The Schistosoma indicum species group in Nepal: presence of a new lineage of schistosome and use of the Indoplanorbis exustus species complex of snail hosts

Abstract

From 2007–2014, 19,360 freshwater snails from the Terai and hilly regions of Nepal were screened for cercariae of mammalian schistosomes. Based on analysis of mitochondrial cytochrome oxidase I (cox1), 12S, 16S and 28S sequences (3,675 bp) of the cercariae recovered, we provide, to our knowledge, the first report of the Schistosoma indicum species group in Nepal. Five samples of Schistosoma nasale, nine of Schistosoma spindale and 17 of Schistosoma sp. were recovered, all from the snail Indoplanorbis exustus. The last-mentioned lineage failed to group in any of our analyses with S. nasale, S. spindale or S. indicum. It diverged in cox1 sequence from them by 16%, 13% and 13%, respectively, levels of difference comparable to well-studied species pairs of Schistosoma. Analysis of cox1, 16S and internal transcribed spacer 1 (ITS1) sequences (1,874 bp) for Nepalese specimens of I. exustus was also surprising in revealing the presence of four genetically distinct clades. They diverged from one another at levels comparable to those noted for species pairs in the sister genus Bulinus. There was no obvious pattern of use by Nepalese Schistosoma of the Indoplanorbis clades. We found high support for a close relationship between S. indicum and Schistosoma haematobium groups, but failed to retrieve support for a clean separation of the two, with a tendency for S. nasale to fall as the most basal representative. If this pattern holds, hypotheses for the origin of the Asian Indoplanorbis-transmitted S. indicum group from the Bulinus-transmitted S. haematobium group may require modification, including consideration of more contemporaneous origins of the two groups. The Indian subcontinent is under-studied with respect to schistosome diversity and our current knowledge of the S. indicum and I. exustus species groups is inadequate. Further study is warranted given the ability of indicum group species to cause veterinary problems and cercarial dermatitis, with a worrisome potential in the future to establish infections in humans.

The phylogeny of the genus Indoplanorbis (Gastropoda, Planorbidae) from Africa and the French West Indies

“…According to the Cox1 and 16S data, the first three clades (A–C) consist mainly of samples originating from continental Asia (India, Nepal, Bangladesh), with the exception of samples from Laos and Myanmar. Similarly to the analysis of strains from Nepal (Devkota et al., ), our results suggest that the genetic diversity of I. exustus is very high for India, Bangladesh, Laos and Myanmar.…”

“…Phylogenetic trees, based on two mitochondrial genes (Cox1 and 16S), showed congruent results with four main clades such as observed by Devkota et al. (). According to the Cox1 and 16S data, the first three clades (A–C) consist mainly of samples originating from continental Asia (India, Nepal, Bangladesh), with the exception of samples from Laos and Myanmar.…”

“…The geographical expansion is probably facilitated by the high self‐fertilisation capacity of I. exustus (Bony et al., and Escobar et al., ) and may have important parasitological implications as it is the natural intermediate host of four species of schistosomes belonging to the genus Schistosoma ( S. indicum , S. nasale, S. spindale and Schistosoma sp.) and at least one avian schistosome (Devkota, Brant, Thapa, & Loker, ; Devkota et al., ). Indeed, when the vector of a parasitosis is present in a geographical area, nothing excludes the emergence of the disease if the parasite is introduced.…”

“…Three main phylogenetic studies have been conducted on I. exustus using various samples from Asia (Sri Lanka, India, Nepal, Bangladesh), South‐East Asia (Indonesia, Philippines, Vietnam, Laos, Malaysia, Thailand, Myanmar) and from the Middle East (Oman). These analyses were computed using different genes, including mtDNA Cox1 and mtDNA 16S (Devkota, Brant, & Loker, ; Gauffre‐Autelin, von Rintelen, Stelbrink, & Albrecht, ; Liu et al., ). All studies showed the presence of four genetically distinct clades with a strong phylogenetic divergence between them, suggesting that I. exustus is a complex of several species.…”

The diverse echinostomes from East Africa: With a focus on species that use Biomphalaria and Bulinus as intermediate hosts

“…For some of the samples, only the cercariae (after shedding of snails) were saved, but its snail host was not preserved. Cercariae can often have adherent snail tissue on them that can be amplified with snail specific primers ( Devkota et al, 2015 ). Therefore, for the cercariae where we did not have the snail host, we used snail cox1 primers to generate amplicons from those cercariae, particularly those shed from Bulinus .…”