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 ( cox 1) 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 cox 1 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.
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.
BackgroundSnails such as Galba truncatula are hosts for trematode flukes causing fascioliasis, a zoonosis that is a major public health problem. Galba truncatula has recently been shown to be a cryptic species complex. African populations of Galba spp. are not yet studied using molecular assessments and is imperative to do so and reconstruct the centre of origin of Galba and to understand when and by what means it may have colonized the highlands of Africa and to what extent humans might have been involved in that process.MethodsSamples from all known sub-ranges throughout Africa and new samples from Europe and Asia were obtained. We used a combination of two mitochondrial (cox1 and 16S) and one nuclear (ITS2) markers and phylogenetic, divergence time estimates and phylogeographical methods to determine the identity and biogeographical affinities. We also reconstructed the colonization history including the likely mode of dispersal and tested for the presence of cryptic Galba species in Africa.ResultsGalba truncatula is restricted to the Palaearctic region of the continent, namely Morocco. All sub-Saharan populations proved to be a distinct species according to the phylogenetic analyses and genetic distance. We propose to use the existing name Galba mweruensis (Connolly, 1929) for this species which is morphologically indistinguishable from the other two species hitherto known to occur in northern Africa, i.e. G. truncatula and G. schirazensis. Sub-tropical Africa has been colonized only once in either the Pliocene and possibly Miocene. Diversification within G. mweruensis is dated to the Plio-Pleistocene and thus human-mediated dispersal can be ruled out for the initial colonization of the isolated mountain ranges. There are potentially even more cryptic species in high altitude areas of Africa as outlined by the distinctness of the population found at the top of Mt. Elgon, Uganda.ConclusionsFrom a novel genetic inspection of available African material, a hitherto neglected distinct species, G. mweruensis, now appears a major host of F. hepatica throughout sub-Saharan Africa. A closer examination of trematode parasites hosted by this species is needed in order to understand transmission patterns in highlands throughout eastern and southern Africa. We encourage future studies to inspect other high altitudes areas in Africa in light of parasites of either veterinary or medical importance.
Mountains are considered island-like systems often characterized by exceptional biodiversity and endemism. There are many highly isolated mountain ranges in Africa that collectively have been called the Afromontane archipelago. Freshwater snails of the genus Bulinus are composed of many veterinary and biomedical important species. These intermediate hosts for schistosomiasis parasites are wide spread and some of the species are considered to be highly adapted to very harsh environmental conditions such as droughts or low temperatures. However, the extent to which the Bulinus have adapted to live in high-altitudes and factors influencing these range shifts are not well investigated. In this study, we analyzed pan-African Bulinus species from various habitats across different altitudinal ranges, focusing on the high mountains or “sky islands” to examine how the contemporary climate and historical geological factors affect species distributions and evolutionary processes. Using a fossil-calibrated multigene phylogeny composed of two mitochondrial genes (cox1, 16S) and two nuclear genes (ITS2 and H3), we tested: 1) how often and when extreme altitudes were colonized, 2) what are the biogeographical affinities and degree of isolation of high-altitude species, 3) which lineages diversified and evolved endemism in the Afromontane environments, and 4) whether the Afromontane regions represent “sky islands”. Bayesian phylogenetic inference employing a fossil-calibrated molecular clock resulted in a strongly supported phylogeny resolving the relationships between the four Bulinus groups. High-altitude colonization exists exclusively within the Bulinus truncatus/tropicus complex. Several independent colonization events occurred in the Pliocene and Pleistocene throughout Africa, mostly from nearby regions of the respective mountain ranges. Most species evolved in low to mid-altitudinal ranges. Endemism is pronounced in the Ethiopian Highlands and those of Kenya and Lesotho. A previously unknown species was found at an extreme altitude (∼4,000 m a.s.l.) on Mt. Elgon/Uganda extending the formerly known altitudinal maximum of the genus by roughly 900 m. The endemic species has already diverged in the Pliocene (∼4 myr) and is currently characterized by low genetic diversity. There is further cryptic diversity in mountain ranges of Lesotho. Our findings are discussed in a biogeographical, conservation and biomedical context.
Schistosomiasis affects over 700 million people globally. 90% of the infected live in sub-Saharan Africa, where the trematode species Schistosoma mansoni and S. haematobium transmitted by intermediate hosts (IH) of the gastropod genera Biomphalaria and Bulinus are the major cause of the human disease burden. Understanding the factors influencing the distribution of the IH is vital towards the control of human schistosomiasis. We explored the applicability of a machine learning algorithm, random forest, to determine significant predictors of IH distribution and their variation across different geographic scales in crater lakes in western Uganda. We found distinct variation in the potential controls of IH snail distribution among the two snail genera as well as across different geographic scales. On the larger scale, geography, diversity of the associated mollusk fauna and climate are important predictors for the presence of Biomphalaria, whereas mollusk diversity, water chemistry and geography mainly control the occurrence of Bulinus. Mollusk diversity and geography are relevant for the presence of both genera combined. On the scale of an individual crater lake field, Biomphalaria is solely controlled by geography, while mollusk diversity is most relevant for the presence of Bulinus. Our study demonstrates the importance of combining a comprehensive set of predictor variables, a method that allows for variable selection and a differentiated assessment of different host genera and geographic scale to reveal relevant predictors of distribution. The results of our study contribute to making realistic predictions of IH snail distribution and schistosomiasis prevalence and can help in supporting strategies towards controlling the disease.
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