Sociality predicts individual variation in the immunity of free-ranging rhesus macaques

Pavez-Fox, Melissa A.; Valle, Josué E. Negrón-Del; Thompson, Indya J; Walker, Christopher S.; Bauman, Samuel; González, Olga; Compo, Nicole; Ruíz-Lambides, Angelina; Martínez, Melween I.; Platt, Michael L.; Montague, Michael J.; Higham, James P.; Snyder‐Mackler, Noah; Brent, Lauren J. N.

doi:10.1016/j.physbeh.2021.113560

Cited by 15 publications

(23 citation statements)

References 64 publications

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“…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 [86]. 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.…”

Section: Discussioncontrasting

confidence: 55%

“…These differences might be explained in part by differences in features of the two study systems. Animals on Cayo Santiago are provisioned with food on a daily basis and access to the nutrients needed to support immune function might not be as skewed as they are in the wild [45]. Notwithstanding, in both systems high social status has been associated with elevated levels of glucocorticoids and androgens [72, 73, 50], well known immune-suppressors, which suggest that in the Cayo Santiago population, unlike the baboons, the benefits of being of high status may not outweigh the costs in terms of injury recovery.…”

Section: Discussionmentioning

confidence: 99%

“…Yet despite clear hypotheses for the potential mechanisms by which social status and affiliative relationships influence lifespan, there remains a lack of empirical evidence for these mechanisms affecting survival. For example, several studies have shown associations between individual variation in sociality with markers of health and immunity [44, 45, 35, 36], yet the consequences of such differences in the face of naturally occurring challenges to health, and the downstream impact those differences might have on survival are unknown. Similarly, studies supporting a relationship between sociality and lifespan usually do not have the detailed physiological or health data required to test potential mechanisms connecting the two [1].…”

mentioning

confidence: 99%

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

Pavez-Fox

Kimock

Rivera-Barreto

et al. 2022

Preprint

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Affiliative social relationships and high social status predict longer lifespans in many mammal species, including humans. Yet, the mechanisms by which these components of sociality influence survival are still largely unknown. Using 10 years of long-term data on the incidence of injuries in a free-ranging population of rhesus macaques (Macaca mulatta), we investigated two possible mechanisms that could underpin the relationship between sociality and survival: sociality (1) reduces injury risk; and/or (2) increases the probability of survival after an injury. Our results showed that injured animals had a near three-fold increase in the probability of dying, confirming that injuries can be fatal in this population. Crucially, we found that sociality may reduce an individual's injury risk, but had no effect on the probability of injured individuals dying. Individuals with more affiliative partners and higher social status experienced fewer injuries compared to less socially integrated or lower status animals, with the effect of social status varying with age. Females living in bigger groups were more likely to be injured than those in smaller groups, while in males, smaller groups were associated with higher chances of being injured. Our study contributes novel evidence that sociality does not provide fitness benefits via socially-mediated promotion of injury recovery, but instead can enhance fitness by reducing the risk of being fatally injured in the first place.

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Section: Discussioncontrasting

confidence: 55%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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

Pavez-Fox

Kimock

Rivera-Barreto

et al. 2022

Preprint

Self Cite

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“…Moreover, direct relationships may be more relevant for biological success in this population, for example, by mitigating the negative consequences of adversity ( 43 ). Notably, markers of immunity also vary more strongly with direct social connections than with social status or indirect connections in this same population ( 44 ). Other aspects of neuroanatomy, such as white matter tract integrity, have revealed a complementary picture of the relationship between sociality and brain structure in humans ( 45 , 46 ), and future studies in macaques should address these possibilities.…”

Section: Discussionmentioning

confidence: 99%

Social connections predict brain structure in a multidimensional free-ranging primate society

et al. 2022

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Reproduction and survival in most primate species reflects management of both competitive and cooperative relationships. Here, we investigated the links between neuroanatomy and sociality in free-ranging rhesus macaques. In adults, the number of social partners predicted the volume of the mid–superior temporal sulcus and ventral-dysgranular insula, implicated in social decision-making and empathy, respectively. We found no link between brain structure and other key social variables such as social status or indirect connectedness in adults, nor between maternal social networks or status and dependent infant brain structure. Our findings demonstrate that the size of specific brain structures varies with the number of direct affiliative social connections and suggest that this relationship may arise during development. These results reinforce proposed links between social network size, biological success, and the expansion of specific brain circuits.

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“…Differences in social status result in differences in the extent to which individuals can access resources (15), which is a feature also commonly seen in human populations. Like humans, social status in macaques affects health and survival (16), with individuals that have more social connections presenting lower white blood cells (17)-possibly affecting inflammatory responses.…”

Section: Introductionmentioning

confidence: 99%

Age, sex, and social environmental effects on immune cell composition in a free-ranging non-human primate

Rosado

Marzan-Rivera

Watowich

et al. 2021

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Aging results in declines in immune function and increases in inflammation, which underlie many age-related diseases. These immunosenescent signatures are similar to those seen in individuals exposed to social adversity, who may age more rapidly than those unexposed. Yet, it is unclear how social adversity alters immunity across demographic factors - data that are essential to identify how it might increase aging-related diseases. Here, we investigated how age, sex, and social adversity predicted immune cell proportions in 250 rhesus macaques living in a semi-naturalistic colony. As macaques aged, they exhibited signatures of immunosenescence. Older individuals had signatures of diminished antibody production and adaptive immunity, with declines in CD20+ B cells, CD20+/CD3+ cell ratio, and the CD4+/CD8+ T cell ratio. At all ages, females had higher CD20+/CD3+ and CD4+/CD8+ ratios, indicative of a stronger antibody and adaptive immune response that may facilitate pathogen clearance even with increasing age. Older individuals had signatures of inflammation, with higher proportions of CD3+/CD8+ Cytotoxic T cells, CD16+/CD3- Natural Killer cells, CD3+/CD4+/CD25+ and CD3+/CD8+/CD25+ T regulatory cells, and CD14+/CD16+/HLA-DR+ intermediate monocytes, combined with lower levels of CD14+/CD16-/HLA-DR+ classical monocytes. Notably, we found an interaction between age and social adversity, where low-status individuals had higher proportions of CD3+/CD4+/CD25+ T regulatory cells for their age, compared to higher-status individuals. Together, our study identifies immune cell types that are affected by age and sex in the premier nonhuman primate model of human biology and behavior, and demonstrate a novel link between inflammatory CD4+ T regulatory cells and social adversity.

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Sociality predicts individual variation in the immunity of free-ranging rhesus macaques

Cited by 15 publications

References 64 publications

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

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

Social connections predict brain structure in a multidimensional free-ranging primate society

Age, sex, and social environmental effects on immune cell composition in a free-ranging non-human primate

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