Genetic diversity of primate strongylid nematodes: Do sympatric nonhuman primates and humans share their strongylid worms?

Abstract

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.

Soil-transmitted helminth infections in free-ranging non-human primates from Cameroon and Gabon

“…in chimpanzees. In this aspect, our results corroborate those of other epidemiological investigations in wild NHP [ 6 , 27 , 28 , 30 , 56 ]. However, sex differences in parasitic infection are commonly observed in many animals [ 32 ] although infection rates can fluctuate according to seasons.…”

“…Our findings confirm that O. stephanostomum is the predominant species in great apes [ 6 , 7 , 15 , 55 , 75 ]. This species seems to be specific to NHP, as previous studies in Gabon, Democratic Republic of the Congo and CAR failed to find zoonotic infections with O. stephanostomum in humans living in sympatry with infected chimpanzee or gorilla populations [ 10 , 27 , 51 ]. However, some zoonotic transmission may be possible, as shown by a study from Uganda [ 7 ].…”

“…Our results show that the prevalence of Oesophagostomum and Necator was relatively high in gorillas and chimpanzees; in contrast, Trichuris infection was low and Ascaris was absent. Previous studies of free-ranging gorillas from Dzanga Sangha Protected Areas, CAR and the Moukalaba-Doudou NP, Gabon, reported a similar prevalence of Necator and Oesophagostomum [ 27 , 51 ]. Trichuris and Ascaris have also been detected in gorillas in Gabon and Rwanda, but at very low prevalence [ 51 , 52 ].…”

“…Past studies have shown that O. bifurcum is rarely found in great apes, but it is common in other NHP species [ 55 ]. A study conducted in the CAR reported a high prevalence of this strongylid in mangabeys but a low relative abundance in gorillas and chimpanzees [ 27 ]. Mixed infections with O. stephanostomum and O. bifurcum have been reported in chimpanzees in Bulindi NP and Kibale NP [ 6 , 7 , 55 ].…”

“…Gorillas, chimpanzees and several Old World monkey species have been reported to be hosts of Nectar americanus based on phenetic characteristics or molecular evidence [ 25 ]. Three other Necator species ( N. congolensis , N. gorillae and N. exilidens ) have also been described in African great apes, and N. gorillae has been reported to infect humans [ 17 , 26 , 27 ]. Finally, eight species of Oesophagostomum have been recorded in free-ranging NHP from the subfamilies Cercopithecinae and Colobinae , and in chimpanzees ( Pan troglodytes ) [ 15 , 28 – 30 ], with three of these ( O. bifurcum, O. oesophagostomum, O. aculeatum ) infecting humans.…”