The close phylogenetic relationship between humans and nonhuman primates (NHPs) can result in a high potential for pathogen exchange. In recent decades, NHP and human interactions have become more frequent due to increasing habitat encroachment and ecotourism. Strongylid communities, which include members of several genera, are typically found in NHPs. Using optimized high-throughput sequencing for strain-level identification of primate strongylids, we studied the structure of strongylid communities in NHPs and humans co-habiting a tropical forest ecosystem in the Central African Republic. General taxonomic assignment of 85 ITS-2 haplotypes indicated that the studied primates harbour at least nine genera of strongylid nematodes, with Oesophagostomum and Necator being the most prevalent. We detected both host-specific and shared strongylid haplotypes. Skin-penetrating Necator gorillaehaplotypes were shared between humans and gorillas but Necator americanus were much more restricted to humans. Strongylid communities of local hunter-gatherers employed as trackers were more similar to those of gorillas compared to their relatives, who spent more time in villages. This was due to lower abundance of human-origin N. americanus in both gorillas and trackers. Habituated gorillas or those under habituation did not show larger overlap of strongylids with humans compared to unhabituated. We concluded that the occurrence of the human-specific strongylids in gorillas does not increase with direct contact between gorillas and humans due to the habituation. Overall, our results indicate that the degree of habitat sharing between hosts, together with mode of parasite transmission, are important factors for parasite spillover among primates.
- MeSH
- Ecosystem MeSH
- Phylogeny MeSH
- Genetic Variation genetics MeSH
- Gorilla gorilla genetics MeSH
- Humans MeSH
- Necator genetics MeSH
- Oesophagostomum genetics MeSH
- Primates genetics MeSH
- Sympatry genetics MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND: Hookworms are important pathogens of humans. To date, Necator americanus is the sole, known species of the genus Necator infecting humans. In contrast, several Necator species have been described in African great apes and other primates. It has not yet been determined whether primate-originating Necator species are also parasitic in humans. METHODOLOGY/PRINCIPAL FINDINGS: The infective larvae of Necator spp. were developed using modified Harada-Mori filter-paper cultures from faeces of humans and great apes inhabiting Dzanga-Sangha Protected Areas, Central African Republic. The first and second internal transcribed spacers (ITS-1 and ITS-2) of nuclear ribosomal DNA and partial cytochrome c oxidase subunit 1 (cox1) gene of mtDNA obtained from the hookworm larvae were sequenced and compared. Three sequence types (I-III) were recognized in the ITS region, and 34 cox1 haplotypes represented three phylogenetic groups (A-C). The combinations determined were I-A, II-B, II-C, III-B and III-C. Combination I-A, corresponding to N. americanus, was demonstrated in humans and western lowland gorillas; II-B and II-C were observed in humans, western lowland gorillas and chimpanzees; III-B and III-C were found only in humans. Pairwise nucleotide difference in the cox1 haplotypes between the groups was more than 8%, while the difference within each group was less than 2.1%. CONCLUSIONS/SIGNIFICANCE: The distinctness of ITS sequence variants and high number of pairwise nucleotide differences among cox1 variants indicate the possible presence of several species of Necator in both humans and great apes. We conclude that Necator hookworms are shared by humans and great apes co-habiting the same tropical forest ecosystems.
- MeSH
- Ecosystem * MeSH
- Phylogeny MeSH
- Genotype MeSH
- Humans MeSH
- DNA, Ribosomal Spacer chemistry genetics MeSH
- Molecular Epidemiology MeSH
- Molecular Sequence Data MeSH
- Necator classification genetics isolation & purification MeSH
- Necatoriasis epidemiology parasitology veterinary MeSH
- Primate Diseases epidemiology parasitology MeSH
- Pan troglodytes MeSH
- Primates MeSH
- Electron Transport Complex IV genetics MeSH
- Sequence Analysis, DNA MeSH
- Sequence Homology MeSH
- Cluster Analysis MeSH
- Trees * MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Central African Republic MeSH