Bulinus globosus (Planorbidae; Gastropoda) populations in the Lake Victoria basin and coastal Kenya show extreme nuclear genetic differentiation

Acta Tropica

Volumn 128, Issue 2, 2013, Pages 226-233

  Nyakaana, Silvester ^a   Stothard, J Russell ^b   Nalugwa, Allen ^a   Webster, Bonnie L ^c   Lange, Charles N ^d   Jørgensen, Aslak ^e   Rollinson, David ^b   Kristensen, Thomas K ^f  

^a MAKERERE UNIVERSITY   (Uganda)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^c DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^d INSTITUTE OF PRIMATE RESEARCH   (Kenya)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Bulinus globosus; Genetic drift; Kenya; Microsatellites; Population structure; Schistosomiasis; Uganda

Indexed keywords

ALGORITHM; BAYESIAN ANALYSIS; EXTINCTION; GENETIC DIFFERENTIATION; GENETIC DRIFT; GENETIC STRUCTURE; PARASITE; POLYMORPHISM; POPULATION STRUCTURE; RECOLONIZATION; SEASONAL VARIATION; SNAIL;

ARTICLE; BULINUS; BULINUS GLOBOSUS; ENVIRONMENTAL RECOLONIZATION; GENE FREQUENCY; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HABITAT PATCHINESS; HETEROZYGOSITY; HETEROZYGOTE; HOMOZYGOSITY; INBREEDING; KENYA; MATING SYSTEM; NONHUMAN; POPULATION GENETICS; POPULATION STRUCTURE; SPECIES EXTINCTION; STATISTICAL ANALYSIS; UGANDA;

EAST AFRICAN LAKES; KENYA; LAKE VICTORIA; UGANDA;

BULINUS GLOBOSUS; GASTROPODA; PLANORBIDAE; SCHISTOSOMA HAEMATOBIUM;

BULINUS GLOBOSUS; GENETIC DRIFT; KENYA; MICROSATELLITES; POPULATION STRUCTURE; SCHISTOSOMIASIS; UGANDA;

ANIMALS; BULINUS; DISEASE VECTORS; FRESH WATER; GENETIC VARIATION; MICROSATELLITE REPEATS;

EID: 84885471197     PISSN: 0001706X     EISSN: 18736254     Source Type: Journal    
DOI: 10.1016/j.actatropica.2012.12.010     Document Type: Article

References (43)

