Molecular identification of Bulinus spp. intermediate host snails of Schistosoma spp. in crater lakes of western Uganda with implications for the transmission of the Schistosoma haematobium group parasites

Abstract

BackgroundHuman schistosomiasis is the second most important tropical disease and occurs in two forms in Africa (intestinal and urogenital) caused by the digenetic trematodes Schistosoma mansoni and Schistosoma haematobium, respectively. A proposed recent shift of schistosomiasis above a previously established altitudinal threshold of 1400 m above sea level in western Ugandan crater lakes has triggered more research interest there.MethodsBased on extensive field sampling in western Uganda and beyond and employing an approach using sequences of the mitochondrial barcoding gene cytochrome c oxidase subunit 1 (cox1) this study aims were: (i) identification and establishment of the phylogenetic affinities of Bulinus species as potential hosts for Schistosoma spp.; (ii) determining diversity, frequency and distribution patterns of Bulinus spp.; and (iii) establishing genetic variability and phylogeographical patterns using Bayesian inference and parsimony network analyses.ResultsOut of the 58 crater lakes surveyed, three species of Bulinus snails were found in 34 crater lakes. Bulinus tropicus was dominating, Bulinus forskalii was found in two lakes and Bulinus truncatus in one. The latter two species are unconfirmed potential hosts for S. haematobium in this region. However, Bulinus tropicus is an important species for schistosomiasis transmission in ruminants. Bulinus tropicus comprised 31 haplotypes while both B. forskalii and B. truncatus exhibited only a single haplotype in the crater lakes. All species clustered with most of the haplotypes from surrounding lake systems forming source regions for the colonization of the crater lakes.ConclusionsThis first detailed malacological study of the crater lakes systems in western Uganda revealed presence of Bulinus species that are either not known or not regionally known to be hosts for S. haematobium, the causing agent of human urogenital schistosomiasis. Though this disease risk is almost negligible, the observed dominance of B. tropicus in the crater lakes shows that there is a likelihood of a high risk of infections with Schistosoma bovis. Thus, extra attention should be accorded to safeguard wild and domestic ruminants in this region as the population benefits from these animals.

Assessing the diversity and distribution of potential intermediate hosts snails for urogenital schistosomiasis: Bulinus spp. (Gastropoda: Planorbidae) of Lake Victoria

“…tropicus occupying the open waters, covering sand beaches, stones and submerged rocks, while B. africanus group dominates the banks, small islands and surrounding marshes. Although the number of species determined by PTP and GMYC was slightly indecisive, the present study supports previous findings [ 27 , 31 , 35 – 37 ] that molecular methods could delineate the monophyletic subclade comprising of B. truncatus and its sibling B. tropicus (Fig. 2 ), which are morphologically difficult to distinguish [ 17 ].…”

“…Our results, on the other hand, corroborate the previous observations that arrange of Bulinus species are present in the lake and are confirmed here to be widespread, but their role in S. haematobium transmission remains uncertain. A widely neglected aspect relates to schistosomiasis as a disease of veterinary concern [ 27 ]. Bulinus tropicus and B. ugandae are a well-known host for S. bovis , a parasite extensively infecting livestock [ 81 ].…”

“…S. haematobium ). However, identifying these potential Bulinus hosts is an initial step in estimating the extent and relevance of urogenital schistosomiasis in the given area [ 26 , 27 ].…”

First report of extraordinary corkscrew gastropods of the genus Bulinus in Lake Malawi

“…3A; A: B. truncatus/tropicus complex, posterior probability, PP 0.95) and three moderately to highly-supported species groups (see Fig. 3A, B: B. africanus group, PP 1.00; C: B. forskalii group, PP 0.90; and D: B. reticulatus group, PP 0.93), which is consistent with previous molecular phylogenetic studies on Bulinus (Jørgensen et al, 2007;Kane et al, 2008;Stothard et al, 2001;Tumwebaze et al, 2019). Accordingly, the B. africanus group forms a highly-supported (PP 0.99) sister to the B. forskalii group, which together are sister to the B. truncatus/tropicus complex (PP 0.95).…”

Mitochondrial genome of Bulinus truncatus (Gastropoda: Lymnaeoidea): Implications for snail systematics and schistosome epidemiology

“…Considerable work ( Stothard et al., 2002 ) has been done in this direction, with a particular focus on defining, assessing and/or using genetic markers in nuclear ribosomal and in mitochondrial (mt) DNAs for specific identification, particularly the second internal transcribed spacer (ITS-2) and cytochrome c oxidase subunit 1 gene ( cox 1), respectively ( Stothard et al., 2002 ; Jorgensen et al., 2013 ). Indeed, mt cox 1 sequences have shown major utility for the identification of species and groups, and to establish the genetic/systematic relationships of species/taxa within the genus Bulinus ( Tumwebaze et al., 2019 ; Chibwana et al., 2020 ), although, in some instances, there has been limited statistical support for some relationships ( Kane et al., 2008 ). The latter finding indicates that the use of a greater number of phylogenetically-informative genetic markers should enhance the taxonomic classification of Bulinus species or subspecies, and could improve the phylogenetic reconstruction of systematic relationships.…”