Natural disaster and immunological aging in a nonhuman primate

Abstract

Weather-related disasters are increasing in frequency and severity, leaving survivors to cope with ensuing mental, financial, and physical hardships. This adversity can exacerbate existing morbidities, trigger new ones, and increase the risk of mortality—features that are also characteristic of advanced age—inviting the hypothesis that extreme weather events may accelerate aging. To test this idea, we examined the impact of Hurricane Maria and its aftermath on immune cell gene expression in large, age-matched, cross-sectional samples from free-ranging rhesus macaques (Macaca mulatta) living on an isolated island. A cross section of macaques was sampled 1 to 4 y before (n = 435) and 1 y after (n = 108) the hurricane. Hurricane Maria was significantly associated with differential expression of 4% of immune-cell-expressed genes, and these effects were correlated with age-associated alterations in gene expression. We further found that individuals exposed to the hurricane had a gene expression profile that was, on average, 1.96 y older than individuals that were not—roughly equivalent to an increase in 7 to 8 y of a human life. Living through an intense hurricane and its aftermath was associated with expression of key immune genes, dysregulated proteostasis networks, and greater expression of inflammatory immune cell-specific marker genes. Together, our findings illuminate potential mechanisms through which the adversity unleashed by extreme weather and potentially other natural disasters might become biologically embedded, accelerate age-related molecular immune phenotypes, and ultimately contribute to earlier onset of disease and death.

Concentrations of urinary neopterin, but not suPAR, positively correlate with age in rhesus macaques

“…In order to investigate how gene expression related to the neopterin and suPAR phenotypes changes across age, we used gene expression data collected as part of an ongoing study. The complete dataset has been published and described in detail elsewhere (Watowich et al, 2022). In brief, whole blood was drawn from sedated rhesus macaques by veterinary staff.…”

“…The ages of these individuals at the time of sampling ranged from 3 to 28 years, with an average age of 8.6 years. A detailed description of RNA extraction and sequencing protocols is provided in Watowich et al (2022). In short, RNA from 457 samples was extracted using MagMAX for Stabilized Blood Tubes RNA Isolation Kits (Thermo Fisher; Cat.…”

The rhesus macaque as a success story of the Anthropocene

“…Following this extreme weather event, individuals increased their number of social connections on the island, illustrating how the species may use social buffering to mitigate the negative consequences of major anthropogenic events ( Testard et al, 2021 ). Additionally, while hurricanes on the island population have had a significant effect on patterns of gene expression ( Watowich et al, 2022 ) , female rhesus macaques have been shown to increase their fertility later in life such that their lifetime reproductive success is not affected by these events ( Morcillo et al, 2020 ).…”

Age-related differences in ocular features of a naturalistic free-ranging population of rhesus macaques

“…9 Importantly, the aging process of rhesus monkeys is highly similar to that of humans, including declines in physical health, physiological integrity, brain function, and peripheral immune regulation. 9-11…”

“…9 Importantly, the aging process of rhesus monkeys is highly similar to that of humans, including declines in physical health, physiological integrity, brain function, and peripheral immune regulation. [9][10][11] Ocular studies of rhesus macaques have shown close anatomical association between NHP and human visual systems, including features of the optic nerve head, retina, and lens. 8,12,13 While those similarities are well established, detailed data on how aging impacts ocular structures in macaques remain limited to a few studies based on small (which was not certified by peer review) is the author/funder.…”