Hidden Population Structure and Cross-species Transmission of Whipworms (Trichuris sp.) in Humans and Non-human Primates in Uganda.

Background: Whipworms (Trichuris sp.) are a globally distributed genus of parasitic helminths that infect a diversity of mammalian hosts. Molecular methods have successfully resolved porcine whipworm, Trichuris suis, from primate whipworm, T. trichiura. However, it remains unclear whether T. trichiura is a multi-host parasite capable of infecting a wide taxonomic breadth of primate hosts or a complex of host specific parasites that infect one or two closely related hosts. Methods and Findings: We examined the phylogenetic structure of whipworms in a multi-species community of non-human primates and humans in Western Uganda, using both traditional microscopy and molecular methods. A newly developed nested polymerase chain reaction (PCR) method applied to non-invasively collected fecal samples detected Trichuris with 100% sensitivity and 97% specificity relative to microscopy. Infection rates varied significantly among host species, from 13.3% in chimpanzees (Pan troglodytes) to 88.9% in olive baboons (Papio anubis). Phylogenetic analyses based on nucleotide sequences of the Trichuris internal transcribed spacer regions 1 and 2 of ribosomal DNA revealed three co-circulating Trichuris groups. Notably, one group was detected only in humans, while another infected all screened host species, indicating that whipworms from this group are transmitted among wild primates and humans. Conclusions and Significance: Our results suggest that the host range of Trichuris varies by taxonomic group, with some groups showing host specificity, and others showing host generality. In particular, one Trichuris taxon should be considered a multi-host pathogen that is capable of infecting wild primates and humans. This challenges past assumptions about the host specificity of this and similar helminth parasites and raises concerns about animal and human health. Author Summary: Whipworms are a group of gastrointestinal worms that are both common and globally distributed. These parasites are known to stunt development, especially in school-aged children, and therefore hinder economic, social, and intellectual growth. Unfortunately, research on whipworms has lagged behind its effects, at least in part because this parasite infects the world's poorest populations. Currently, a single species of whipworm is assumed capable of infecting both humans and non-human primates. In this study, we tested this assumption by collecting fecal samples from humans and overlapping non-human primate populations containing monkeys and chimpanzees in Western Uganda. Using molecular analyses, we examined patterns of genetic similarity between human and nonhuman primate whipworms. We identified three genetically distinct groups of whipworms that could not be distinguished by microscopic examination of their eggs. One of these groups was found in all nine species of primates examined, including humans. These findings suggest that some varieties of whipworms are indeed transmissible between humans and non-human primates, which raises concerns for both human health and conservation. [ABSTRACT FROM AUTHOR]