Bulinus snails in the Lake Victoria Basin in Kenya: Systematics and their role as hosts for schistosomes

Abstract

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.

Fig 1. Phylogenetic relationships among Kenyan bulinids based on partial cox1 sequences.

Phylogenetic relationships of bulinids from this study and from GenBank (with accession numbers) based on 621 bp of the cytochrome oxidase subunit 1 gene inferred from ML analysis under the GTR+G+I model. Bootstrap values over 95% are indicated by an asterisk. Bolded sequences were generated during this study and listed by MSB:Host: number. Additional information for specimens can be found in Table 1. Specimens recovered within the LVB by this study are color coded by species. B. africanus group species are in warm colors, B. forskalii group species in greens, and B. truncatus/tropicus group species in blues. Wave icons indicates species found within Lake Victoria. Cow icons indicate species with naturally occurring S. bovis infections. Human icons indicate species with naturally occurring S. haematobium infections.

Fig 2. Phylogenetic relationships of bulinids based on concatenated cox1 + 16S sequences.

Phylogenetic relationships of bulinids from this study and from GenBank based on 1163 bp of combined cox1 and 16S sequences inferred from ML analysis under the GTR+G+I model. Bootstrap values above 95 are indicated by an asterisk. Sequences generated during this study are listed by MSB:Host number. Additional information for specimens can be found in Table 1. Specimens recovered within the LVB by this study are color coded by species. B. africanus group species are in warm colors, B. forskalii group species in greens, and B. truncatus/tropicus group species in blues. Wave icons indicates species found within Lake Victoria. Cow icons indicate species with naturally occurring S. bovis infections. Human icons indicate species with naturally occurring S. haematobium infections.

Fig 3. Prevalence of natural infections among field collected bulinids.

Natural infection prevalence of 6 cercarial types shed from Bulinus snails collected between January 2014 and March 2021 from various localities in Kenya (S1 Table).

Fig 4. Phylogenetic relationships among Kenyan schistosomes based on concatenated cox1 + ITS sequences.

Phylogenetic relationships of schistosomes from this study and from GenBank based on 1166 bp of concatenated cox1 + partial ITS1 + 5.8S + partial ITS2 sequences inferred from ML analysis. Bootstrap values over 95% are indicated by an asterisk. Specimens are listed by MSB:Para: number followed by the host species. Bolded sequences were generated during this study and additional information for specimens can be found in Table 3.