Simultaneous outbreaks of respiratory disease in wild chimpanzees caused by distinct viruses of human origin

Abstract

Respiratory viruses of human origin infect wild apes across Africa, sometimes lethally. Here we report simultaneous outbreaks of two distinct human respiratory viruses, human metapneumovirus (MPV; Pneumoviridae : Metapneumovirus ) and human respirovirus 3 (HRV3; Paramyxoviridae ; Respirovirus , formerly known as parainfluenza virus 3), in two chimpanzee ( Pan troglodytes schweinfurthii ) communities in the same forest in Uganda in December 2016 and January 2017. The viruses were absent before the outbreaks, but each was present in ill chimpanzees from one community during the outbreak period. Clinical signs and gross pathologic changes in affected chimpanzees closely mirrored symptoms and pathology commonly observed in humans for each virus. Epidemiologic modelling showed that MPV and HRV3 were similarly transmissible ( R 0 of 1.27 and 1.48, respectively), but MPV caused 12.2% mortality mainly in infants and older chimpanzees, whereas HRV3 caused no direct mortality. These results are consistent with the higher virulence of MPV than HRV3 in humans, although both MPV and HRV3 cause a significant global disease burden. Both viruses clustered phylogenetically within groups of known human variants, with MPV closely related to a lethal 2009 variant from mountain gorillas ( Gorilla beringei beringei ), suggesting two independent and simultaneous reverse zoonotic origins, either directly from humans or via intermediary hosts. These findings expand our knowledge of human origin viruses threatening wild chimpanzees and suggest that such viruses might be differentiated by their comparative epidemiological dynamics and pathogenicity in wild apes. Our results also caution against assuming common causation in coincident outbreaks.

Lack of Rule-Adherence During Mountain Gorilla Tourism Encounters in Bwindi Impenetrable National Park, Uganda, Places Gorillas at Risk From Human Disease

“…Benefits beyond revenue generation include protection of gorillas and their habitats, daily monitoring to identify any gorilla health issues, and facilitation of detailed research on behavior and ecology offering enhanced understanding of population dynamics including births, deaths, and dispersal patterns [e.g., (4,11,12)]. Costs of habituation include reduced avoidance of humans (13), potentially increasing the likelihood of crop raiding and/or susceptibility to poaching [e.g., (14)(15)(16)], and increased risk of disease spread by close proximity with humans and livestock (5,7,(17)(18)(19)(20)(21)(22)(23)(24)(25). This risk is intensified by the high number of international visitors, generating potential for exposure to foreign infections to which local humans and great apes lack resistance (21,(26)(27)(28)(29)(30)(31).…”

Genetic diversity of primate strongylid nematodes: Do sympatric nonhuman primates and humans share their strongylid worms?

“…Other examples of successful application of genotyping tools to study helminth infections in humans and NHPs include e.g., Schistosoma (Červená et al, ) and Enterobius (Nakano, Okamoto, Ikeda, & Hasegawa, ). Nevertheless, there can also be challenges with these methods (see e.g., anoplocephalid tapeworms: Doležalová et al, ) and compared to the growing body of evidence for cross‐species infections by viruses and bacteria (e.g., Negrey et al, ; Rwego, Isabirye‐Basuta, Gillespie, & Goldberg, ), there is still much less known about the molecular diversity and transmission of protozoans and helminths infecting sympatric humans and wild NHPs.…”

“…Nevertheless, there can also be challenges with these methods (see e.g., anoplocephalid tapeworms: Doležalová et al, 2015) and compared to the growing body of evidence for cross-species infections by viruses and bacteria (e.g., Negrey et al, 2019;Rwego, Isabirye-Basuta, Gillespie, & Goldberg, 2008), there is still much less known about the molecular diversity and transmission of protozoans and helminths infecting sympatric humans and wild NHPs. Strongylids (Nematoda: Secernentea: Strongylida) represent a major radiation of nematodes, with a vast diversity of mammalian gastrointestinal parasites (Lichtenfels, Kharchenko, & Dvojnos, 2008;Rothman & Bowman, 2003;Van Wyk, Cabaret, & Michael, 2004), including some important human pathogens (Brooker, Bethony, & Hotez, 2004).…”

Periodic catastrophes over human evolutionary history are necessary to explain the forager population paradox

“…have experienced atypical circumstances: Ngogo experienced high mortality from respiratory infection shortly after the study period (32), and its current age distribution suggests their low mortality profile may reflect a transient phase. Likewise, Taï chimpanzees experienced anthropogenic impacts, including an Ebola epidemic and respiratory infection (23).…”