Genetic Diversity of Neotropical Primates: Phylogeny, Population Genetics, and Animal Models for Infectious Diseases

Moreira, Miguel A. M.; Bonvicino, Cibele Rodrigues; Soares, Marcelo A.; Seuánez, Héctor N.

doi:10.1159/000291485

Cited by 5 publications

(6 citation statements)

References 183 publications

(120 reference statements)

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“…S1). One clear example is the clustering of SFV pol sequences from an African green monkey (agm) and chimpanzee (cpz) within a NWM clade which have been shown previously to form distinct phylogenetic clades [18] (Fig. S1).…”

Section: Resultsmentioning

confidence: 93%

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Identification and Characterization of Highly Divergent Simian Foamy Viruses in a Wide Range of New World Primates from Brazil

et al. 2013

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Foamy viruses naturally infect a wide range of mammals, including Old World (OWP) and New World primates (NWP), which are collectively called simian foamy viruses (SFV). While NWP species in Central and South America are highly diverse, only SFV from captive marmoset, spider monkey, and squirrel monkey have been genetically characterized and the molecular epidemiology of SFV infection in NWPs remains unknown. We tested a large collection of genomic DNA (n = 332) comprising 14 genera of NWP species for the presence of SFV polymerase (pol) sequences using generic PCR primers. Further molecular characterization of positive samples was carried out by LTR-gag and larger pol sequence analysis. We identified novel SFVs infecting nine NWP genera. Prevalence rates varied between 14–30% in different species for which at least 10 specimens were tested. High SFV genetic diversity among NWP up to 50% in LTR-gag and 40% in pol was revealed by intragenus and intrafamilial comparisons. Two different SFV strains infecting two captive yellow-breasted capuchins did not group in species-specific lineages but rather clustered with SFVs from marmoset and spider monkeys, indicating independent cross-species transmission events. We describe the first SFV epidemiology study of NWP, and the first evidence of SFV infection in wild NWPs. We also document a wide distribution of distinct SFVs in 14 NWP genera, including two novel co-speciating SFVs in capuchins and howler monkeys, suggestive of an ancient evolutionary history in NWPs for at least 28 million years. A high SFV genetic diversity was seen among NWP, yet these viruses seem able to jump between NWP species and even genera. Our results raise concerns for the risk of zoonotic transmission of NWP SFV to humans as these primates are regularly hunted for food or kept as pets in forest regions of South America.

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Section: Resultsmentioning

confidence: 93%

“…NWP are a diverse group of American primates, comprising over 110 different species in 15–19 genera and three families (Atelidae, Aotidae, Cebidae, and Pitheciidae) [18], [19]. However, molecular characterization of SFV has been reported for only three species of captive NWP, Ateles sp .…”

Section: Introductionmentioning

confidence: 99%

Identification and Characterization of Highly Divergent Simian Foamy Viruses in a Wide Range of New World Primates from Brazil

et al. 2013

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“…Another possibility is that these animals were exposed, mounted an immune response but were not persistently infected. Genetic heterogeneity of NWP SFV sequences at the primer locations [ 19 ] could also explain the false-negative PCR results. Maternal antibodies passed from mother to child may also explain such results and can persist for 6–12 months.…”

Section: Discussionmentioning

confidence: 99%

“…South and Central America are home to the parvorder Platyrrhini, also known as New World primates (NWP), which comprise three families, Cebidae, Atelidae, and Pitheciidae, consisting of at least 110 different species of neotropical primates [ 19 ]. In the 1970s and 1980s, the presence of SFV infecting NWP was first identified in cell cultures of saliva specimens from spider monkeys ( Ateles sp .…”

Section: Introductionmentioning

confidence: 99%

An expanded search for simian foamy viruses (SFV) in Brazilian New World primates identifies novel SFV lineages and host age-related infections

