Josue E. Negron-Del Valle

Exposure to early life adversity is linked to detrimental fitness outcomes across taxa. Owing to the challenges of collecting longitudinal data, direct evidence for long-term fitness effects of early life adversity from long-lived species remains relatively scarce. Here, we test the effects of early life adversity on male and female longevity in a free-ranging population of rhesus macaques ( Macaca mulatta ) on Cayo Santiago, Puerto Rico. We leveraged six decades of data to quantify the relative importance of 10 forms of early life adversity for 6599 macaques. Individuals that experienced more early life adversity died earlier than those that experienced less adversity. Mortality risk was highest during early life, defined as birth to 4 years old, but heightened mortality risk was also present in macaques that survived to adulthood. Females and males were affected differently by some forms of adversity, and these differences might be driven by varying energetic demands and dispersal patterns. Our results show that the fitness consequences of early life adversity are not uniform across individuals but vary as a function of the type of adversity, timing and social context, and thus contribute to our limited but growing understanding of the evolution of early life sensitivities. 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 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’.

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.