Melissa A. Pavez-Fox

Social relationships and environmental disturbances both shape health and survival, yet the immune processes linking sociality to health remain poorly understood, particularly in populations experiencing ecological disruption. Here, we examine how social relationships, demographic factors and environmental disturbance relate to variation in white blood cell (leukocyte) composition in free-ranging rhesus macaques (Macaca mulatta). First, we tested whether relationship quality (weak and strong affiliative ties), social status, sex and age were associated with three leukocyte measures: the neutrophil-to-lymphocyte ratio, neutrophil count and eosinophil count. We found opposing sex-specific effects on eosinophil counts. Females with more weak social ties had lower counts whereas males with stronger ties had higher counts. We then used opportunistic cross-sectional data to evaluate how a major natural disaster, Hurricane Maria (in 2017), influenced these immune measures and their link to sociality. Individuals exposed to the hurricane showed elevated leukocyte counts across all three measures but neither social status nor affiliative relationships moderated these effects. Together, these findings document sex-specific links between social structure and immune cell composition, alongside broad immune alterations associated with ecological disturbance. Longitudinal studies will be essential to disentangle causal mechanisms and to understand how social and environmental factors jointly shape immunity in natural populations.

Competition over access to resources, such as food and mates, is one of the major costs associated with group living. Two socioecological factors believed to drive the intensity of competition are group size and sex ratio. However, empirical evidence linking these factors to physical aggression and injuries is scarce. Here, we leveraged 10 years of data from free-ranging female and male rhesus macaques to test whether group size and adult sex ratio predicted the risk of inter and intrasexual aggression, as well as injury risk. We found evidence for an optimal group size at which the risk of intragroup aggression was minimized for both sexes. Despite male-male aggression being lowest in mid-sized groups, males in smaller groups experienced higher injury risk, suggesting within-group aggression might not be the main cause of male injury. Additionally, we found that sex ratio influenced aggression, but not injury risk. Specifically, female aggression toward other females was heightened during the birth season when groups had fewer available males, suggesting either female competition for male friends or exacerbated female-female competition due to the energetic costs of lactation. Male aggression towards females was higher in female-biased groups during the birth season and in male-biased groups during the mating season, which could reflect male competition with females over feeding opportunities and male coercion of females, respectively. Together, these findings provide insights into fitness costs (i.e., injury risk) of inter and intrasexual competition in primates in relation to key aspects of social organization. Significance statement: While theory suggests that group size and sex ratio influence competition, studies linking these factors to aggression and injury rates are limited. Using long-term data on demography, aggression, and injury from a group-living primate, we show that both males and females experience aggression less often at intermediate group sizes. However, males in smaller groups faced higher injury risks. Although sex ratio did not predict injury risk, it did influence intra- and intersexual aggression, with patterns varying by reproductive season. Overall, our findings provide insights into how competition shapes intra and intersexual dynamics in relation to aspects of social organization.

The benefits of social living are well established, but sociality also comes with costs, including infectious disease risk. This cost–benefit ratio of sociality is expected to change across individuals’ lifespans, which may drive changes in social behaviour with age. To explore this idea, we combine data from a group-living primate for which social ageing has been described with epidemiological models to show that having lower social connectedness when older can protect against the costs of a hypothetical, directly transmitted endemic pathogen. Assuming no age differences in epidemiological characteristics (susceptibility to, severity and duration of infection), older individuals suffered lower infection costs, which was explained largely because they were less connected in their social networks than younger individuals. This benefit of ‘social ageing’ depended on epidemiological characteristics and was greatest when infection severity increased with age. When infection duration increased with age, social ageing was beneficial only when pathogen transmissibility was low. Older individuals benefited most from having a lower frequency of interactions (strength) and network embeddedness (closeness) and benefited less from having fewer social partners (degree). Our study provides a first examination of the epidemiology of social ageing, demonstrating the potential for pathogens to influence the evolutionary dynamics of social ageing in natural populations. This article is part of the discussion meeting issue ‘Understanding age and society using natural populations’.

