Molecular characterization of nodule worm in a community of Bornean primates

Abstract

Strongyles are commonly reported parasites in studies of primate parasite biodiversity. Among them, nodule worm species are often overlooked as a serious concern despite having been observed to cause serious disease in nonhuman primates and humans. In this study, we investigated whether strongyles found in Bornean primates are the nodule worm Oesophagostomum spp., and to what extent these parasites are shared among members of the community. To test this, we propose two hypotheses that use the parasite genetic structure to infer transmission processes within the community. In the first scenario, the absence of parasite genetic substructuring would reflect high levels of parasite transmission among primate hosts, as primates’ home ranges overlap in the study area. In the second scenario, the presence of parasite substructuring would suggest cryptic diversity within the parasite genus and the existence of phylogenetic barriers to cross‐species transmission. By using molecular markers, we identify strongyles infecting this primate community as O. aculeatum , the only species of nodule worm currently known to infect Asian nonhuman primates. Furthermore, the little to no genetic substructuring supports a scenario with no phylogenetic barriers to transmission and where host movements across the landscape would enable gene flow between host populations. This work shows that the parasite's high adaptability could act as a buffer against local parasite extinctions. Surveys targeting human populations living in close proximity to nonhuman primates could help clarify whether this species of nodule worm presents the zoonotic potential found in the other two species infecting African nonhuman primates.

Genetic characterization of nodular worm infections in Asian Apes

“…However, in our study we used ITS sequences to discriminate nematode species as the ITS regions are among the most variable nuclear loci, with a sufficient number of comparative sequences in databases. Our result demonstrated the same phylogenetic similarity observed from Frias et al 38 . Accordingly, the rapid mode of ITS evolution including frequent indels makes alignment of ITS haplotypes more challenging compared to protein-coding markers, which can adversely affect the reliability of phylogenetic reconstruction 42 .…”

“…Mitochondrial and nuclear genes are used in phylogenetic studies on strongylid species 41 . Based on the mitochondrial cox1 gene, Frias et al 38 showed that Bornean primates are subject to O. aculeatum infection. However, in our study we used ITS sequences to discriminate nematode species as the ITS regions are among the most variable nuclear loci, with a sufficient number of comparative sequences in databases.…”

“…Interestingly, we did not detect any other nodular worm infections in our dataset, as it is known that the primer set used in our study are able to detect other Oesophagostomum species 46 , suggesting that O. aculeatum is the only or at least the predominant Oesophagostomum species that parasitizes orangutans and gibbons in our study area. Recently, Frias et al 38 showed that O. aculeatum is widely distributed in Borneo and that it infected all studied members of host species, such as long‐tailed macaques, silvered langurs, proboscis monkeys and Bornean orangutans, with little clear genetic differentiation among them.…”

“…Arizono et al 37 molecularly identified O. aculeatum infections for the first time in Japanese macaques. Recently, molecular markers showed a widespread distribution of O. aculeatum in the Bornean primate community, including orangutans 38 , although there is a paucity of investigations in gibbons. Currently, there is no study done on O. aculeatum distribution in the Sumatran NHPs community.…”

Potentially zoonotic gastrointestinal nematodes co-infecting free ranging non-human primates in Kenyan urban centres

“…Of concern are soil-transmitted helminths (STHs) whose partial development outside their hosts allows persistence of infective stages in the environment, enabling transmission between closely related host species Cibot et al, 2015). Several studies have described cases of zoonotic STHs transmission in sympatric populations of NHPs and humans (Cibot et al, 2015;Frias et al, 2019). However, little is known about urban zoonoses and possible reservoir hosts despite having abundant wildlife in most urban habitats in Africa.…”