Early life adversity has sex-dependent effects on survival across the lifespan in rhesus macaques

Abstract

Exposure to adversity during early life is linked to lasting detrimental effects on evolutionary fitness across many taxa. However, due to the challenges of collecting longitudinal data, especially in species where one sex disperses, direct evidence 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) at Cayo Santiago, Puerto Rico. We leveraged six decades of data to quantify the relative importance of ten forms of early life adversity for 6,599 macaques (3,230 male, 3,369 female), with a smaller sample size (N=299) for one form of adversity (maternal social isolation) which required high-resolution behavioral data. We found that individuals who experienced more early life adversity died earlier than those who experienced less adversity. Mortality risk was highest during early life, defined as birth to four years old, suggesting acute survival effects of adversity, but heightened mortality risk was also present in macaques who survived to adulthood. Females and males were affected differently by some forms of adversity, and these differences might be driven by varying energetic demands, female philopatry, and male dispersal. By leveraging data on thousands of macaques collected over decades, 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 in long-lived species. Significance Statement Exposure to early life adversity, even when conditions subsequently improve, can have profound and persistent consequences for human health. Negative effects of early life adversity appear widespread across the animal kingdom. To date, however, direct evidence from long-lived species is relatively scarce due to the difficulties of collecting data from early life till death. We leverage six decades of observations on thousands of free-ranging male and female rhesus macaques to examine the complex ways early life adversity impacts survival. Our results suggest that the type of adversity and life history factors intersect to impact immediate and downstream survival. By studying early life adversity across environments, cultures, contexts, and species, we can better understand the evolutionary underpinnings of early life sensitivities.