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Assessing the Diversity and Distribution of Potential Intermediate Hosts Snails for Urogenital Schistosomiasis: Bulinus Spp

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Assessing the Diversity and Distribution of Potential Intermediate Hosts Snails for Urogenital Schistosomiasis: Bulinus Spp Chibwana et al. Parasites Vectors (2020) 13:418 https://doi.org/10.1186/s13071-020-04281-1 Parasites & Vectors RESEARCH Open Access Assessing the diversity and distribution of potential intermediate hosts snails for urogenital schistosomiasis: Bulinus spp. (Gastropoda: Planorbidae) of Lake Victoria Fred D. Chibwana1,2*, Immaculate Tumwebaze1, Anna Mahulu1, Arthur F. Sands1 and Christian Albrecht1 Abstract Background: The Lake Victoria basin is one of the most persistent hotspots of schistosomiasis in Africa, the intesti- nal 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 afnities, 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 neigh- bouring aquatic systems) – an indication that haplotypes are specifc 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 occur- rence 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. Keywords: African lakes, Epidemiology, Phylogeography, Neglected tropical diseases, Schistosoma haematobium *Correspondence: [email protected]; [email protected] 1 Department of Animal Ecology and Systematics, Justus Liebig University Giessen, Giessen, Germany Full list of author information is available at the end of the article © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Chibwana et al. Parasites Vectors (2020) 13:418 Page 2 of 18 Background Te current water body arose about 14,600 years ago [15, Schistosomiasis is a parasitic disease caused by digenean 16], which is relatively shorter for snail species radiation trematodes of the genus Schistosoma and is a socio-nota- [10, 17]. Nevertheless, Brown et al. [17] listed 28 gastro- ble disease in tropical and subtropical regions. It is preva- pod species in Lake Victoria, of which six are medically lent in more than 78 countries and territories infecting signifcant species within genera Bulinus (4 species) and more than 250 million people worldwide, most of whom Biomphalaria (2 species). Lake Victoria, which is shared inhabit sub-Saharan Africa [1, 2]. Although more than between Tanzania, Uganda and Kenya, therefore plays 20 Schistosoma species are recognised, only Schistosoma a signifcant role in the persistence of schistosomiasis in mansoni and S. haematobium are ubiquitously known in these surrounding countries [18–20]. Despite the increas- sub-Saharan Africa due to their capability to cause intes- ing eforts to control schistosomiasis with praziquantel tinal and urogenital schistosomiasis, respectively [1, 3, 4]. through mass drug administration (MDA) programmes, Te highest infections and disease burdens are frequently East African countries are still among the hotspots for found in school-aged children, particularly in settings this parasitic disease. Herein, the majority of schistoso- with poor hygiene and sanitary facilities [5]. Human hosts miasis cases are reported from fshing communities and infected with these Schistosoma species experience acute particularly in school-aged children surrounding Lake hyperaemia, abnormal growth, internal haemorrhag- Victoria [21–24]. Te vast majority of studies focusing on ing, fbrosis and tissue thickening [6]. As a result, infec- Schistosoma and their intermediate hosts in Lake Victoria tion with S. mansoni culminates with liver fbrosis, portal and neighbouring aquatic systems have mainly focused hypertension and ascites, while bladder cancer is the fnal on S. mansoni and Biomphalaria spp. [13, 18, 25] while stage of a S. haematobium infection [7]. Furthermore, overlooking Bulinus spp. and their potential role in the genital schistosomiasis complications associated with urogenital schistosomiasis transmission (i.e. S. haemato- S. haematobium infections include hypertrophic and bium). However, identifying these potential Bulinus hosts ulcerative lesions of the female genital tract [8]. Schisto- is an initial step in estimating the extent and relevance of soma species, like other digenean trematodes, utilise pul- urogenital schistosomiasis in the given area [26, 27]. monate snails to complete their two-host life-cycles; i.e. Te genus Bulinus consists of 37 species occurring Biomphalaria spp. for S. mansoni and Bulinus spp. for S. mainly in Africa, the Middle East and in the Mediterra- haematobium [1, 3, 4]. nean Area [17]. Te recognized Bulinus species fall into Te Lake Victoria ecoregion of the East African Rift four groups, namely the Bulinus africanus, B. reticulatus, System, is characterized by a wealth of extraordinary and B. forskalii species groups, and the B. truncatus/B. freshwater biodiversity that has accumulated through- tropicus species complex. Many species within these out the Quaternary, including almost 700 species of groups except, for example, B. tropicus and B. ugandae cichlid fshes [9, 10]. Major geological and climatological are involved in the transmission of S. haematobium [28, changes occurred in this region during this period. Tese 29]. Moreover, B. africanus group species play an impor- changes are linked to the development of the East Afri- tant role in the transmission of S. haematobium and S. can Rift. More recently, anthropogenic pressures in the bovis in Central East Africa [17]. However, precise spe- Lake Victoria ecoregion have grown exponentially due cies identifcation of snails of the genus Bulinus is often to multifactorial stressors such as habitat degradation, difcult because of strong morphological similarities and pollution, exploitation, the introduction of invasive spe- overlap among species, the coexistence of diferent forms cies, ecosystem modifcations and climate change [11, and groups in a narrow area and the lack of well-defned 12]. Insights into the consequences of recent and historic criteria by which to distinguish species [17, 29]. Addi- environmental changes in the region are crucial to under- tionally, some studies have also reported the existence of standing the diversifcation dynamics of freshwater biota. cryptic species in some localities [30, 31], which further Efects of ecosystem changes on the community com- exacerbates the taxonomic uncertainties within genus position and demography of benthic organisms remain Bulinus. poorly assessed since few studies have been conducted Te knowledge of the number of Bulinus species apart from cichlid fshes and the schistosome intermedi- occurring within or nearby Lake Victoria is obscure. For ate host snail genus Biomphalaria [13]. instance, Mandahl-Barth [29] recognised B. trigonus and Lake Victoria is endowed with a remarkable mollusc B. transversalis as independent species, but Brown [17] fauna, although it is less diverse than in lakes Malawi viewed them as lacustrine morphs of B. tropicus and B. and Tanganyika, perhaps due to its younger age and rela- truncatus or synonyms of unnamed Bulinus species tive shallowness
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