Alberts, S. | Search bioRxiv

bioRxiv2025

Lifetime fitness and annual survival are heritable and highly genetically correlated in a wild primate population

The additive genetic variance (VA) of fitness quantifies the expected response to selection; lifetime breeding success (LBS) is an effective metric of fitness in animal populations. However, data on LBS are relatively rare for wild populations of long-lived species, while time-limited metrics such as annual survival or fertility are more readily available. The magnitude of VA for these time-limited metrics, and the degree to which they are genetically correlated with LBS, remains unclear in most cases. Here we estimated the VA and heritability (h2) of LBS and four time-limited fitness metrics in wild female baboons in Kenya. The most highly heritable metrics were LBS (h2=0.25) and annual survival (h2=0.23). Notably, all the VA for LBS was attributable to survival to first successful reproduction. Furthermore, all fitness metrics examined were highly genetically correlated with each other, supporting the potential use of time-limited metrics where LBS data are limited. Our analyses predicted faster phenotypic evolution than we observed, raising the possibility that environmental effects have masked responses to selection ("cryptic evolution") or that social effects inflate estimated VA. Together, our findings reveal a substantial genetic contribution to variation in survival, and in turn, to fitness and contemporary evolution in a long-lived animal.

evolutionary biology↗

bioRxiv2020

The costs of competition: high social status males experience accelerated epigenetic aging in wild baboons

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.

genomics↗

bioRxiv2018

Dominance rank-associated immune gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons

In humans and other hierarchical species, social status is tightly linked to variation in health and fitness-related traits. Experimental manipulations of social status in female rhesus macaques suggest that this relationship is partially explained by status effects on immune gene regulation. However, social hierarchies are established and maintained in different ways across species: while some are based on kin-directed nepotism, others emerge from direct physical competition. We investigated how this variation influences the relationship between social status and immune gene regulation in wild baboons, where hierarchies in males are based on fighting ability but female hierarchies are nepotistic. We measured rank-related variation in gene expression levels in adult baboons of both sexes at baseline and in response to ex vivo stimulation with the bacterial endotoxin lipopolysaccharide (LPS). We identified >2000 rank- associated genes in males, an order of magnitude more than in females. In males, high status predicted increased expression of genes involved in innate immunity and preferential activation of the NFkB-mediated pro-inflammatory pathway, a pattern previously associated with low status in female rhesus macaques. Using Mendelian randomization, we reconcile these observations by demonstrating that high status-associated gene expression patterns are precursors, not consequences, of high social status in males, in support of the idea that physiological condition determines who attains high rank. Together, our work provides the first test of the relationship between social status and immune gene regulation in wild primates. It also emphasizes the importance of social context in shaping the relationship between social status and immune function.\n\nSIGNIFICANCESocial status predicts fitness outcomes in social animals, motivating efforts to understand its physiological causes and consequences. We investigated the relationship between social status and immune gene expression in wild baboons, where female status is determined by kinship but male status is determined by fighting ability. We uncover pervasive status-gene expression associations in males, but not females. High status males exhibit high levels of pro-inflammatory gene expression, in contrast to previous findings in hierarchies that are not competitively determined. Using Mendelian randomization, we show that this status-associated variation precedes dominance rank attainment: males who compete successfully for high status are already immunologically distinct. The nature of social hierarchies thus fundamentally shapes the relationship between social status and immune function.

evolutionary biology↗