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

The social environment is a major determinant of morbidity, mortality and Darwinian fitness in social animals. Recent studies have begun to uncover the molecular processes associated with these relationships, but the degree to which they vary across different dimensions of the social environment remains unclear. Here, we draw on a long-term field study of wild baboons to compare the signatures of affiliative and competitive aspects of the social environment in white blood cell gene regulation, under both immune-stimulated and non-stimulated conditions. We find that the effects of dominance rank on gene expression are directionally opposite in males versus females, such that high-ranking males resemble low-ranking females, and vice versa. Among females, rank and social bond strength are both reflected in the activity of cellular metabolism and proliferation genes. However, while we observe pronounced rank-related differences in baseline immune gene activity, only bond strength predicts the fold-change response to immune (lipopolysaccharide) stimulation. Together, our results indicate that the directionality and magnitude of social effects on gene regulation depend on the aspect of the social environment under study. This heterogeneity may help explain why social environmental effects on health and longevity can also vary between measures. This article is part of the theme issue ‘The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies’.

Better baboon break-ups: collective decision theory of complex social network fissions

Many social groups are made up of complex social networks in which each individual associates with a distinct subset of its groupmates. If social groups become larger over time, competition often leads to a permanent group fission. During such fissions, complex social networks present a collective decision problem and a multidimensional optimization problem: it is advantageous for each individual to remain with their closest allies after a fission, but impossible for every individual to do so. Here, we develop computational algorithms designed to simulate group fissions in a network-theoretic framework. We focus on three fission algorithms (democracy, community and despotism) that fall on a spectrum from a democratic to a dictatorial collective decision. We parameterize our social networks with data from wild baboons ( Papio cynocephalus ) and compare our simulated fissions with actual baboon fission events. We find that the democracy and community algorithms (egalitarian decisions where each individual influences the outcome) better maintain social networks during simulated fissions than despotic decisions (driven primarily by a single individual). We also find that egalitarian decisions are better at predicting the observed individual-level outcomes of observed fissions, although the observed fissions often disturbed their social networks more than the simulated egalitarian fissions.

Synchrony and idiosyncrasy in the gut microbiome of wild primates

Human gut microbial dynamics are highly individualized, making it challenging to link microbiota to health and to design universal microbiome therapies. This individuality is typically attributed to variation in diets, environments, and medications, but it could also emerge from fundamental ecological forces that shape primate microbiota more generally. Here we leverage extensive gut microbiome time series from wild baboons-hosts who experience little interindividual dietary and environmental heterogeneity-to test whether gut microbial dynamics are synchronized across hosts or largely idiosyncratic. Despite their shared lifestyles, we find strong evidence for idiosyncrasy. Over time, samples from the same baboon were much more similar than samples from different baboons, and host-specific factors collectively explained 30% of the deviance in microbiome dynamics, compared to just 3% for factors shared across hosts. Hence, individualization may be common to mammalian gut microbiota, and designing universal microbiome interventions may face challenges beyond heterogeneity in human lifestyles.

Gut microbiome heritability is nearly universal but environmentally contingent

Relatives have more similar gut microbiomes than nonrelatives, but the degree to which this similarity results from shared genotypes versus shared environments has been controversial. Here, we leveraged 16,234 gut microbiome profiles, collected over 14 years from 585 wild baboons, to reveal that host genetic effects on the gut microbiome are nearly universal. Controlling for diet, age, and socioecological variation, 97% of microbiome phenotypes were significantly heritable, including several reported as heritable in humans. Heritability was typically low (mean = 0.068) but was systematically greater in the dry season, with low diet diversity, and in older hosts. We show that longitudinal profiles and large sample sizes are crucial to quantifying microbiome heritability, and indicate scope for selection on microbiome characteristics as a host phenotype.

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

The social environment is a major determinant of morbidity, mortality, and Darwinian fitness in social animals. Recent studies have begun to uncover the molecular processes associated with these relationships, but the degree to which they vary across different dimensions of the social environment remains unclear. Here, we draw on a long-term field study of wild baboons to compare the signatures of affiliative and competitive aspects of the social environment in white blood cell gene regulation, under both immune stimulated and non-stimulated conditions. We find that the effects of dominance rank on gene expression are directionally opposite in males versus females, such that high-ranking males resemble low-ranking females, and vice-versa. Among females, rank and social bond strength are both reflected in the activity of cellular metabolism and proliferation genes. However, pronounced rank-related differences in baseline immune gene activity are near-absent for social bond strength, while only bond strength predicts the fold-change response to immune (lipopolysaccharide) stimulation. Together, our results indicate that the directionality and magnitude of social effects on gene regulation depend on the aspect of the social environment under study. This heterogeneity may help explain why social environmental effects on health and longevity can also vary between measures.

The temporary cost of dominance

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

Social bonds, social status and survival in wild baboons: a tale of two sexes

People who are more socially integrated or have higher socio-economic status live longer. Recent studies in non-human primates show striking convergences with this human pattern: female primates with more social partners, stronger social bonds or higher dominance rank all lead longer lives. However, it remains unclear whether social environments also predict survival in male non-human primates, as it does in men. This gap persists because, in most primates, males disperse among social groups, resulting in many males who disappear with unknown fate and have unknown dates of birth. We present a Bayesian model to estimate the effects of time-varying social covariates on age-specific adult mortality in both sexes of wild baboons. We compare how the survival trajectories of both sexes are linked to social bonds and social status over the life. We find that, parallel to females, male baboons who are more strongly bonded to females have longer lifespans. However, males with higher dominance rank for their age appear to have shorter lifespans. This finding brings new understanding to the adaptive significance of heterosexual social bonds for male baboons: in addition to protecting the male's offspring from infanticide, these bonds may have direct benefits to males themselves. This article is part of the theme issue ‘Evolution of the primate ageing process'.