Viruses associated with ill health in wild chimpanzees

Abstract

Viral infection is a major cause of ill health in wild chimpanzees (Pan troglodytes), but most evidence to date has come from conspicuous disease outbreaks with high morbidity and mortality. To examine the relationship between viral infection and ill health during periods not associated with disease outbreaks, we conducted a longitudinal study of wild eastern chimpanzees (P. t. schweinfurthii) in the Kanyawara and Ngogo communities of Kibale National Park, Uganda. We collected standardized, observational health data for 4 years and then used metagenomics to characterize gastrointestinal viromes (i.e., all viruses recovered from fecal samples) in individual chimpanzees before and during episodes of clinical disease. We restricted our analyses to viruses thought to infect mammals or primarily associated with mammals, discarding viruses associated with nonmammalian hosts. We found 18 viruses (nine of which were previously identified in this population) from at least five viral families. Viral richness (number of viruses per sample) did not vary by health status. By contrast, total viral load (normalized proportion of sequences mapping to viruses) was significantly higher in ill individuals compared with healthy individuals. Furthermore, when ill, Kanyawara chimpanzees exhibited higher viral loads than Ngogo chimpanzees, and males, but not females, exhibited higher infection rates with certain viruses and higher total viral loads as they aged. Post-hoc analyses, including the use of a machine-learning classification method, indicated that one virus, salivirus (Picornaviridae), was the main contributor to health-related and community-level variation in viral loads. Another virus, chimpanzee stool-associated virus (chisavirus; unclassified Picornavirales), was associated with ill health at Ngogo but not at Kanyawara. Chisavirus, chimpanzee adenovirus (Adenoviridae), and bufavirus (Parvoviridae) were also associated with increased age in males. Associations with sex and age are consistent with the hypothesis that nonlethal viral infections cumulatively reflect or contribute to senescence in long-lived species such as chimpanzees.

Keywords: chimpanzee; conservation; disease; health; metagenomics; virus.

Figure 1.

Heatmap of viral loads for all 19 chimpanzees, grouped by community and health status. Values range from 0 (lightest) to 3.3 Log₁₀(vRPM/kb) (darkest). Viruses are numbered as per Table 1.

Figure 2.

Chimpanzee gastrointestinal total viral load as a function of clinical signs (a) in all individuals and (b) by study community. In 2b, light and dark boxes represent Kanyawara and Ngogo, respectively. Thick horizontal bars represent medians, and the upper and lower bounds of each box represent the 75th and 25th percentiles, respectively.

Figure 3.

Mean viral loads for (a) all chimpanzees by health status and (b) male chimpanzees by age. “Prime” and “past-prime” refer to individuals aged <30 years and ≥30 years, respectively. Vertical bars indicate standard deviations.