{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,8]],"date-time":"2025-10-08T10:40:45Z","timestamp":1759920045069,"version":"build-2065373602"},"reference-count":34,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2025,1,10]],"date-time":"2025-01-10T00:00:00Z","timestamp":1736467200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Research Council of Thailand (NRCT): High-Potential Research Team Grant Program","award":["N42A670561"],"award-info":[{"award-number":["N42A670561"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>Urinary schistosomiasis is caused by the blood fluke Schistosoma haematobium, which is predominantly found in Africa. The freshwater snail Bulinus globosus is its main intermediate host. The species that make up the B. globosus group are genetically complex, and their taxonomic status remains controversial. Genetic variation, heterozygosity, and DNA recombination in B. globosus were examined using the mitochondrial cytochrome c oxidase subunit 1 (COI) and the intron 3 region of the arginine kinase gene (AkInt3). A total of 81 B. globosus snails were collected from three different localities in Kwale County, Kenya. Genomic diversity, heterozygosity, DNA recombination, and haplotype network were calculated using AkInt3 sequences. Low polymorphism in the COI sequence divided B. globosus into six haplotypes (C1\u2013C6). However, AkInt3 sequencing studies showed high polymorphisms, classifying 81 B. globosus snails into 44 haplotypes (H1\u2013H44). These haplotypes were separated into three haplogroups (I\u2013III). AkInt3 sequence heterozygosity was also found. DNA recombination haplotypes between haplogroups were commonly found in heterozygous samples. AkInt3 sequence studies showed high levels of genetic polymorphism and heterozygosity, supporting its use as a genetic marker for elucidating the population genetics of B. globosus. Furthermore, our study showed that B. globosus populations in Kenya form a \u201cspecies complex\u201d.<\/jats:p>","DOI":"10.3390\/biology14010053","type":"journal-article","created":{"date-parts":[[2025,1,10]],"date-time":"2025-01-10T10:06:38Z","timestamp":1736503598000},"page":"53","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Nuclear Intron Sequence Variation of the Bulinus globosus Complex (Mollusca: Planorbidae): Implications for Molecular Systematic Analyses"],"prefix":"10.3390","volume":"14","author":[{"given":"Chairat","family":"Tantrawatpan","sequence":"first","affiliation":[{"name":"Division of Cell Biology, Department of Preclinical Sciences, Faculty of Medicine, and Center of Excellence in Stem Cell Research and Innovation, Thammasat University, Rangsit Campus, Pathum Thani 12120, Thailand"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kotchaphon","family":"Vaisusuk","sequence":"additional","affiliation":[{"name":"Department of Veterinary Technology, Faculty of Agricultural Technology, Rajabhat Maha Sarakham University, Maha Sarakham 44000, Thailand"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5788-7920","authenticated-orcid":false,"given":"Chrysantus M.","family":"Tanga","sequence":"additional","affiliation":[{"name":"Plant Health Theme, International Centre of Insect Physiology and Ecology, Nairobi 00100, Kenya"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Warayutt","family":"Pilap","sequence":"additional","affiliation":[{"name":"Walai Rukhavej Botanical Research Institute, Mahasarakham University, Maha Sarakham 44150, Thailand"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Naruemon","family":"Bunchom","sequence":"additional","affiliation":[{"name":"Department of Tropical Medicine and Malaria, Research Institute, National Center for Global Health and Medicine, 1-21-1 Toyama, Shinjuku-Ku, Tokyo 162-8655, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9053-7631","authenticated-orcid":false,"given":"Ross H.","family":"Andrews","sequence":"additional","affiliation":[{"name":"Department of Surgery & Cancer, Faculty of Medicine, Imperial College London, South Kensington Campus, London SW7 2AZ, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tongjit","family":"Thanchomnang","sequence":"additional","affiliation":[{"name":"Biomedical Science Research Unit, Faculty of Medicine, Mahasarakham University, Maha Sarakham 44000, Thailand"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6726-3759","authenticated-orcid":false,"given":"Wanchai","family":"Maleewong","sequence":"additional","affiliation":[{"name":"Department of Parasitology, Faculty of Medicine, and Mekong Health Science Research Institute, Khon Kaen University, Khon Kaen 40002, Thailand"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4789-297X","authenticated-orcid":false,"given":"Weerachai","family":"Saijuntha","sequence":"additional","affiliation":[{"name":"Biomedical Science Research