RESEARCH PAPER
Genetic diversity of the freshwater snail Biomphalaria tenagophila (d’Orbigny, 1835) (Gastropoda: Hygrophila: Planorbidae) across two coastal areas of southeast Brazil
 
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1
School of Public Health USP, São Paulo, Brazil
 
2
University of Campinas, Campinas, Brazil
 
3
Superintendence of Control of Endemic Diseases, São Paulo, Brazil
 
 
Submission date: 2018-06-26
 
 
Final revision date: 2018-10-25
 
 
Acceptance date: 2018-10-27
 
 
Publication date: 2018-12-04
 
 
Corresponding author
Roseli Tuan   

Superintendence of Control of Endemic Diseases, Rua Paula Sousa 166, 01027-000 São Paulo, Brazil
 
 
Folia Malacol. 2018;26(4):221-229
 
KEYWORDS
ABSTRACT
This study uses two mitochondrial (COI, 16SrRNA) and one nuclear marker (ITS2) to explore genetic diversity between populations of B. tenagophila (d’Orbigny), the most common intermediate host for Schistosoma mansoni in southeast Brazil. The snails were collected in freshwater bodies along the southern coastal region of Ribeira do Iguape river basin and along the northern coastal region of the state of São Paulo, Brazil. The estimates of genetic differentiation between the populations (Φ) indicate that there is no genetic isolation between northern and southern populations. The haplotype diversity observed in B. tenagophila shows a complex pattern of distribution: in the southern region, the genetic variation in B. tenagophila is partitioned into small and more heterogeneous mitochondrial haplotypes, whereas in the northern region there were one to three homogeneous haplotypes. The results may suggest a different colonisation history across the study area.
 
REFERENCES (45)
1.
Avise J. C., Neigel J. E., Arnold J. 1984. Demographic influences on mitochondrial DNA lineage survivorship in animal populations. Journal of Molecular Evolution 20: 99–105. https://doi.org/10.1007/BF0225....
 
2.
Barbosa F. S., Pereira C. D. P., Arruda F. 1985. Competitive interactions between species of freshwater snails. I. Laboratory studies: IC. Comparative survival of Biomphalaria glabrata and B. straminea kept out of water. Memórias do Instituto Oswaldo Cruz 80: 155–157. https://doi.org/10.1590/S0074-....
 
3.
Barboza D. M., Zhang C., Santos N. C., Silva M. M. B. L., Rollemberg C. V. V., Amorim F. J. R., Ueta M. T., Melo C. M. de, Almeida J. A. P. de, Lourdes Sierpe Jeraldo V. de, Jesus A. R. 2012. Biomphalaria species distribution and its effect on human Schistosoma mansoni infection in an irrigated area used for rice cultivation in northeast Brazil. Geospatial Health 6: S103–S109. https://doi.org/10.4081/gh.201....
 
4.
Carnaval A. C., Waltari E., Rodrigues M. T., Rosauer D., Van Der Wal J., Damasceno R., Prates I., Strangas M., Spanos Z., Rivera D., Pie M. R., Firkowski C. R., Bornschein M. R., Ribeiro L. F., Moritz C. 2014. Prediction of phylogeographic endemism in an environmentally complex biome. Proceedings of the Royal Society B, Biological Sciences 281: 1–8. https://doi.org/10.1098/rspb.2....
 
5.
Charbonnel N., Angers B., Rasatavonjizay R., Bremond P., Jarne P. 2002. Evolutionary aspects of the metapopulation dynamics of Biomphalaria pfeifferi, the intermediate host of Schistosoma mansoni. Journal of Evolutionary Biology 15: 248–261. https://doi.org/10.1046/j.1420....
 
6.
Clement M., Posada D., Crandall K. A. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659. https://doi.org/10.1046/j.1365....
 
7.
Excoffier L., Lischer H. E. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567. https://doi.org/10.1111/j.1755....
 
8.
Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294.
 
9.
Fu Y. X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925.
 
10.
Guimarães M. C. D. A., Menezes R. M. T. D., Tuan R. 2016. Experimental study on reproduction of the freshwater snail Biomphalaria tenagophila (d’Orbigny, 1835). Invertebrate Reproduction & Development 60: 1–7. https://doi.org/10.1080/079242....
 
