Genetic characterisation and phylogenetic status of whipworms (Trichuris spp.) from captive non-human primates in China, determined by nuclear and mitochondrial sequencing

Yue Xie,Bo Zhao,Guangyou Yang,Mei Li,Xiaobin Gu,Xuerong Peng,Eric P Hoberg,Xuan Zhou,Weimin Lai

doi:10.1186/s13071-018-3100-5

Yue Xie, Bo Zhao + Show 7 more

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https://doi.org/10.1186/s13071-018-3100-5

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Abstract

BackgroundWhipworms (Nematoda: Trichuridae), among the most common soil-transmitted helminths (STHs), can cause the socioeconomically important disease trichuriasis in various mammalian hosts including humans and non-human primates. For many years, Trichuris from non-human primates has been assigned to the same species as the one infecting humans Trichuris trichiura. More recently, several molecular reports challenged this assumption following recognition of a Trichuris species complex observed in humans and non-human primates. A refined concept for species limits within Trichuris contributes to an understanding of diversity and the potential (zoonotic) transmission among humans and non-human primates. In this study, we expanded previous investigations by exploring the diversity of Trichuris among eight primates including three Asian autochthonous species (i.e. Rhinopithecus roxellana, Rhinopithecus bieti and Nomascus leucogenys). Species-level identification, whether novel or assignable to known lineages of Trichuris, was based on analyses of nuclear internal transcribed spacers (ITS) and mitochondrial cytochrome c oxidase subunit 1 (cox1) genes.ResultsIn total, seven genetically distinct subgroups of whipworms were determined to be present among the primates sampled. Most Trichuris lineages, including Subgroups 1, 1’, 3, 5 and 6, showed a broad host range and were not restricted to particular primate species; in addition to T. trichiura, a complex of Trichuris species was shown infecting primates. Furthermore, it was assumed that Trichuris spp. from either N. leucogenys and P. hamadryas or R. roxellana and R. bieti, respectively, were conspecific. Each pair was indicated to be a discrete lineage of Trichuris, designated, respectively, as Subgroups 1 or 1’ and 2, based on integrated genetic and phylogenetic evidence.ConclusionThese results emphasise that the taxonomy and genetic variations of Trichuris are more complicated than previously acknowledged. These cumulative molecular and phylogenetic data provide a better understanding of the taxonomy, genetics and evolutionary biology of the whipworms.

Highlights

Whipworms (Nematoda: Trichuridae), among the most common soil-transmitted helminths (STHs), can cause the socioeconomically important disease trichuriasis in various mammalian hosts including humans and non-human primates
Sequence characterisation The final matrix of the internal transcribed spacers (ITS) region obtained from each specimen of Trichuris collected from R. roxellana, R. bieti, C. aethiops, M. mulatta, N. leucogenys, M. leonina, P. anubis and P. hamadryas, respectively, was determined to be approximately 1200 bp in length after manual assembly
Sequence analysis revealed that Trichuris from N. leucogenys and P. hamadryas shared the highest identity (100%), followed by 99.8% identity between Trichuris from R. roxellana and R. bieti and 95.5–97.2% identity between Trichuris from C. aethiops, M. leonina and P. anubis

Summary

Introduction

Whipworms (Nematoda: Trichuridae), among the most common soil-transmitted helminths (STHs), can cause the socioeconomically important disease trichuriasis in various mammalian hosts including humans and non-human primates. Whipworms (Nematoda: Trichuridae) are among the most common soil-transmitted helminths (STHs) and cause trichuriasis in various mammalian hosts with important socioeconomic impact [1]. About 80 valid species are identified in the genus Trichuris, with most considered specific to particular taxonomic groups of hosts [8] Among them, both species of Trichuris, namely Trichuris trichiura (Linnaeus, 1771) and Trichuris suis Schrank, 1788, are regarded as zoonotic parasites and pose threats to public health [9]. Non-human primates, the closest human relatives, can endure high whipworm infections that are typically assumed to be T. trichiura according to morphological criteria [14,15,16,17,18]. This assumption appears reasonable because T. trichiura has previously been found in such primates as macaques (Macaca mulatta Zimmerman, 1780), crab-eating macaques (Macaca fascicularis Raffles, 1821) and other Old and New World monkeys [19,20,21,22]

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