Unit, Faculty of Medicine, Mahasarakham University, Maha Sarakham 44000, Thailand"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,1,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Brown, D.S. (1994). Freshwater Snails of Africa and Their Medical Importance, Taylor and Francis Ltd.","DOI":"10.1201\/9781482295184"},{"key":"ref_2","unstructured":"World Health Organization (2021, March 18). Schistosomiasis (Health Topics). Available online: https:\/\/www.who.int\/news-room\/fact-sheets\/detail\/schistosomiasis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1186\/1756-3305-1-15","article-title":"Molecular characterization of freshwater snails in the genus Bulinus: A role for barcodes?","volume":"1","author":"Kane","year":"2008","journal-title":"Parasit. Vectors"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Zein-Eddine, R., Djuikwo-Teukeng, F.F., Al-Jawhari, M., Senghor, B., Huyse, T., and Dreyfuss, G. (2014). Phylogeny of seven Bulinus species originating from endemic areas in three African countries, in relation to the human blood fluke Schistosoma haematobium. BMC Evol. Biol., 14.","DOI":"10.1186\/s12862-014-0271-3"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/S0001-706X(03)00029-9","article-title":"Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa","volume":"86","author":"Brooker","year":"2003","journal-title":"Acta Trop."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Aula, O.P., McManus, D.P., Jones, M.K., and Gordon, C.A. (2021). Schistosomiasis with a Focus on Africa. Trop. Med. Infect. Dis., 6.","DOI":"10.3390\/tropicalmed6030109"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1111\/j.1469-7998.2006.00274.x","article-title":"Spatial and temporal population genetic survey of Bulinus globosus from Zanzibar: An intermediate host of Schistosoma haematobium","volume":"272","author":"Wilkinson","year":"2007","journal-title":"J. Zool."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.actatropica.2016.06.001","article-title":"Population genetic structure of the freshwater snail, Bulinus globosus, (Gastropoda: Planorbidae) from selected habitats of KwaZulu-Natal, South Africa","volume":"161","author":"Mkize","year":"2016","journal-title":"Acta Trop."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.2307\/2409721","article-title":"Self-Fertilization Versus Cross-Fertilization in the Hermaphroditic Freshwater Snail Bulinus globosus","volume":"45","author":"Jarne","year":"1991","journal-title":"Evolution"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1590\/S0074-02762002000900008","article-title":"Identification of snails within the Bulinus africanus group from East Africa by multiplex SNaPshot trade mark analysis of single nucleotide polymorphisms within the cytochrome oxidase subunit I","volume":"97","author":"Stothard","year":"2002","journal-title":"Mem. Inst. Oswaldo. Cruz."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.actatropica.2014.04.014","article-title":"Significant population genetic structure of the Cameroonian fresh water snail, Bulinus globosus, (Gastropoda: Planorbidae) revealed by nuclear microsatellite loci analysis","volume":"137","author":"Njiokou","year":"2014","journal-title":"Acta Trop."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.molbiopara.2018.06.004","article-title":"Revealing genetic hybridization and DNA recombination of Fasciola hepatica and Fasciola gigantica in nuclear introns of the hybrid Fasciola flukes","volume":"223","author":"Saijuntha","year":"2018","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Tantrawatpan, C., Maleewong, W., Thanchomnang, T., Pilap, W., Agasuma, T., Andrews, R.H., Sithithaworn, P., and Saijuntha, W. (2023). Intron regions as genetic markers for population genetic investigations of Opisthorchis viverrini sensu lato and Clonorchis sinensis. Animals, 13.","DOI":"10.3390\/ani13203200"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1093\/mollus\/eyu053","article-title":"Characterization of arginine kinase from the caenogastropod Semisulcospira libertina, an intermediate host of Paragonimus westermani","volume":"80","author":"Jarilla","year":"2014","journal-title":"J. Molluscan Stud."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1080\/13235818.2020.1794294","article-title":"Characterization of arginine kinase intron regions and their potential as molecular markers for population genetic studies of Bithynia snails (Gastropoda: Bithyniidae) in Thailand","volume":"40","author":"Bunchom","year":"2020","journal-title":"Molluscan Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"449","DOI":"10.4269\/ajtmh.2004.70.449","article-title":"Distribution patterns and cercarial shedding of Bulinus nasutus and other snails in the Msambweni area, Coast Province, Kenya","volume":"70","author":"Kariuki","year":"2004","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_17","unstructured":"Kristensen, T.K. (1987). A Field Guide to African Freshwater Snails, Danish Bilharziasis Laboratory. [2nd ed.]