1. Boag D.A. Dispersal in pond snails: potential role of waterfowl. Can. J. Zool. 1986, 64:904-909.
2. Brown D.S. Freshwater Snails of Africa and their Medical Importance 1980, Taylor and Francis, London.
3. Brown D.S. Freshwater Snails of Africa and Their Medical Importance 1994, Taylor & Francis, London. 2nd ed.
4. Chapuis M.P., Estoup A. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 2007, 24:621-631.
5. Charbonnel N., Angers B., Rasatavonjizay R., Bremond P., Jarne P. Evolutionary aspects of the metapopulation dynamics of Biomphalaria pfeifferi, the intermediate host of Schistosoma mansoni. J. Evol. Biol. 2002, 15:248-261.
6. Couvet D. Deleterious effects of restricted gene flow in fragmented populations. Conserv. Biol. 2002, 16:369-376.
7. Darwin C.R. The Various Contrivances by Which Orchids are Fertilized by Insects 1877, John Murray, London. 2nd ed.
8. Darwin C.R. The Effects of Cross and Self-fertilization in the Vegetable Kingdom 1878, John Murray, London. 2nd ed.
9. DBL-WHO A Field Guide to African Freshwater Snails 1998, Danish Bilharziasis Laboratory. WHO Collaborating Centre for Applied Malacology, Charlottenlund, Denmark.
10. Emery A.M., Loxton N.J., Stothard J.R., Jones C.S., Spinks J., Llewellyn-Hughes J., Noble L.R., Rollinson D. Microsatellites in the freshwater snail Bulinus globosus (Gastropoda: Planorbidae) from Zanzibar. Mol. Ecol. Notes 2003, 3:108-110.
11. Ersts, P.J., Internet. Geographic Distance Matrix Generator (Version 1.2.3). American Museum of Natural History, Center for Biodiversity and Conservation. Available from: (accessed November 28, 2012). http://biodiversityinformatics.amnh.org/open_source/gdmg.
12. Excoffier L., Laval G., Schneider S. Arlequin ver. 3.1: an integrated software package for population genetics data analysis. Evol. Bioinform. 2005, 1:47-50.
13. Green A.J., Figuerola J. Recent advances in the study of long distance dispersal of aquatic invertebrates via birds. Divers. Distrib. 2005, 11:149-156.
14. Jarne P., Delay B. Population genetics of freshwater snails. Trends Ecol. Evol. 1991, 6:383-386.
15. Jarne P., Finot L., Delay B., Thaler L. Self-fertilization versus cross-fertilization in the hermaphrodite freshwater snail Bulinus globosus. Evolution 1991, 45:1136-1146.
16. Jensen J.L., Bohonak A.J., Kelley S.T. Isolation by distance, web service. BMC Genet. 2005, 6:13.
17. Kabatereine N.B., Brooker S., Tukahebwa E.M., Kazibwe F., Onapa A.W. Epidemiology and geography of Schistosoma mansoni in Uganda: implications for planning control. Trop. Med. Int. Health 2004, 9:372-380.
18. Keller L.F., Waller D.M. Inbreeding effects in wild populations. Trends Ecol. Evol. 2002, 17:230-241.
19. Kristensen T.K. A Field Guide to African Freshwater Snails. East African Species 1987, Danish Bilharziasis Laboratory, Copenhagen, pp. 45-48. 2nd ed.
20. Marti H.P., Tanner M. Field observations on the influence of low velocities on drifting of Bulinus globosus. Hydrobiologia 1988, 157:119-123.
21. Mavárez J., Amarista M., Pointier J.-P., Jarne P. Fine-scale population structure and dispersal in Biomphalaria glabrata, the intermediate snail host of Schistosoma mansoni, in Venezuela. Mol. Ecol. 2002, 11:879-889.
22. Mavárez J., Pointier J.-P., David P., Delay B., Jarne P. Genetic differentiation, dispersal and mating system in the schistosome-transmitting freshwater snail Biomphalaria glabrata. Heredity 2002, 89:258-265.
23. Nalugwa A., Jørgensen A., Nyakaana S., Kristensen T.K. Genetic variation within and between populations of hermaphroditic Bulinus truncatus tetraploid freshwater snails of the Albertine Rift, East Africa. Hydrobiologia 2011, 673:53-61.
24. Nei M. Molecular Evolutionary Genetics 1987, Columbia University Press, New York.
25. Pashley D.P., Bush G.L. The use of allozymes in studying insect movement with special reference to the codling moth, Laspeyresia pomonells (L) (Olethreutidae). Movement of Highly Mobile Insects: Concepts and Methodology in Research 1980, 333-341. North Carolina State University Press, Raleigh, NC. R.L. Rabb, G.G. Kennedy (Eds.).
26. Pritchard J.K., Stephens M., Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
27. Raymond M., Rousset F. An exact test for population differentiation. Evolution 1995, 49:1280-1283.
28. Rice W.R. Analyzing tables of statistical tests. Evolution 1989, 43:223-225.
29. Rousset F. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 1997, 145:1219-1228.
30. Rousset F. Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour. 2008, 8:103-106.
31. Ryman N., Palm S. POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol. Ecol. 2006, 6:600-602.
32. Saiki R.K., Sharf S., Faloona F., Mullis K.B., Horn G.T., Erlich H.A., Arnheim N. Enzymic amplification of β-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 1985, 230:1350-1354.
33. Saiki R.K., Gelfand D.H., Stoffel S., Scharf S.J., Higuchi R., Horn G.T., Mullis K.B., Erlich H.A. Primer-directed enzymatic amplification of DNA with thermostable DNA polymerase. Science 1988, 239:487-491.
34. Schaal B.A., Leverich W.J. Molecular variation in isolated plant populations. Plant Species Biol. 1996, 11:33-40.
35. Slatkin M. Gene flow in natural populations. Ann. Rev. Ecol. Syst. 1985, 16:393-430.
36. Slatkin M. Rare alleles as indicators of gene flow. Evolution 1985, 39:53-65.
37. Wade M.J., McCauley D.E. Extinction and recolonization: their effects on the genetic differentiation of local populations. Evolution 1988, 42:995-1005.
38. Webbe G. Schistosomiasis: some advances. Brit. Med. J. 1981, 283:1104-1106.
39. Weir B.S., Cockerham B.B. Estimating F-statistics for the analysis of population structure. Evolution 1984, 38:1358-1370.
40. Wethington A.R., Zadovna M., Smith M.K., Oliviera G., Lewis F., Minchella D.J. Population genetic structure of Biomphalaria glabrata in a schistosomiasis-endemic region in Brazil. J. Mollusc. Stud. 2007, 73:45-52.
41. WHO, 2010. Scistosomiasis, Fact Sheet No. 115. Available from: http://www.who.int/mediacentre/facesheets/fs115/en/index.html.
42. Wilkinson S., Emery A.M., Khamis I.S., Mgeni A.F., Stothard J.R., Rollinson D. Spatial and temporal population genetic survey of Bulinus globosus from Zanzibar: an intermediate host of Schistosoma haematobium. J. Zool. 2007, 272:329-339.
43. Woolhouse M.E.J., Chandiwana S.K. Spatial and temporal heterogeneity in the population dynamics of Bulinus globosus and Biomphalaria pfeifferi and in the epidemiology of their infection with schistosomes. Parasitology 1989, 98:21-34.