1. Evolutionary Biology
  2. Genetics and Genomics
Download icon

Aging: The temporary cost of dominance

  1. Calen P Ryan
  2. Christopher W Kuzawa  Is a corresponding author
  1. Department of Anthropology, Northwestern University, United States
  2. Institute for Policy Research, Northwestern University, United States
Insight
  • Cited 0
  • Views 892
  • Annotations
Cite this article as: eLife 2021;10:e68790 doi: 10.7554/eLife.68790

Abstract

In a population of wild baboons, a new way to assess biological age reveals a surprising effect of social hierarchy.

Main text

Aging is inevitable, but also unfair: individuals can share the same number of years, yet their bodies may be getting older at different rates. Accurate ways of measuring this ‘biological aging’ would help to assess which individuals in a population are aging faster, and why.

Epigenetic clocks measure the regular unfolding of chemical marks on DNA, and can predict chronological age – that is, the amount of time since birth (Horvath and Raj, 2018; Ryan, 2020). In many species, including humans, the difference between epigenetic and chronological age serves as an index for how quickly the body of an animal is aging. In fact, people who look epigenetically older than their chronological age tend to have shorter lives (Marioni et al., 2015). Now, in eLife, Jenny Tung and colleagues – including Jordan Anderson and Rachel Johnston as joint first authors – report that in a population of wild baboons from Amboseli National Park in Kenya, social factors might speed up epigenetic aging in unexpected ways (Anderson et al., 2021).

The team (who are based in various institutions in the United States and Kenya) developed an epigenetic clock that rivaled or exceeded better-established methods to estimate the chronological age of a baboon. Yet, despite this accuracy, some animals were predicted to be older or younger than their years. The Amboseli group has been closely observed for 50 years, and previous studies have shown that monkeys in this population had reduced lifespans if they faced challenges early in life (Alberts and Altmann, 2012). Such experiences included being born to a low-status mother, competing with siblings, and growing up during a drought or at times of high population density (Archie et al., 2014; Tung et al., 2016). In addition, having fewer social bonds has also been linked to reduced lifespans in this group (Silk et al., 2010). However, Anderson et al. found that none of these factors were associated with epigenetic aging.

In contrast, male baboons with higher dominance ranks – who fiercely compete for their place in the hierarchy – looked epigenetically older than their chronological age. This link was not seen in females, who do not fight for their social status but instead inherit it from their mother. To further explore the association between a male’s place in the social hierarchy and his biological aging, the researchers tested whether males who increased or dropped in rank also experienced changes in their epigenetic age (Figure 1). As predicted, males’ epigenetic clocks tended to accelerate with an increase in rank. Intriguingly, however, losing social status also made males look epigenetically younger. These findings suggest that the competitive behaviors which help males achieve dominance and increase mating opportunities also come at the price of biological wear and tear, and a sped-up epigenetic clock. However, these costs seem to be temporary and reversible.

Change in social status alters the relationship between biological and chronological aging in wild baboons.

Chronological age (how many years an individual has been alive for) can differ from epigenetic (that is, biological) age. The dotted diagonal line shows the rate where both measures match; individuals above this line are biologically older than their actual age, and individuals below are biologically younger than their chronological age. Male baboons who are socially dominant (upright, walking figure) tended to be epigenetically ‘older’ than expected given their chronological age. This relationship was reversed for male individuals of lesser ranks (sitting figure). However, changes in social status between two time points (gray arrows) alter the speed of the epigenetic clock. Low status males (male B, in blue) which gained dominance tended to become epigenetically ‘older’ relative to chronological age. In contrast, when a dominant male (male A, in red) lost status, his epigenetic age tended to decline. These findings suggest that the epigenetic clock accelerates as baboons gain social dominance, but that these aspects of biological aging are transient. This could mean that this epigenetic measure might not be associated with mortality or lifespan, as it is found for other species.