."},{"key":"ref_18","first-page":"294","article-title":"DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates","volume":"3","author":"Folmer","year":"1994","journal-title":"Mol. Mar. Biol. Biotechnol."},{"key":"ref_19","first-page":"95","article-title":"BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95\/98\/NT","volume":"41","author":"Hall","year":"1999","journal-title":"Nucleic Acids Symp. Ser."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J. Mol. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2947","DOI":"10.1093\/bioinformatics\/btm404","article-title":"Clustal W and Clustal X version 2.0","volume":"23","author":"Larkin","year":"2007","journal-title":"Bioinformatics"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1451","DOI":"10.1093\/bioinformatics\/btp187","article-title":"DnaSP v5: A software for comprehensive analysis of DNA polymorphism data","volume":"25","author":"Librado","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1007\/BF01731581","article-title":"A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences","volume":"16","author":"Kimura","year":"1980","journal-title":"J. Mol. Evol."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Nei, M., and Kumar, S. (2000). Molecular Evolution and Phylogenetics, Oxford University Press.","DOI":"10.1093\/oso\/9780195135848.001.0001"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1093\/oxfordjournals.molbev.a026036","article-title":"Median-joining networks for inferring intraspecific phylogenies","volume":"16","author":"Bandelt","year":"1999","journal-title":"Mol. Biol. Evol."},{"key":"ref_27","first-page":"11","article-title":"Polyploidy in Bulinid Snails, with Emphasis on Bulinus truncatus\/tropicus Complex (Planorbidae: Pulmonate Mollusks) from Various Localities in Ethiopia","volume":"3","author":"Yusuf","year":"2017","journal-title":"World J. Cell Biol. Genet."},{"key":"ref_28","first-page":"855","article-title":"Karyotype analysis of bulinid snails","volume":"45","author":"Claugher","year":"1971","journal-title":"Bull. World Health Organ."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.ijpara.2019.10.007","article-title":"Genetic structure and geographical variation of Bithynia siamensis goniomphalos sensu lato (Gastropoda: Bithyniidae), the snail intermediate host of Opisthorchis viverrini sensu lato (Digenea: Opisthorchiidae) in the Lower Mekong Basin revealed by mitochondrial DNA sequences","volume":"50","author":"Tantrawatpan","year":"2020","journal-title":"Int. J. Parasitol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.4269\/ajtmh.13-0260","article-title":"Genetic structure inferred from mitochondrial 12S ribosomal RNA sequence of Oncomelania quadrasi, the intermediate snail host of Schistosoma japonicum in the Philippines","volume":"90","author":"Saijuntha","year":"2014","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"S211","DOI":"10.1017\/S0031182001007703","article-title":"Schistosoma mansoni and Biomphalaria: Past history and future trends","volume":"123","author":"Morgan","year":"2001","journal-title":"Parasitology"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1627","DOI":"10.2307\/2411336","article-title":"Selection and Strain Specificity of Compatibility between Snail Intermediate Hosts and Their Parasitic Schistosomes","volume":"52","author":"Webster","year":"1998","journal-title":"Evolution"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Babbitt, C.R., Laidemitt, M.R., Mutuku, M.W., Oraro, P.O., Brant, S.V., Mkoji, G.M., and Loker, E.S. (2023). Bulinus snails in the Lake Victoria Basin in Kenya: Systematics and their role as hosts for schistosomes. PLoS Negl. Trop. Dis., 17.","DOI":"10.1371\/journal.pntd.0010752"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.meegid.2014.04.025","article-title":"Multi-parasite host susceptibility and multi-host parasite infectivity: A new approach of the Biomphalaria glabrata\/Schistosoma mansoni compatibility polymorphism","volume":"26","author":"Theron","year":"2014","journal-title":"Infect. Genet. Evol."}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/14\/1\/53\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,8]],"date-time":"2025-10-08T10:26:41Z","timestamp":1759919201000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/14\/1\/53"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,10]]},"references-count":34,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,1]]}},"alternative-id":["biology14010053"],"URL":"https:\/\/doi.org\/10.3390\/biology14010053","relation":{},"ISSN":["2079-7737"],"issn-type":[{"type":"electronic","value":"2079-7737"}],"subject":[],"published":{"date-parts":[[2025,1,10]]}}}