The biology of aging in a social world: Insights from free-ranging rhesus macaques

Abstract

Social adversity can increase the age-associated risk of disease and death, yet the biological mechanisms that link social adversities to aging remain poorly understood. Long-term naturalistic studies of nonhuman animals are crucial for integrating observations of social behavior throughout an individual's life with detailed anatomical, physiological, and molecular measurements. Here, we synthesize the body of research from one such naturalistic study system, Cayo Santiago, which is home to the world's longest continuously monitored free-ranging population of rhesus macaques (Macaca mulatta). We review recent studies of age-related variation in morphology, gene regulation, microbiome composition, and immune function. We also discuss ecological and social modifiers of age-markers in this population. In particular, we summarize how a major natural disaster, Hurricane Maria, affected rhesus macaque physiology and social structure and highlight the context-dependent and domain-specific nature of aging modifiers. Finally, we conclude by providing directions for future study, on Cayo Santiago and elsewhere, that will further our understanding of aging across different domains and how social adversity modifies aging processes.

Keywords: Aging; Cayo Santiago; Primate; Senescence; Social behavior.

Figure 1.

Aging in macaques and humans. Rhesus macaques display a similar but condensed survival trajectory compared to humans, aging at a rate of about three to four times higher. Median lifespan for captive rhesus macaques (indicated by an asterisk) is likely lower than indicated here, as the survival curve is generated from a previously published study (Mattison et al., 2017) that enrolled monkeys cross-sectionally, potentially introducing selection bias and minimizing sources of infant mortality. Reprinted with permission from “Rhesus macaques as a tractable physiological model of human ageing,” by KL Chiou et al., 2020, Philosophical Transactions of the Royal Society B: Biological Sciences, 375. Copyright 2020 by The Royal Society.

Figure 2.

Deeply phenotyped Cayo Santiago rhesus macaques. Demographic data collection (i.e., births, deaths, group membership) on Cayo Santiago was initiated in 1956. Since then, data collection methods have continued to expand: biological samples and behavioral data are collected both cross-sectionally and longitudinally across hundreds of individuals. From these biological samples, it is possible to generate numerous biomarkers of aging. This combination of rich biological, behavioral, and demographic data allows an unparalleled phenotyping and characterization of sociality and aging across biological systems in this nonhuman primate population. Original macaque photo by L.J.N. Brent. All other graphics were created with BioRender.com.