This study is among the first to develop an epigenetic clock to explore the social determinants of epigenetic aging in a wild animal population, and confirm that this method tracks chronological age quite well. Yet the findings by Anderson et al. also raise new questions about the dimensions of biological change that epigenetic clocks may capture. For instance, it is still unclear why dominance rank predicts the acceleration of epigenetic age in male baboons, while other factors associated with lifespan in both sexes do not. More generally, the biological meaning of this sped-up clock remains to be explored in this population. If males can appear older or younger than their chronological age based on their current dominance rank, how do these transient effects impact their lifespan or functional decline – as similar measures have been shown to do in other species (Marioni et al., 2015; Stubbs et al., 2017)?

The transient effect of dominance on epigenetic age was a surprising finding that will likely require more work to unpack. The epigenetic clock that Anderson et al. developed was based upon analysis of genetic material from immune cells present in the blood, and may therefore reflect changes in the immune profile of an individual at the time they were sampled. In fact, switches in dominance rank in male baboons are accompanied by shifts in immune function (Lea et al., 2018); this might explain how the clocks could temporarily reflect a male’s current status. Future research in wild animals like the Amboseli baboons, especially in the social and natural environments in which they evolved, will help further dissect epigenetic clocks, and clarify what makes them tick.

References

  1. Book
    1. Alberts SC
    2. Altmann J
    (2012) The Amboseli Baboon Research Project: 40 Years of Continuity and Change
    In: Kappeler P. M, Watts D. P, editors. Long-Term Field Studies of Primates. Berlin: Springer. pp. 261–287.
    https://doi.org/10.1007/978-3-642-22514-7

Article and author information

Author details

  1. Calen P Ryan

    Calen P Ryan is in the Department of Anthropology, Northwestern University, Evanston, United States

    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0550-7949
  2. Christopher W Kuzawa

    Christopher W Kuzawa is in the Department of Anthropology and the Institute for Policy Research, Northwestern University, Evanston, United States

    For correspondence
    kuzawa@northwestern.edu
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0649-8677

Publication history

  1. Version of Record published: April 30, 2021 (version 1)

Copyright

© 2021, Ryan and Kuzawa

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

Metrics

  • 892
    Page views
  • 45
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Evolutionary Biology
    2. Genetics and Genomics
    Gabriela Santos-Rodriguez et al.
    Research Article Updated

    Many primate genes produce circular RNAs (circRNAs). However, the extent of circRNA conservation between closely related species remains unclear. By comparing tissue-specific transcriptomes across over 70 million years of primate evolution, we identify that within 3 million years circRNA expression profiles diverged such that they are more related to species identity than organ type. However, our analysis also revealed a subset of circRNAs with conserved neural expression across tens of millions of years of evolution. By comparing to species-specific circRNAs, we identified that the downstream intron of the conserved circRNAs display a dramatic lengthening during evolution due to the insertion of novel retrotransposons. Our work provides comparative analyses of the mechanisms promoting circRNAs to generate increased transcriptomic complexity in primates.

    1. Evolutionary Biology
    2. Genetics and Genomics
    Franziska Gruhl et al.
    Research Article Updated

    Circular RNAs (circRNAs) are found across eukaryotes and can function in post-transcriptional gene regulation. Their biogenesis through a circle-forming backsplicing reaction is facilitated by reverse-complementary repetitive sequences promoting pre-mRNA folding. Orthologous genes from which circRNAs arise, overall contain more strongly conserved splice sites and exons than other genes, yet it remains unclear to what extent this conservation reflects purifying selection acting on the circRNAs themselves. Our analyses of circRNA repertoires from five species representing three mammalian lineages (marsupials, eutherians: rodents, primates) reveal that surprisingly few circRNAs arise from orthologous exonic loci across all species. Even the circRNAs from orthologous loci are associated with young, recently active and species-specific transposable elements, rather than with common, ancient transposon integration events. These observations suggest that many circRNAs emerged convergently during evolution – as a byproduct of splicing in orthologs prone to transposon insertion. Overall, our findings argue against widespread functional circRNA conservation.