock for the Amboseli baboons, and then looking to see which factors predict deviations in epigenetic age relative to chronological age. This is an important study, and perhaps the first of its kind from a free-ranging primate population. I believe it will be influential and well-cited.

    In particular, it is extremely thorough in the data and analyses that it presents. It is also clearly structured and easy to follow, despite covering some dense material.

    In sum, this manuscript is a high-quality and important manuscript that I believe will be influential.

  4. eLife

    Reviewer #2 (Public Review):

    Anderson et al construct an epigenetic clock using samples from 245 individuals in the long-running Amboseli study of wild baboons. Their epigenetic clock tracks chronological age reasonably well, and also relates to other metrics of developmental tempo. Contrary to expectations from studies in humans and other species, deviations between epigenetic age and chronological age are unrelated to important predictors of life expectancy in this sample, including measures of early adversity and social integration. Instead, the key predictor of epigenetic aging is dominance rank: In males, more dominant animals show evidence for accelerated epigenetic aging using the epigenetic clock that they derive. In a longitudinal analysis the relationship between dominance and biological aging is shown to be at least partially transient and reversible, pointing to possible concurrent rather than cumulative or non-reversible effects. Although reproductive effort in the form of larger body size and muscularity are plausible factors linking dominance to epigenetic aging, the relationships documented here are shown to be largely independent of measures of body size and relative weight.

    This study is important because the authors generate an epigenetic clock, a method increasingly important in research on human aging and life history, for use in this species of baboon. To achieve this, they use a long-running study in which the actual ages of animals are known. Their findings suggest that the aspect of biological aging indexed by this clock is distinct from other important influences on lifespan previously documented in this species, and specifically points to reproductive effort related to maintaining dominance as a key driver of this variation in males.

  5. Version published to 10.1101/2020.02.22.961052v2 on bioRxiv
  6. Version published to 10.1101/2020.02.22.961052v1 on bioRxiv