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, 12S, 16S and 28S sequences (3,675bp) 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 sequences (1,874bp) 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.

Keywords: Host switch; Host–parasite relationships; Indoplanorbis exustus; Nepal; Schistosoma indicum group; Schistosomes; Schistosomiasis.