Viruses in sanctuary chimpanzees across Africa

Abstract

Infectious disease is a major concern for both wild and captive primate populations. Primate sanctuaries in Africa provide critical protection to thousands of wild-born, orphan primates confiscated from the bushmeat and pet trades. However, uncertainty about the infectious agents these individuals potentially harbor has important implications for their individual care and long-term conservation strategies. We used metagenomic next-generation sequencing to identify viruses in blood samples from chimpanzees (Pan troglodytes) in three sanctuaries in West, Central, and East Africa. Our goal was to evaluate whether viruses of human origin or other "atypical" or unknown viruses might infect these chimpanzees. We identified viruses from eight families: Anelloviridae, Flaviviridae, Genomoviridae, Hepadnaviridae, Parvoviridae, Picobirnaviridae, Picornaviridae, and Rhabdoviridae. The majority (15/26) of viruses identified were members of the family Anelloviridae and represent the genera Alphatorquevirus (torque teno viruses) and Betatorquevirus (torque teno mini viruses), which are common in chimpanzees and apathogenic. Of the remaining 11 viruses, 9 were typical constituents of the chimpanzee virome that have been identified in previous studies and are also thought to be apathogenic. One virus, a novel tibrovirus (Rhabdoviridae: Tibrovirus) is related to Bas-Congo virus, which was originally thought to be a human pathogen but is currently thought to be apathogenic, incidental, and vector-borne. The only virus associated with disease was rhinovirus C (Picornaviridae: Enterovirus) infecting one chimpanzee subsequent to an outbreak of respiratory illness at that sanctuary. Our results suggest that the blood-borne virome of African sanctuary chimpanzees does not differ appreciably from that of their wild counterparts, and that persistent infection with exogenous viruses may be less common than often assumed.

Keywords: conservation; great ape; health; metagenomics; virome.

Figure 1

(A) Tacugama Chimpanzee Sanctuary (TCS) in Sierra Leone (orange). (B) Tchimpounga Chimpanzee Rehabilitation Centre (TCRC) in Republic of Congo (purple). (C) Ngamba Island Chimpanzee Sanctuary (NICS) in Uganda (blue). Map created using R v. 4.0.2 (R Core Team, 2020).

Figure 2

Viral prevalence in sanctuary chimpanzees at TCS, TCRC, and NICS. Barplot displays the proportion of individuals at each sanctuary who were positive for at least one virus from the family. ^†Viral genera were assigned using phylogenetic analyses (Supporting Information: Figures S1‐S2). NICS, Ngamba Island Chimpanzee Sanctuary; TCRC, Tchimpounga Chimpanzee Rehabilitation Centre; TCS, Tacugama Chimpanzee Sanctuary.

Figure 3

Heatmap of viral loads of sanctuary chimpanzees at TCS, TCRC, and NICS. Displays viral load data (log₁₀vRPM/kb for each virus: 1–26) and total viral load data (log₁₀vRPM/kb for all viruses) for each individual at each sanctuary. Values range from 0 (lightest) to 4.0 (darkest). ^†Refers to ID in Table 1. NICS, Ngamba Island Chimpanzee Sanctuary; TCRC, Tchimpounga Chimpanzee Rehabilitation Centre; TCS, Tacugama Chimpanzee Sanctuary.

Figure 4

Boxplots of (a) viral richness and (b) total viral load (log₁₀vRPM/kb) for each sanctuary chimpanzee population (TCS, TCRC, and NICS). Kruskal–Wallis test significant p values (<0.05) are displayed. Significant p values for subsequent pairwise comparisons using Wilcoxon rank‐sum tests with the Benjamini‐Hochberg adjustment applied are indicated as follows: *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001. Original and adjusted p values are provided in Supporting Information: Table S6. NICS, Ngamba Island Chimpanzee Sanctuary; TCRC, Tchimpounga Chimpanzee Rehabilitation Centre; TCS, Tacugama Chimpanzee Sanctuary.