Demography, life-history trade-offs, and the gastrointestinal virome of wild chimpanzees

Abstract

In humans, senescence increases susceptibility to viral infection. However, comparative data on viral infection in free-living non-human primates—even in our closest living relatives, chimpanzees and bonobos ( Pan troglodytes and P. paniscus )—are relatively scarce, thereby constraining an evolutionary understanding of age-related patterns of viral infection. We investigated a population of wild eastern chimpanzees ( P. t. schweinfurthii ), using metagenomics to characterize viromes (full viral communities) in the faeces of 42 sexually mature chimpanzees (22 males, 20 females) from the Kanyawara and Ngogo communities of Kibale National Park, Uganda. We identified 12 viruses from at least four viral families possessing genomes of both single-stranded RNA and single-stranded DNA. Faecal viromes of both sexes varied with chimpanzee age, but viral richness increased with age only in males. This effect was largely due to three viruses, salivirus, porprismacovirus and chimpanzee stool-associated RNA virus (chisavirus), which occurred most frequently in samples from older males. This finding is consistent with the hypothesis that selection on males for early-life reproduction compromises investment in somatic maintenance, which has delayed consequences for health later in life, in this case reflected in viral infection and/or shedding. Faecal viromes are therefore useful for studying processes related to the divergent reproductive strategies of males and females, ageing, and sex differences in longevity. This article is part of the theme issue ‘Evolution of the primate ageing process'.

Viruses associated with ill health in wild chimpanzees

“…For the last 27 to 34 years, both communities have grown in size and exhibit high individual survival, with life expectancy higher at Ngogo than at Kanyawara (Muller & Wrangham, 2014;Wood et al, 2017). Using methods previously applied to this chimpanzee population (Negrey et al, 2020), we investigated links between gastrointestinal viruses and general health. Our goal was to identify which viruses, if any, were associated with observed episodes of ill health in this population and may act as biomarkers of illness.…”

Bat Flies of the Family Streblidae (Diptera: Hippoboscoidea) Host Relatives of Medically and Agriculturally Important “Bat-Associated” Viruses

“…We measured viral concentrations as viral reads per million total reads per kilobase of target sequence (vRPM/kb), which is a metagenomic proxy for viral load that has been validated by comparison to quantitative real time polymerase chain reaction [ 28 , 29 , 30 ]. We calculated this measure for each virus in each sample by mapping reads to the polymerase gene sequence (or obtained portion thereof, when available) of each identified virus at 90% sequence identity then log 10 transforming the results for ease of visualization.…”

Insights from evolutionarily relevant models for human ageing

“…Two other papers translate clinical approaches to frailty to field conditions, examining ecologically relevant measures of physical performance in wild chimpanzees [90] and African foragers and pastoralists [91]. Other papers test for immunosenescence, which is difficult to measure directly in wild primates, but is detectable through its functional outcomes: age-related increases in parasitic [92] and viral infections [93]. Others have taken the opposite approach of dissecting complex phenomena like cognitive [94,95]), neurobiological [96] and skeletal ageing [97] to examine whether they result from common mechanisms across species.…”

“…The contributions in this volume highlight extensive similarities in the ageing processes between humans and other primates across a variety of domains. For example, several contributions demonstrate shared patterns of immunosenescence, both in its specific regulatory mechanisms [64] and its effects on infectious disease burden in the wild [92,93]). While the process of immunosenescence in human ageing is well recognized, the role of infectious disease in driving late-age mortality has diminished in industrialized nations relative to the role of degenerative diseases.…”

“…Compared with humans, many primates exhibit high levels of aggressive male competition, generating both direct and indirect impacts on health via risk of injury, physiological stress and energetic expenditure [101]. Contributed studies indicate that wild chimpanzee males are more vulnerable to viral infections and losses of physical condition with age than are females [90,93] and that wild male baboons who attain high social status pay the price of a reduced lifespan [102]. Conversely, among chimpanzees in sanctuaries, females exhibited more proatherogenic lipid profiles than males across the lifespan [98].…”