High social status males experience accelerated epigenetic aging in wild baboons

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.

Distinct gene regulatory signatures of dominance rank and social bond strength in wild baboons

“…In contrast, little signature of rank was detectable in females [15]. This result is consistent with findings that high rank in males (but not females) predicts accelerated epigenetic aging, elevated glucocorticoid and testosterone levels, and, to a lesser extent, higher mortality rates [14, 45,80]. However, it contrasts with the hypothesis of a highly consistent gene regulatory response to the social environment [66].…”

“…To measure social bond strength, we used the dyadic sociality index (DSI, as in [45,80,101]). The DSI calculates the mean grooming-based bond strength between a focal female and her top three grooming partners in the year prior to sample collection, controlling for observer effort and dyad co-residency times (see details in the Supplementary Methods).…”

Pan-primate DNA methylation clocks

“…Another group has previously presented a blood clock for baboons based on DNA methylation profiles that were generated using a different methylation profiling platform (Reduced Representation Bisulfite Sequencing) [38]. We could not evaluate this blood clock in our data because the two genomic platforms profiled different sets of CpGs and furthermore, we did not profile blood samples in baboons.…”

Group structure, but not dominance rank, predicts fecal androgen metabolite concentrations of wild male mountain gorillas (Gorilla beringei beringei)

“…Having exclusive control over a group of females has obvious fitness benefits, but if sustained elevated androgen production is one of the costs males must pay to do so (e.g., in geladas, harem‐holding males have higher testosterone than bachelor males across the year: Pappano & Beehner, 2014), this may help explain why multimale groups are so common. A recent study from the Amboseli Baboon Research Project found that male baboons appear epigenetically “old” for their age when they are high ranking (Anderson et al, 2021). It seems plausible that androgens may be one mechanism via which these biological changes occur.…”