11.
Hall T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98. http://brownlab.mbio.ncsu.edu/....
 
12.
Handley L. J. L., Estoup A., Evans D. M., Thomas C. E., Lombaert E., Facon B., Aebi A., Roy H. E. 2011. Ecological genetics of invasive alien species. BioControl 56: 409. https://doi.org/10.1007/s10526....
 
13.
Henriques J. M., Silva G. J. C., Ashikaga F. Y., Hanner R., Foresti F., Oliveira C. 2015. Use of DNA barcode in the identification of fish species from Ribeira de Iguape Basin and coastal rivers from São Paulo State (Brazil). DNA Barcodes 3: 118–128. https://doi.org/10.1515/dna-20....
 
14.
Huelsenbeck J. P., Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. https://doi.org/10.1093/bioinf....
 
15.
Langand J., Theron A., Pointier J. P., Delay B., Jourdane J. 1999. Population structure of Biomphalaria glabrata, intermediate snail host of Schistosoma mansoni in Guadeloupe island, using RAPD markers. Journal of Molluscan Studies 65: 425–433. https://doi.org/10.1093/mollus....
 
16.
Librado P., Rozas J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452. https://doi.org/10.1093/bioinf....
 
17.
Mavárez J., Steiner C., Pointier J. P., Jarne P. 2002. Evolutionary history and phylogeography of the schistosome-vector freshwater snail Biomphalaria glabrata based on nuclear and mitochondrial DNA sequences. Heredity 89: 266–272. https://doi.org/10.1038/sj.hdy....
 
18.
Mulvey M., Vrijenhoek R. C. 1982. Population structure in Biomphalaria glabrata: examination of an hypothesis for the patchy distribution of susceptibility to schistosomes. The American Journal of Tropical Medicine and Hygiene 31: 1195. https://doi.org/10.4269/ajtmh.....
 
19.
Nylander J. A. A. 2004. Bayesian phylogenetics and the evolution of gall wasps. Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 937.
 
20.
Palasio R. G. S. 2013. Polimorfismo dos genes mitocondrial 16S rRNA e nuclear ITS2 em populações de Biomphalaria tenagophila da Bacia Litorânea do estado de São Paulo e estudo da suscetibilidade dos caramujos ao Schistosoma mansoni. Ph.D. Thesis, Universidade Estadual de Campinas, Campinas, São Paulo.
 
21.
Palasio R. G. S., Guimarães M. C. A., Ohlweiler F. P., Tuan R. 2017. Molecular and morphological identification of Biomphalaria species from the state of São Paulo, Brazil. ZooKeys 668: 11–32. https://doi.org/10.3897/zookey....
 
22.
Palumbi S. R. 1996. Nucleic acids II: the polymerase chain reaction. In: Hillis D. M., Moritz C., Mable B. K. (eds). Molecular systematics. Sinauer Associates, Inc., Sunderland 2(1): 205–247.
 
23.
Paraense W. L. 1975. Estado atual da sistemática dos planorbídeos brasileiros. Arquivos do Museu Nacional 55: 105–128.
 
24.
Paraense W. L. 1981. Biomphalaria occidentalis sp. n. from South America (Mollusca Basommatophora Pulmonata). Memórias do Instituto Oswaldo Cruz 76: 199–211. https://doi.org/10.1590/S0074-....
 
25.
Paraense W. L. 2001. The schistosome vectors in the Americas. Memórias do Instituto Oswaldo Cruz 96: 7–16. https://doi.org/10.1590/S0074-....
 
26.
Plens C. R. 2009. O papel dos amontoados de conchas no sambaqui fluvial. Revista de Arqueologia 22: 77–93. https://doi.org/10.24885/sab.v....
 
27.
Por F. D., Imperatriz-Fonseca V. L. 1984. The Juréia Ecological Reserve, São Paulo, Brazil – facts and plans. Environmental Conservation 11: 67–70. https://doi.org/10.1017/S03768....
 
28.
Ronquist F., Huelsenbeck J. P. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. https://doi.org/10.1093/bioinf....
 
