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, 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’.

Reduced injury risk links sociality to survival in a group-living primate

“…We found no support for the second hypothesized mechanism that we explored to link sociality to survival; none of the measures of sociality analyzed influenced an individual's survival trajectory following injury. Despite a vast body of literature supporting differences in health and immunity between individuals of different social status [44,35,39], we found no evidence for an effect of social status on the survival trajectories of injured animals. These findings contrast with a previous study on wild baboons where high status males had faster healing rates than lower status males [37].…”

“…Growing literature has supported a strong relationship between the social environment and survival in many mammal species [3], but the ultimate function of some components of sociality, such as social relationships, remain unclear [77]. Although sociality has been demonstrated to enhance health and immunity [44,35,45], here we showed that these benefits did not translate to an improved ability to cope with the risk of death from injuries. Instead, we found that sociality plays an important role in preventing individuals from suffering injuries that would likely lead to death.…”

The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies

“…A few cross-cutting themes emerge from the contributions to this theme issue as vibrant areas of ongoing or future progress, supporting the suggestion by Hobson [5] that we may be entering a more cross-disciplinary phase in the study of dominance hierarchies. Many contributions highlight the rapid development of advanced quantitative tools for social network analysis as playing an important role in driving new insight into the structure and function of dominance hierarchies (Tibbetts et al [67] and Dehnen et al [75]), comparative approaches (Strauss et al [22]), theoretical frameworks (Lewis [69], Zeng et al [24] and Strauss & Shizuka [78]) and modelling (Hamilton & Benincasa [76]), the theme issue highlights how research into dominance hierarchies uses the full breadth of tools available to modern biologists.…”

“…[ 74 ]), long-term individual-based observational studies (Anderson et al . [ 67 ] and Dehnen et al . [ 75 ]), comparative approaches (Strauss et al .…”

“…Finally, ongoing work on the influence of social gradients on health continues to shed new light on the specific mechanisms linking dominance status to individual outcomes ([ 7 , 11 ]; see also Anderson et al . [ 67 ] and Simons et al . [ 68 ] in this theme issue).…”