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  Is a corresponding author
  1. Duke University, United States
  2. Princeton University, United States
  3. University of Texas at San Antonio, United States
  4. National Museums of Kenya, Kenya
  5. University of Notre Dame, United States

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.

Data availability

All sequencing data generated during this study are available in the NCBI Sequence Read Archive (project accession PRJNA648767), and processed counts data are available in the Dryad digital repository (doi:10.5061/dryad.qjq2bvqf0).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Jordan A Anderson

    Department of Evolutionary Anthropology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  2. Rachel A Johnston

    Department of Evolutionary Anthropology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8965-1162
  3. Amanda J Lea

    Lewis-Sigler Institute for Integrative Genomics, Carl Icahn Laboratory, Princeton University, Princeton, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8827-2750
  4. Fernando A Campos

    Anthropology, University of Texas at San Antonio, San Antonio, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9826-751X
  5. Tawni N Voyles

    Department of Evolutionary Anthropology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  6. Mercy Y Akinyi

    Institute of Primate Research, National Museums of Kenya, Nairobi, Kenya
    Competing interests
    No competing interests declared.
  7. Susan C Alberts

    Department of Biology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1313-488X
  8. Elizabeth A Archie

    Department of Biological Sciences, University of Notre Dame, Notre Dame, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1187-0998
  9. Jenny Tung

    Evolutionary Anthropology, Biology, Duke University, Durham, NC, United States
    For correspondence
    jenny.tung@duke.edu
    Competing interests
    Jenny Tung, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0416-2958

Funding

National Science Foundation (IOS 1456832)

  • Susan C Alberts

Center for Population Health and Aging (P30AG034424)

  • Jenny Tung

Canadian Institute for Advanced Research

  • Jenny Tung

National Institutes of Health (R01AG053308)

  • Susan C Alberts

National Institutes of Health (R01AG053330)

  • Elizabeth A Archie

National Institutes of Health (R01HD088558)

  • Jenny Tung

National Institutes of Health (P01AG031719)

  • Susan C Alberts

National Institutes of Health (F32HD095616)

  • Rachel A Johnston

National Science Foundation (2018264636)

  • Jordan A Anderson

Foerster-Bernstein Foundation (Postdoctoral Fellowship)

  • Rachel A Johnston

North Carolina Biotechnology Center (2016-IDG-1013)

  • Jenny Tung

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Samples were obtained under approval from the Institutional Animal Care and Use Committee (IACUC) of Duke University (#A273-17-12) and adhered to all the laws and regulations of Kenya.

Reviewing Editor

  1. George H Perry, Pennsylvania State University, United States

Publication history

  1. Received: December 30, 2020
  2. Accepted: March 18, 2021
  3. Accepted Manuscript published: April 6, 2021 (version 1)
  4. Version of Record published: April 30, 2021 (version 2)

Copyright

© 2021, Anderson et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  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
(2021)
High social status males experience accelerated epigenetic aging in wild baboons
eLife 10:e66128.
https://doi.org/10.7554/eLife.66128
  1. Further reading

Further reading

    1. Evolutionary Biology
    2. Epidemiology and Global Health
    3. Microbiology and Infectious Disease
    4. Genetics and Genomics
    Edited by George H Perry et al.
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  1. Competing for high social status speeds up aging in male baboons