Molecular Ecology and Natural History of Simian Foamy Virus Infection in Wild-Living Chimpanzees

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 SFVcpz-specific 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.

Retroviruses in Wild-Born Semi-Captive East African Sanctuary Chimpanzees (Pan troglodytes schweinfurthii)~!2010-01-28~!2010-03-24~!2010-04-20~!

“…However, no clustering according to the geographic origin of the chimpanzees was found. The comparison of the strains described here with recently published SFV strains from wild P. t. schweinfurthii from Uganda, Congo and Tanzania [4] could also not identify clustering by geographical origin. These results are consistent with previous findings [4] which could not show region-specific clusters of SFV strains within one chimpanzee subspecies.…”

“…The comparison of the strains described here with recently published SFV strains from wild P. t. schweinfurthii from Uganda, Congo and Tanzania [4] could also not identify clustering by geographical origin. These results are consistent with previous findings [4] which could not show region-specific clusters of SFV strains within one chimpanzee subspecies. However, this study shows in principle the possibility of pathogen introduction to great ape communities in sanctuaries which can cause co-infections with multiple virus strains.…”

“…Phylogenetic tree analysis was performed with the NJ method using the 23 SFV sequences generated in this study and published relevant SFV sequences from all chimpanzee subspecies, as well as from gorilla, bonobo, orangutan, African and Asian monkeys and one sequence of an SFVinfected human [4,6,[8][9][10].…”

“…The prevalence rates ranged from 44% to 100% with several individuals infected with more than one strain [3,4]. An age-dependent prevalence was revealed, with older individuals showing a higher prevalence [4]. Not much is known about the prevalence of STLV in wild chimpanzees.…”

Progress and prospects: Foamy virus vectors enter a new age

“…When Hahn's group looked for evidence of foamy virus infection in wild equatorial African chimpanzees by testing for antibody and nucleic acid in fecal samples, they confirmed a prevalence of between 44 and 100%. 2 Morozov et al 3 found that 12 of 14 free living chimpanzees in Tai National Park (Cô te d'Ivoir) were Semliki forest virus (SFV) infected. The sensitive assays used by Jones-Engel et al 4 found, not only that more than 92% of wild non-human primates were SFV positive in Thailand but that some had already been seroconverted by the age of 3.…”