et al. 2015

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BackgroundWhile simian foamy viruses have co-evolved with their primate hosts for millennia, most scientific studies have focused on understanding infection in Old World primates with little knowledge available on the epidemiology and natural history of SFV infection in New World primates (NWPs). To better understand the geographic and species distribution and evolutionary history of SFV in NWPs we extend our previous studies in Brazil by screening 15 genera consisting of 29 NWP species (140 monkeys total), including five genera (Brachyteles, Cacajao, Callimico, Mico, and Pithecia) not previously analyzed. Monkey blood specimens were tested using a combination of both serology and PCR to more accurately estimate prevalence and investigate transmission patterns. Sequences were phylogenetically analyzed to infer SFV and host evolutionary histories.ResultsThe overall serologic and molecular prevalences were 42.8 and 33.6 %, respectively, with a combined assay prevalence of 55.8 %. Discordant serology and PCR results were observed for 28.5 % of the samples, indicating that both methods are currently necessary for estimating NWP SFV prevalence. SFV prevalence in sexually mature NWPs with a positive result in any of the WB or PCR assays was 51/107 (47.7 %) compared to 20/33 (61 %) for immature animals. Epidemiological analyses revealed an increase in SFV prevalence with age in captive Cebus monkeys. Phylogenetic analysis identified novel SFVs in Cacajao,Leontopithecus, and Chiropotes species that had 6–37 % nucleotide divergence to other NWP SFV. Comparison of host and SFV phylogenies showed an overall cospeciation evolutionary history with rare ancient and contemporaneous host-switching for Saimiri and Leontopithecus and Cebus xanthosternos, respectively.ConclusionsWe identified novel SFV in four neotropical monkey genera in Brazil and demonstrate that SFV prevalence increases with age in Cebus monkeys. Importantly, our test results suggest that both molecular and serological screening are currently required to accurately determine infection with NWP SFV. Our study significantly expands knowledge of the epidemiology and natural history of NWP SFVs. The tools and information provided in our study will facilitate further investigation of SFV in NWPs and the potential for zoonotic infection with these viruses.

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“…An alternative, noninvasive method was used for SFV detection by PCR in fecal samples of wild NHPs and in captive OWPs sharing the same enclosure [ 18 ]. However, this technique requires the development of species-specific microsatellite methods for individual identification, a difficult task given the greater diversity of NWPs with over 110 distinct species described to date [ 19 ]. Combined with reports of SFV replication in the oral mucosa [ 20 ] and saliva of infected humans and OWPs [ 16 , 21 – 23 ], we evaluated the use of noninvasively collected buccal swabs to detect and quantify NWP SFV compared with detection in matching blood specimens.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2017

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Simian foamy viruses (SFVs) co-evolved with a wide range of Old World and New World primates (OWPs and NWPs, respectively) and occasionally transmit to humans. Previous studies of OWPs showed that the predominant site of SFV replication is the oral mucosa. However, very little is known about SFV viral loads (VLs) in the oral mucosa or blood of NWPs. NWPs have smaller body sizes, limiting collection of sufficient whole blood volumes to molecularly detect and quantify SFV. Our study evaluated the use of noninvasively collected buccal swabs to detect NWP SFV compared with detection in blood using a new NWP SFV quantitative PCR (qPCR) assay. Buccal and blood samples were collected from 107 captive NWPs in Brazil comprising eleven distinct genera at the Primate Center of Rio de Janeiro (n = 58) and at Fundação Jardim Zoológico da Cidade do Rio Janeiro (n = 49). NWP SFV western blot (WB) testing was performed on a subset of animals for comparison with PCR results. The qPCR assay was validated using distinct SFV polymerase sequences from seven NWP genera (Callithrix, Sapajus, Saimiri, Ateles, Alouatta, Cacajao and Pithecia). Assay sensitivity was 20 copies/106 cells, detectable in 90% of replicates. SFV DNA VLs were higher in buccal swabs (5 log copies/106 cells) compared to peripheral blood mononuclear cells (PBMCs) (3 log copies/106 cells). The qPCR assay was also more sensitive than nested PCR for detection of NWP SFV infection and identified an additional 27 SFV-infected monkeys of which 18 (90%) were WB-positive and three that were WB-negative. We show the utility of using both blood and buccal swabs and our new qPCR assay for detection and quantification of diverse NWP SFV, which will assist a better understanding of the epidemiology of SFV in NWPs and any potential zoonotic infection risk for humans exposed to NWPs.

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Genetic Diversity of Neotropical Primates: Phylogeny, Population Genetics, and Animal Models for Infectious Diseases

Cited by 5 publications

References 183 publications

Identification and Characterization of Highly Divergent Simian Foamy Viruses in a Wide Range of New World Primates from Brazil

Identification and Characterization of Highly Divergent Simian Foamy Viruses in a Wide Range of New World Primates from Brazil

An expanded search for simian foamy viruses (SFV) in Brazilian New World primates identifies novel SFV lineages and host age-related infections

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

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