Lurking in the dark: Cryptic Strongyloides in a Bornean slow loris

Abstract

Within host communities, related species are more likely to share common parasitic agents, and as a result, morphological similarities have led researchers to conclude that parasites infecting closely related hosts within a community represent a single species. However, genetic diversity within parasite genera and host range remain poorly investigated in most systems. Strongyloides is a genus of soil-transmitted nematode that has been reported from several primate species in Africa and Asia, and has been estimated to infect hundreds of millions of people worldwide, although no precise estimates are available. Here we describe a case of infection with a cryptic species of Strongyloides in a Bornean (Philippine) slow loris (Nycticebus menagensis) living within a diverse community of several primate species in the Lower Kinabatangan Wildlife Sanctuary, Malaysian Borneo. Fresh fecal samples were collected from five primate species and nematode larvae cultured from these samples were selected for phylogenetic analyses. Sequences obtained for most larvae were identified as S. fuelleborni, grouping into three different clusters and showing no aggregation within specific hosts or geographic location. In contrast, a set of parasite sequences obtained from a slow loris clustered closely with S. stercoralis into a different group, being genetically distinct to sequences reported from other primate hosts, humans included. Our results suggest that although S. fuelleborni infects all haplorrhines sampled in this primate community, a different species might be infecting the slow loris, the only strepsirrhine in Borneo and one of the least studied primates in the region. Although more data are needed to support this conclusion, we propose that Strongyloides species in primates might be more diverse than previously thought, with potential implications for ecological and evolutionary host-parasite associations, as well as epidemiological dynamics.

Molecular characterization of nodule worm in a community of Bornean primates

“…In conclusion, our results show a widespread distribution of O. aculeatum in this primate community, in agreement with previous observations of a different soil‐transmitted helminth ( Strongyloides spp.) infecting the same community (Frias et al, ), further suggesting that extensive habitat overlap in primates may be contributing to the little parasite genetic substructuring observed. Continuous parasite gene flow between host species suggests a high transmission potential enabled by host movement (Blouin, Yowell, Courtney, & Dame, ).…”

“…As many samples were not collected after observing defecation, and most primate species have overlapping ranges in the area, we conducted host species identification for all samples used in coprocultures by extracting whole DNA from each collected fecal sample and amplifying a small fragment of the cytochrome b ( cytb ) gene, following the protocol described in Frias et al (). Then, 64 strongylid larvae were individually selected at random for DNA extraction (Table ) using a QIAamp DNA micro kit (Qiagen, Japan).…”

Advances in the Molecular and Cellular Biology of Strongyloides spp.

“…Distinct haplotypes of S. fuelleborni from humans and long-tailed macaques in Thailand and Laos were also described and phylogenetically characterized using partial cox1 sequences [5]. Three distinct clades of S. fuelleborni and other cryptic Strongyloides spp., which were close to S. stercoralis isolated from primates, were also discovered in Malaysia using partial cox1 sequence genotyping [3].…”

“…S. fuelleborni infections have also been widely reported in humans and several nonhuman primates such as chimpanzees, gorillas, macaques, and baboons [3][4][5]12]. However, due to the absence of autoinfection in S. fuelleborni infections, the disease associated with them in humans is not as severe as in S. stercoralis infections [46].…”

“…Strongyloidiasis, caused mainly by Strongyloides stercoralis, is one of the most neglected soil-borne tropical diseases. Human infections with Strongyloides fuelleborni and S. fuelleborni kellyi have also been reported in Asia, Papua New Guinea, and some African locales [1][2][3][4][5]. Globally, S. stercoralis is reported to infect more than 370 million people mainly in tropical and subtropical regions [6].…”