Wide distribution and ancient evolutionary history of simian foamy viruses in New World primates

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.

A non-invasive specimen collection method and a novel simian foamy virus (SFV) DNA quantification assay in New World primates reveal aspects of tissue tropism and improved SFV detection

“…For example, primers for our original diagnostic nested PCR assay that detects short pol sequences were designed using the only three complete NWP SFV genomes that were available at that time [ 11 ]. Primer design for the qPCR assay used additional NWP pol sequences available at GenBank from a broader diversity of NWP SFV and was able to detect SFV in more NWPs most of which were also WB-positive, including two additional species of Leontopithecus , and one species each of Callimico and Saguinus previously found to be SFV-negative using the original nested PCR assay [ 11 , 12 ]. Altogether, our findings suggest that the combined use of the novel qPCR assay described herein and WB testing will provide a more accurate estimate of SFV prevalence in NWPs.…”

“…For the diagnostic pol PCR assay, each sample was tested in triplicate in three different assay runs and a sample was considered positive if any of the replicates tested positive. This diagnostic pol PCR assay has a high sensitivity for detection of diverse NWP SFV variants with a reported 100% (92–100%, 95% confidence interval (CI)) sensitivity, and 91% specificity (79–97%, 95% CI) when compared with WB results [ 11 , 12 ].…”

“…More recently, Ghersi et al . developed and validated specific ELISA and western blot (WB) tests as well as generic PCR assays to assess the prevalence of SFV in NWPs living in U.S. zoos and at rescue centers and trade markets in Peru [ 12 ]. Of the captive NWPs from the U.S., 45% were SFV WB-positive, while 38% of captive and wild-caught NWPs from Peru were positive [ 12 ].…”

“…developed and validated specific ELISA and western blot (WB) tests as well as generic PCR assays to assess the prevalence of SFV in NWPs living in U.S. zoos and at rescue centers and trade markets in Peru [ 12 ]. Of the captive NWPs from the U.S., 45% were SFV WB-positive, while 38% of captive and wild-caught NWPs from Peru were positive [ 12 ]. Following this study, we used the same serologic and PCR methods to investigate the prevalence and species distribution of NWP SFV in 140 captive monkeys from Brazil, finding an overall serologic and molecular prevalence of 43% and 34%, respectively, and identified distinct SFV in four NWP genera [ 13 ].…”

Genome Analysis and Replication Studies of the African Green Monkey Simian Foamy Virus Serotype 3 Strain FV2014

“…The large number of studies demonstrating broad distribution of SFVs in Old World and New World NHPs and species-specific prevalence of SFV strains have been based on sequence analysis of genomic regions [8,[24][25][26][27][28][29][30][31][32][33][34]. Whole-genome analysis of some isolates has shown that genetically-diverse SFV strains circulating in different NHP species have contributed to the generation of recombinant viruses involving the SU region in env [11,12,35].…”