The benefits of social living are well established, but sociality also comes with costs, including infectious disease risk. This cost-benefit ratio of sociality is expected to change across individuals’ lifespans, which may drive changes in social behaviour with age. To explore this idea, we combine data from a group-living primate for which social ageing has been described with epidemiological models to show that having lower social connectedness when older can protect against the costs of a hypothetical, directly transmitted endemic pathogen. Assuming no age differences in epidemiological characteristics (susceptibility to, severity, and duration of infection), older individuals suffered lower infection costs, which was explained largely because they were less connected in their social networks than younger individuals. This benefit of ‘social ageing’ depended on epidemiological characteristics and was greatest when infection severity increased with age. When infection duration increased with age, social ageing was beneficial only when pathogen transmissibility was low. Older individuals benefited most from having a lower frequency of interactions (strength) and network embeddedness (closeness) and benefited less from having fewer social partners (degree). Our study provides a first examination of the epidemiology of social ageing, demonstrating the potential for pathogens to influence evolutionary dynamics of social ageing in natural populations.

Competition over access to resources, such as food and mates, is believed to be one of the major costs associated with group living. Two socioecological factors suggested to predict the intensity of competition are group size and the relative abundance of sexually active individuals. However, empirical evidence linking these factors to injuries and survival costs is scarce. Here, we leveraged 10 years of data from free-ranging rhesus macaques where injuries inflicted by conspecifics are associated with a high mortality risk. We tested if group size and adult sex ratio predicted the occurrence of injuries and used data on physical aggression to contextualise these results. We found that males were less likely to be injured when living in larger groups, potentially due to advantages in intergroup encounters. Females, instead, had higher injury risk when living in larger groups but this was not explained by within-group aggression among females. Further, male-biased sex ratios predicted a weak increase in injury risk in females and were positively related to male-female aggression, indicating that male coercion during mating competition may be a cause of injuries in females. Overall, our results provide insights into sex differences in the fitness-related costs of competition and empirical evidence for long-standing predictions on the evolution of group living.

Increasing age is associated with dysregulated immune function and increased inflammation—patterns that are also observed in individuals exposed to chronic social adversity. Yet we still know little about how social adversity impacts the immune system and how it might promote age-related diseases. Here, we investigated how immune cell diversity varied with age, sex and social adversity (operationalized as low social status) in free-ranging rhesus macaques. We found age-related signatures of immunosenescence, including lower proportions of CD20 + B cells, CD20 + /CD3 + ratio, and CD4 + /CD8 + T cell ratio – all signs of diminished antibody production. Age was associated with higher proportions of CD3 + /CD8 + Cytotoxic T cells, CD16 + /CD3- Natural Killer cells, CD3 + /CD4 + /CD25 + and CD3 + /CD8 + /CD25 + T cells, and CD14 + /CD16 + /HLA-DR + intermediate monocytes, and lower levels of CD14 + /CD16-/HLA-DR + classical monocytes, indicating greater amounts of inflammation and immune dysregulation. We also found a sex-dependent effect of exposure to social adversity (i.e., low social status). High-status males, relative to females, had higher CD20 + /CD3 + ratios and CD16 + /CD3 Natural Killer cell proportions, and lower proportions of CD8 + Cytotoxic T cells. Further, low-status females had higher proportions of cytotoxic T cells than high-status females, while the opposite was observed in males. High-status males had higher CD20 + /CD3 + ratios than low-status males. Together, our study identifies the strong age and sex-dependent effects of social adversity on immune cell proportions in a human-relevant primate model. Thus, these results provide novel insights into the combined effects of demography and social adversity on immunity and their potential contribution to age-related diseases in humans and other animals.

Parasites and infectious diseases constitute an important challenge to the health of group-living animals. Social contact and shared space can both increase disease transmission risk, while individual differences in social resources can help prevent infections. For example, high social status individuals and those with more or stronger social relationships may have better immunity and, thus, lower parasitic burden. To test for health trade-offs in the costs and benefits of sociality, we quantified how parasitic load varied with an individual’s social status, as well as with their weak and strong affiliative relationships in a free-ranging population of rhesus macaques ( Macaca mulatta ). Social resources may also protect against infection under environmentally challenging situations, such as natural disasters. We additionally examined the impact of a major hurricane on the sociality-parasite relationship in this system. We found that both weak and strong proximity partners, but not grooming partners, were associated with lower protozoa infection risk. Social status was not linked to infection risk, even after the hurricane. Overall, our study highlights the buffering against infection that affiliative partners may provide, suggesting individuals can compensate for the health costs of sociality by having partners who tolerate their presence.