Abstract
BackgroundAlthough simian foamy viruses (SFV) are the only exogenous retroviruses to infect New World monkeys (NWMs), little is known about their evolutionary history and epidemiology. Previous reports show distinct SFVs among NWMs but were limited to small numbers of captive or wild monkeys from five (Cebus, Saimiri, Ateles, Alouatta, and Callithrix) of the 15 NWM genera. Other studies also used only PCR testing or serological assays with limited validation and may have missed infection in some species. We developed and validated new serological and PCR assays to determine the prevalence of SFV in blood specimens from a large number of captive NWMs in the US (n = 274) and in captive and wild-caught NWMs (n = 236) in Peruvian zoos, rescue centers, and illegal trade markets. Phylogenetic and co-speciation reconciliation analyses of new SFV polymerase (pol) and host mitochondrial cytochrome B sequences, were performed to infer SFV and host co-evolutionary histories.Results124/274 (45.2 %) of NWMs captive in the US and 59/157 (37.5 %) of captive and wild-caught NWMs in Peru were SFV WB-positive representing 11 different genera (Alouatta, Aotus, Ateles, Cacajao, Callithrix, Cebus, Lagothrix, Leontopithecus, Pithecia, Saguinus and Saimiri). Seroprevalences were lower at rescue centers (10/53, 18.9 %) compared to zoos (46/97, 47.4 %) and illegal trade markets (3/7, 8/19, 42.9 %) in Peru. Analyses showed that the trees of NWM hosts and SFVs have remarkably similar topologies at the level of species and sub-populations suggestive of co-speciation. Phylogenetic reconciliation confirmed 12 co-speciation events (p < 0.002) which was further supported by obtaining highly similar divergence dates for SFV and host genera and correlated SFV-host branch times. However, four ancient cross-genus transmission events were also inferred for Pitheciinae to Atelidae, Cacajao to ancestral Callithrix or Cebus monkeys, between Callithrix and Cebus monkeys, and Lagothrix to Alouatta.ConclusionsWe demonstrate a broad distribution and stable co-speciation history of SFV in NWMs at the species level. Additional studies are necessary to further explore the epidemiology and natural history of SFV infection of NWMs and to determine the zoonotic potential for persons exposed to infected monkeys in captivity and in the wild.Electronic supplementary materialThe online version of this article (doi:10.1186/s12977-015-0214-0) contains supplementary material, which is available to authorized users.
Highlights
Simian foamy viruses (SFV) are the only exogenous retroviruses to infect New World monkeys (NWMs), little is known about their evolutionary history and epidemiology
SFV sequences were detected in 61 individual animals (57 %) from seven genera in each of the three NWM families Pitheciidae, Atelidae, and Cebidae, including Cebus apella (24/28, 85.7 %), Cebus albifrons (3/3, 100 %), Alouatta palliata (1/1), Alouatta seniculus sara (3/3, 100 %), Callithrix jacchus (1/10, 10 %), Ateles species (1/1), Ateles belzebuth hybridus (1/1, 100 %), Ateles geoffroyi (15/17, 88.2 %), Ateles fusciceps robustus (3/5, 60 %), Saimiri boliviensis (3/6, 50 %), Saimiri boliviensis peruviensis (3/7, 42.9 %), Cacajao rubicundus (2/2), and Pithecia pithecia (1/1)
These results demonstrate the ability of the diagnostic primers to broadly detect SFV diversity in a wide range of divergent NWM species
Summary
Simian foamy viruses (SFV) are the only exogenous retroviruses to infect New World monkeys (NWMs), little is known about their evolutionary history and epidemiology. Simian foamy viruses (SFVs) were first described in 1954 as contaminants in primary monkey kidney cultures [6] and since have been identified in many Old World and New World primate species using a variety of laboratory methods [5, 7]. Humans can be zoonotically infected with a variety of SFVs originating from Old World monkeys and apes (OWMA) through occupational and natural exposures but demonstrate an apparently asymptomatic though persistent infection [5, 8, 9]. Most humans infected with SFV reported NHP bite or scratch exposures with higher prevalences seen in persons with severe bite wounds [10, 18,19,20,21]
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