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

ABSTRACT: BACKGROUND:The Lake Victoria basin is one of the most persistent hotspots of schistosomiasis in Africa, the intestinal form of the disease being studied more often than the urogenital form. Most schistosomiasis studies have been directed to Schistosoma mansoni and their corresponding intermediate snail hosts of the genus Biomphalaria, while neglecting S. haematobium and their intermediate snail hosts of the genus Bulinus. In the present study, we used DNA sequences from part of the cytochrome c oxidase subunit 1 (cox1) gene and the internal transcribed spacer 2 (ITS2) region to investigate Bulinus populations obtained from a longitudinal survey in Lake Victoria and neighbouring systems during 2010-2019. METHODS:Sequences were obtained to (i) determine specimen identities, diversity and phylogenetic positions, (ii) reconstruct phylogeographical affinities, and (iii) determine the population structure to discuss the results and their implications for the transmission and epidemiology of urogenital schistosomiasis in Lake Victoria. RESULTS:Phylogenies, species delimitation methods (SDMs) and statistical parsimony networks revealed the presence of two main groups of Bulinus species occurring in Lake Victoria; B. truncatus/B. tropicus complex with three species (B. truncatus, B. tropicus and Bulinus sp. 1), dominating the lake proper, and a B. africanus group, prevalent in banks and marshes. Although a total of 47 cox1 haplotypes, were detected within and outside Lake Victoria, there was limited haplotype sharing (only Haplotype 6 was shared between populations from Lake Victoria open waters and neighbouring aquatic systems) - an indication that haplotypes are specific to habitats. CONCLUSIONS:The Bulinus fauna of Lake Victoria consists of at least B. truncatus, B. tropicus, Bulinus sp. 1 (B. trigonus?) and B. ugandae. The occurrence and wide distribution of Bulinus species in Lake Victoria potentially implies the occurrence of urogenital schistosomiasis in communities living along the shores and on islands of the lake who depend solely on the lake for their livelihood. More in-depth studies are needed to obtain a better picture of the extent of the disease in the Lake Victoria basin.

SUBMITTER: Chibwana FD

PROVIDER: S-EPMC7427762 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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

Chibwana Fred D FD Tumwebaze Immaculate I Mahulu Anna A Sands Arthur F AF Albrecht Christian C

Parasites & vectors 20200814 1

<h4>Background</h4>The Lake Victoria basin is one of the most persistent hotspots of schistosomiasis in Africa, the intestinal form of the disease being studied more often than the urogenital form. Most schistosomiasis studies have been directed to Schistosoma mansoni and their corresponding intermediate snail hosts of the genus Biomphalaria, while neglecting S. haematobium and their intermediate snail hosts of the genus Bulinus. In the present study, we used DNA sequences from part of the cytoc ...[more]

PMID: 32795373

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Project description:The planorbid gastropod genus Bulinus consists of 38 species that vary in their ability to vector Schistosoma haematobium (the causative agent of human urogenital schistosomiasis), other Schistosoma species, and non-schistosome trematodes. Relying on sequence-based identifications of bulinids (partial cox1 and 16S) and Schistosoma (cox1 and ITS), we examined Bulinus species in the Lake Victoria Basin in Kenya for naturally acquired infections with Schistosoma species. We collected 6,133 bulinids from 11 sites between 2014-2021, 226 (3.7%) of which harbored Schistosoma infections. We found 4 Bulinus taxa from Lake Victoria (B. truncatus, B. tropicus, B. ugandae, and B. cf. transversalis), and an additional 4 from other habitats (B. globosus, B. productus, B. forskalii, and B. scalaris). S. haematobium infections were found in B. globosus and B. productus (with infections in the former predominating) whereas S. bovis infections were identified in B. globosus, B. productus, B. forskalii, and B. ugandae. No nuclear/mitochondrial discordance potentially indicative of S. haematobium/S. bovis hybridization was detected. We highlight the presence of Bulinus ugandae as a distinct lake-dwelling taxon closely related to B. globosus yet, unlike all other members of the B. africanus species group, is likely not a vector for S. haematobium, though it does exhibit susceptibility to S. bovis. Other lake-dwelling bulinids also lacked S. haematobium infections, supporting the possibility that they all lack compatibility with local S. haematobium, thereby preventing widespread transmission of urogenital schistosomiasis in the lake's waters. We support B. productus as a distinct species from B. nasutus, B. scalaris as distinct from B. forskalii, and add further evidence for a B. globosus species complex with three lineages represented in Kenya alone. This study serves as an essential prelude for investigating why these patterns in compatibility exist and whether the underlying biological mechanisms may be exploited for the purpose of limiting schistosome transmission.

