Molecular ecology and natural history of Simian foamy virus infection in wild-living chimpanzees

Weimin Liu, Michael Worobey, Yingying Li, Brandon F. Keele, Frederic Bibollet-Ruche, Yuanyuan Guo, Paul A. Goepfert, Mario L. Santiago, Jean Bosco N Ndjango, Cecile Neel, Stephen L. Clifford, Crickette Sanz, Shadrack Kamenya, Michael L. Wilson, Anne E. Pusey, Nicole Gross-Camp, Christophe Boesch, Vince Smith, Koichiro Zamma, Michael A. HuffmanJohn C. Mitani, David P. Watts, Martine Peeters, George M. Shaw, William M. Switzer, Paul M. Sharp, Beatrice H. Hahn

Research output: Contribution to journalArticlepeer-review

122 Scopus citations

Abstract

Identifying microbial pathogens with zoonotic potential in wild-living primates can be important to human health, as evidenced by human immunodeficiency viruses types 1 and 2 (HIV-1 and HIV-2) and Ebola virus. Simian foamy viruses (SFVs) are ancient retroviruses that infect Old and New World monkeys and apes. Although not known to cause disease, these viruses are of public health interest because they have the potential to infect humans and thus provide a more general indication of zoonotic exposure risks. Surprisingly, no information exists concerning the prevalence, geographic distribution, and genetic diversity of SFVs in wild-living monkeys and apes. Here, we report the first comprehensive survey of SFVcpz infection in free-ranging chimpanzees (Pan troglodytes) using newly developed, fecal-based assays. Chimpanzee fecal samples (n = 724) were collected at 25 field sites throughout equatorial Africa and tested for SFVcpzspecific antibodies (n = 706) or viral nucleic acids (n = 392). SFVcpz infection was documented at all field sites, with prevalence rates ranging from 44% to 100%. In two habituated communities, adult chimpanzees had significantly higher SFVcpz infection rates than infants and juveniles, indicating predominantly horizontal rather than vertical transmission routes. Some chimpanzees were co-infected with simian immunodeficiency virus (SIVcpz); however, there was no evidence that SFVcpz and SIVcpz were epidemiologically linked. SFVcpz nucleic acids were recovered from 177 fecal samples, all of which contained SFVcpz RNA and not DNA. Phylogenetic analysis of partial gag (616 bp), pol-RT (717 bp), and pol-IN (425 bp) sequences identified a diverse group of viruses, which could be subdivided into four distinct SFVcpz lineages according to their chimpanzee subspecies of origin. Within these lineages, there was evidence of frequent superinfection and viral recombination. One chimpanzee was infected by a foamy virus from a Cercopithecus monkey species, indicating cross-species transmission of SFVs in the wild. These data indicate that SFVcpz (i) is widely distributed among all chimpanzee subspecies; (ii) is shed in fecal samples as viral RNA; (iii) is transmitted predominantly by horizontal routes; (iv) is prone to superinfection and recombination; (v) has co-evolved with its natural host; and (vi) represents a sensitive marker of population structure that may be useful for chimpanzee taxonomy and conservation strategies.

Original languageEnglish (US)
Article numbere1000097
JournalPLoS pathogens
Volume4
Issue number7
DOIs
StatePublished - Jul 2008

Bibliographical note

Funding Information:
We thank Bienvenue Yangda, Aimee Mebenga, Innocent Ndong Bass, and Eitel Mpoudi-Ngole for field work and logistical support in Cameroon; Kadaha John, Matendo Msafiri, Iddi Issa, Gabo Paulo, Tofiki Mikidadi, and Elizabeth Lonsdorf for sample collection and logistical support in Gombe National Park (Tanzania); Jeremiah Lwanga, Adolph Magoba, Godfrey Mbabazi, Lawrence Ndegezi, and Alfred Tumusiime for sample collection and logistical support at Ngogo (Uganda); Henry Cirhuza and Jean-Claude Kyungu for sample collection in Walikale (DRC); Karl Amman for sample collection in Bondo (DRC); David Morgan for sample collection in the Goualougo Triangle (Republic of Congo); the Ivorian Ministry of the Environment and Forests, the Ivorian Ministry of Research, and the Swiss Research Center in Côte d'Ivoire for permission to conduct research in the Taï National Park; the Cameroonian Ministries of Health, Environment and Forestry, and Research for permission to collect samples in Cameroon; the Republic of Congo Ministry of Science and Technology and Ministry of Forest Economy for permission to collect samples in the Goualougo Triangle; the Tanzania National Parks, the Tanzania Commission for Science and Technology, and the Tanzania Wildlife Research Institute for permission to conduct research in Gombe and Mahale Mountains National Parks; the Uganda Wildlife Authority, the Uganda National Council for Science and Technology, and the Makerere University Biological Field Station for permission to conduct research in Ngogo; the Rwandan Office of Tourism and National Parks for permission to collect samples in Nyungwe National Park; the Department of Ecology and Management of Plant and Animal Resources (University of Kisangani) for authorization to collect samples in DRC; researchers at the Institut Congolais pour la Conservation et la Nature, the Parc National de la Lopé, the Conservation Project of the Nyungwe Forest, and the Gombe Stream Research Centre for logistical support; the Yerkes Primate Center staff for shipping fecal samples from SFVcpz infected captive chimpanzees; Joann Schumacher-Stankey for demographic records of Gombe chimpanzees; Fabian Leendertz and Fran van Heuverswyn for providing unpublished data; Maxine Lineal, Paul Bieniasz, and John Brookfield for helpful discussions; Maria Salazar, Yalu Chen, and Barry Cochran for expert technical assistance; and Jamie White for artwork and manuscript preparation. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.

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