Decoupling social status and status certainty effects on health in macaques: a network approach

Abstract

BackgroundAlthough a wealth of literature points to the importance of social factors on health, a detailed understanding of the complex interplay between social and biological systems is lacking. Social status is one aspect of social life that is made up of multiple structural (humans: income, education; animals: mating system, dominance rank) and relational components (perceived social status, dominance interactions). In a nonhuman primate model we use novel network techniques to decouple two components of social status, dominance rank (a commonly used measure of social status in animal models) and dominance certainty (the relative certainty vs. ambiguity of an individual’s status), allowing for a more complex examination of how social status impacts health.MethodsBehavioral observations were conducted on three outdoor captive groups of rhesus macaques (N = 252 subjects). Subjects’ general physical health (diarrhea) was assessed twice weekly, and blood was drawn once to assess biomarkers of inflammation (interleukin-6 (IL-6), tumor necrosis factor-alpha (TNF-α), and C-reactive protein (CRP)).ResultsDominance rank alone did not fully account for the complex way that social status exerted its effect on health. Instead, dominance certainty modified the impact of rank on biomarkers of inflammation. Specifically, high-ranked animals with more ambiguous status relationships had higher levels of inflammation than low-ranked animals, whereas little effect of rank was seen for animals with more certain status relationships. The impact of status on physical health was more straightforward: individuals with more ambiguous status relationships had more frequent diarrhea; there was marginal evidence that high-ranked animals had less frequent diarrhea.DiscussionSocial status has a complex and multi-faceted impact on individual health. Our work suggests an important role of uncertainty in one’s social status in status-health research. This work also suggests that in order to fully explore the mechanisms for how social life influences health, more complex metrics of social systems and their dynamics are needed.

Interindividual differences in neonatal sociality and emotionality predict juvenile social status in rhesus monkeys

“…This difference is meaningful because this indicates that social status within primate groups is dependent on group membership, which may change and consequently change social status (i.e., Snyder-Mackler et al, 2016;Tung et al, 2012), whereas SES in humans is theoretically independent of group membership and potentially stable. However, given that the group memberships remained stable throughout the study period and that the broad definition of SES in humans refers to the relative access to power with which they can obtain resources (McLoyd, 1998), we and others (e.g., Jarrell et al, 2008;Massart et al, 2017;Snyder-Mackler et al, 2018;Vandeleest et al, 2016) argue that the social construct of status in nonhuman primates is still a good translational model for humans.…”

Juvenile rank acquisition influences fitness independent of adult rank

“…Considerable evidence suggests that adverse conditions in early in life can have profound and long-lasting consequences [26]. Social defeat and social uncertainty in dominance relationships have been shown to incur costs [24,25,41]. Here, juveniles that were defeated by peers that they would eventually come to dominate showed reduced survival and impaired reproductive success, suggesting that social uncertainty coupled with social defeat could be a source of early life adversity in spotted hyenas.…”

“…There are multiple reasons why the process of rank acquisition might relate to fitness, independent of the ranks juveniles ultimately acquire. First, social uncertainty is costly [24,25], and a tumultuous process of rank acquisition could be a source of significant social uncertainty, and thus adversity, in early life. Early-life adversity is associated with downstream consequences in many species [26–28], so costs of social uncertainty in early life could potentially have far reaching fitness consequences.…”

Social bufferingandcontact transmission: network connections have beneficial and detrimental effects onShigellainfection risk among captive rhesus macaques

“…Biologically, it may be a more important moderator (than rank) on health outcomes. For instance, a recent study on the CNPRC rhesus macaques showed that individuals that face greater unpredictability in their dominance encounters also showed pronounced biomarkers of poor health, including inflammatory proteins and diarrhea (Vandeleest et al, 2016). Under such circumstances, the beneficial impact of possessing strong social connections in buffering individuals against infection risk may be more clearly discernible.…”

“…Specifically, we asked whether Shigella infection was least likely among high-ranking females who typically form the strongest social bonds. Further, given that increased uncertainty in dominance relationships could be more stressful (Vandeleest et al, 2016), we asked whether the effect of possessing increased connections on socially buffering individuals from infection risk was more clearly discernible among individuals who also had more uncertain compared to certain dominance relationships.…”