Project description:BACKGROUND:Bulinus species are freshwater snails that transmit the parasitic trematode Schistosoma haematobium. Despite their importance, the diversity of these intermediate host snails and their evolutionary history is still unclear in Zimbabwe. Bulinus globosus and B. truncatus collected from a urogenital schistosomiasis endemic region in the Madziwa area of Zimbabwe were characterized using molecular methods. METHODS:Malacological survey sites were mapped and snails were collected from water contact sites in four communities in the Madziwa area, Shamva district for a period of one year, at three-month intervals. Schistosoma haematobium infections in snails were determined by cercarial shedding and the partial mitochondrial cytochrome c oxidase subunit 1 gene (cox1) was used to investigate the phylogeny and genetic variability of the Bulinus spp. collected. RESULTS:Among the 1570 Bulinus spp. snails collected, 30 (1.9%) B. globosus were shedding morphologically identified schistosomes. None of the B. truncatus snails were shedding. The mitochondrial cox1 data from 166 and 16 samples for B. globosus and B. truncatus, respectively, showed genetically diverse populations within the two species. Twelve cox1 haplotypes were found from the 166 B. globosus samples and three from the 16 B. truncatus samples with phylogenetic analysis showing that the haplotypes fall into well-supported clusters within their species groups. Both B. truncatus and B. globosus clustered into two distinct lineages. Overall, significant negative values for both Tajima's D statistic and the Fu's Fs statistic were observed for B. globosus and B. truncatus. CONCLUSIONS:The study provided new insights into the levels of genetic diversity within B. globosus and additional information on B. truncatus collected from a small geographical area in Zimbabwe. Low prevalence levels of infection observed in the snails may reflect the low transmission level of urogenital schistosomiasis in the area. Our results contribute towards the understanding of the distribution and population genetic structure of Bulinus spp. supporting the mapping of the transmission or risk of transmission of urogenital schistosomiasis, particularly in Zimbabwe.

Project description:PurposeAccurate identification of medically important intermediate host and vector species is crucial for understanding disease transmission and control. Identifying Bulinus snails which act as intermediate host species for the transmission of schistosomiasis is typically undertaken using conchological and genital morphology as well as molecular methods.MethodsHere, a landmark-based morphometric analysis of shell morphology was undertaken to determine its utility to distinguish the closely related and morphologically similar sister species Bulinus senegalensis and Bulinus forskalii. The method was developed to increase the accuracy of conchological morphology methods to identify Bulinus species in the field. Both species are found in West Africa, but only B. senegalensis is implicated in the transmission of urogenital schistosomiasis.ResultsWe found when scaled down to the same length, 3-whorl and 4-whorl (juvenile) B. senegalensis shells had a longer spire, narrower body whorl and shorter aperture than B. forskalii. In contrast, 5-whorl (adult) B. senegalensis had a shorter spire, but still had a shorter aperture and narrower body whorl than B. forskalii. Canonical Variate Analysis (CVA) showed minimal overlap between B. senegalensis and B. forskalii for 3-whorl and 4-whorl shells, with a clear separation for 5-whorl shells. Overall, B. senegalensis had a consistently shorter aperture size and narrower body whorl than B. forskalii for all development stages. Spire length was variable depending on the stage of development, with 3-whorl and 4-whorl shells having the opposite trends of adult shells.ConclusionsOur study demonstrates the applicability of landmark-based morphometrics in distinguishing the medically important, Bulinus senegalensis from its morphologically similar sister species, Bulinus forskalii. We recommend using measurements based on spire length, penultimate whorl length, body whorl width and aperture size to differentiate B. senegalensis and B. forskalii, when used with the appropriate information for each shell's development stage.

Dataset Information

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

Publications

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

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