High social status males experience accelerated epigenetic aging in wild baboons

Jordan A Anderson,Rachel A Johnston,Fernando A Campos,Tawni N Voyles,Susan C Alberts,Amanda J Lea,Mercy Y Akinyi,Elizabeth A Archie,Jenny Tung

doi:10.7554/elife.66128

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.

Highlights

Aging, the nearly ubiquitous functional decline experienced by organisms over time[1], is a fundamental component of most animal life histories[2]
Clock sites were more likely to be found in regions that exhibit enhancer-like activity in a massively parallel reporter assay[26] and in regions implicated in the gene expression response to bacteria in the Amboseli baboon population
Our findings indicate that major environmental predictors of lifespan and mortality risk— social bond strength and early life adversity in this population—do not necessarily predict epigenetic measures of biological age

Summary

Introduction

The nearly ubiquitous functional decline experienced by organisms over time[1], is a fundamental component of most animal life histories[2]. Recent work suggests that DNA methylation data can provide exceptionally accurate estimates of chronological age[4]. Some versions of these clocks predict disease risk and mortality, suggesting that they capture aspects of biological aging that are not captured by chronological age alone[8]. Accelerated epigenetic age is in turn predicted by environmental factors with known links to health and lifespan, including childhood social adversity[12,13] and cumulative lifetime stress[14]. While DNA methylation data have been used to estimate the age structure of wild populations (where birthdates are frequently unknown)[18,19,20,21], they have not been applied to investigating sources of variance in biological aging in the wild

Methods

Results

Conclusion