The Costs of Competition: High Social Status Males Experience Accelerated Epigenetic Aging in Wild Baboons

Abstract

Aging, for virtually all life, is inescapable. However, within species and populations, rates of biological aging (i.e., physical decline with age) vary across individuals. Understanding sources of variation in biological aging is therefore central to understanding the biodemography of natural populations. Here, we constructed a DNA methylation-based predictor of chronological age for a population of wild baboons in which behavioral, ecological, and life history data have been collected for almost 50 years (N = 277 blood samples from 245 individuals, including 30 who were longitudinally sampled). Consistent with findings in humans and model organisms, DNA methylation patterns exhibit a strong, clock-like association with chronological age, but individuals are often predicted to be somewhat older or younger than their known age. However, the two most robust predictors of lifespan described for this population—cumulative early adversity and social bond strength—do not explain this deviation. Instead, the single most predictive factor is male dominance rank: high-ranking males are predicted to be biologically older than their true chronological age, such that alpha males appear to be nearly a year older than their known age. Longitudinal sampling indicates that males who climb the social hierarchy subsequently look epigenetically “older,” likely reflecting the high energetic costs of rank attainment and maintenance in male baboons. Together, our results indicate that environmental effects on survival and epigenetic age can be disjunct, and that achieving high rank for male baboons—the best predictor of reproductive success—imposes physiological costs consistent with a “live fast, die young” life history strategy.