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

Abstract

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.

Selection against admixture and gene regulatory divergence in a long-term primate field study

“…To test for selection against gene regulatory divergence in baboons, we paired genetic ancestry data with blood-derived RNA-sequencing data from 145 unique individuals (n=157 samples [50][51][52] ; Table S1; Supplementary Methods). This data set includes whole blood collected from 2007 to 2010 and white blood cells collected from 2013 to 2018, which were processed and sequenced using distinct methods [50][51][52] . We therefore analyzed global and local ancestry effects on gene expression separately in these two data sets, controlling for age, sex, and kinship.…”

Socioeconomic status effects on health vary between rural and urban Turkana

“…For example, work in humans and captive female macaques has emphasized the association between low social status and increased expression of innate immune and inflammation-related genes [5,73,74]. However, in wild baboons, weak effects in the expected direction were observed in females [12], while strong patterns in the opposite direction were observed in males [66] (i.e., high social status predicted increased expression of inflammation-related genes). Importantly, social status is attained through direct physical competition in male baboons but not in any of the other species or sexes, suggesting that the heterogeneity between studies reflects differences in the nature of social hierarchies.…”

“…While there is overwhelming support for a consistent relationship between wealth-based measures of SES and human health, most evidence to date comes from studies of high-income countries (HICs) [8,9]. This limited scope undermines our ability to understand whether SEShealth relationships are consistent across contexts, or instead vary as a function of resource availability and distribution, the nature of social relationships and hierarchies, or other socioecological features of a population (as has been shown for other species [10][11][12]). In particular, it has been hypothesized that the steep social gradients in health observed in "Western" HICs are recent byproducts of environmental changes precipitated by urbanization, globalized markets, capitalism, and other modern advancements [13,14].…”

Neurogenomic landscape associated with status-dependent cooperative behavior

“…The differential global regulation of telomeres may explain the relative stability of telomere length in territorial wire-tailed manakin males (Vernasco et al, 2021), suggesting metabolic profiles associated with territoriality. Cooperation itself may also have metabolic costs, as more cooperative male manakins have been shown to have shorter telomeres (Vernasco et al, 2021), and social bond strength has been associated with signatures of energy metabolism and stress (Anderson et al, 2022;Simons et al, 2022).…”