29.
Sevá Filho A., Kalinowski L. M. 2012. River diversion and hydropower plants: The unknown Ribeira Valley (PR-SP). Estudos Avançados 26: 269–286. https://doi.org/10.1590/S0103-....
 
30.
Sire C., Langand J., Barral V., Théron A. 2001. Parasite (Schistosoma mansoni) and host (Biomphalaria glabrata) genetic diversity: population structure in a fragmented landscape. Parasitology 122: 545–554. https://doi.org/10.1017/S00311....
 
31.
Souza C. R. G. 2005. Suscetibilidade morfométrica de bacias de drenagem ao desenvolvimento de inundações em áreas costeiras. Revista Brasileira de Geomorfologia 6: 45–61. https://doi.org/10.20502/rbg.v....
 
32.
Standley C. J., Goodacre S. L., Wade C. M., Stothard J. R. 2014. The population genetic structure of Biomphalaria choanomphala in Lake Victoria, East Africa: implications for schistosomiasis transmission. Parasites & Vectors 7: 524. https://doi.org/10.1186/s13071....
 
33.
Swofford D. L. 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
 
34.
Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.
 
35.
Theodorovicz A., Theodorovicz Â. M. D. G. 2007. Atlas geoambiental: subsídio ao planejamento territorial e à gestão ambiental da bacia hidrográfica do rio Ribeira de Iguape. 2. ed. Rev. CPRM, São Paulo.
 
36.
Thiele E. A., Corrêa Oliveira G., Gazzinelli A., Minchella D. J. 2013. Elucidating the temporal and spatial dynamics of Biomphalaria glabrata genetic diversity in three Brazilian villages. Tropical Medicine & International Health 18: 1164–1173. https://doi.org/10.1111/tmi.12....
 
37.
Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876–4882. https://doi.org/10.1093/nar/25....
 
38.
Tuan R., Ohweiller F., Palasio R. G. S., Zanna R., Guimarães M. C. A. 2012. Pattern of genetic divergence of mitochondrial DNA sequences in Biomphalaria tenagophila complex species under barcoding perspective. In: Rokni M. B. (ed.). Schistosomiasis. IntechOpen, London, pp. 293–310. https://doi.org/10.5772/25550.
 
39.
Tuan R., Santos P. 2007. ITS2 variability of Biomphalaria (Mollusca, Planorbidae) species from the Paranapanema Valley (São Paulo State, Brazil): diversity patterns, population structure and phylogenetic relationships. Genetics and Molecular Biology 30: 139–144. https://doi.org/10.1590/S1415-....
 
40.
Tuan R., Simões L. C. G. 1989. Spermatogenesis and desiccation in Biomphalaria tenagophila (Orbigny, 1835) (Gastropoda, Planorbidae). Revista Brasileira de Genetica Ribeirão Preto 12: 881–885.
 
41.
Vaz J. F. 1989. Distribuição e dispersão de Biomphalaria tenagophila (d’Orbigny, 1835) (Gastropoda-Pulmonata). Ciência e Cultura 41: 14–27.
 
42.
Vianey-Liaud M., Lancastre F. 1986. Laboratory studies on the desiccation of immature stages of the freshwater snail Biomphalaria glabrata. Annals of Tropical Medicine and Parasitology 80: 257–259. https://doi.org/10.1080/000349....
 
43.
Vidigal T. H. D. A., Kissinger J. C., Caldeira R. L., Pires E. C. R., Monteiro E., Simpson A. J. G., Carvalho O. S. 2000. Phylogenetic relationships among Brazilian Biomphalaria species (Mollusca: Planorbidae) based upon analysis of ribosomal ITS2 sequences. Parasitology 121: 611–620. https://doi.org/10.1017/S00311....
 
44.
Weir S. M., Salice C. J. 2012. High tolerance to abiotic stressors and invasion success of the slow growing freshwater snail, Melanoides tuberculatus. Biological Invasions 14: 385–394. https://doi.org/10.1007/s10530....
 
45.
Zein-Eddine R., Djuikwo-Teukeng F. F., Dar Y., Dreyfuss G., Van den Broeck F. 2017. Population genetics of the Schistosoma snail host Bulinus truncatus in Egypt. Acta Tropica 172: 36–43. https://doi.org/10.1016/j.acta....
 
 
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