Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-26T06:53:57.442Z Has data issue: false hasContentIssue false

Do self-fertilization and genetic drift promote a very low genetic variability in the allotetraploid Bulinus truncatus (Gastropoda: Planorbidae) populations?

Published online by Cambridge University Press:  14 April 2009

Flobert Njiokou
Affiliation:
Laboratoire d'Epidémiologic des Maladies à Vecteurs, ORSTOM, 911 Avenue Agropolis B. P. 5045, 34032 Montpellier, France
Christian Bellec
Affiliation:
Laboratoire d'Epidémiologic des Maladies à Vecteurs, ORSTOM, 911 Avenue Agropolis B. P. 5045, 34032 Montpellier, France
Patrick Berrebi
Affiliation:
Génome et Populations (CNRS, URA 1493), Université Montpellier II, Place E. Bataillon, 34095 Montpellier Cedex 5, France
Bernard Delay
Affiliation:
Génétique et Environnement, Institut des Sciences de I'Evolution, Université Montpellier II, Place E. Bataillon, 34095 Montpellier Cedex 5, France
Philippe Jarne*
Affiliation:
Génétique et Environnement, Institut des Sciences de I'Evolution, Université Montpellier II, Place E. Bataillon, 34095 Montpellier Cedex 5, France
*
* Corresponding author.
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Bulinus truncatus, one of the intermediate hosts of the genus Schistosoma is an hermaphrodite freshwater snail species occupying a variety of environments over almost all Africa. These environments are subjected to large variations in water availability. B. truncatus is allotetraploid and its populations exhibit various frequencies of aphallic individuals (unable to reproduce as male). Both traits probably favour a reproduction by self-fertilization. Here we investigate the genetic structure of populations of B. truncatus of Niger and Ivory Coast using protein electrophoresis to analyse the influence of the environment and of both the last traits. To obtain an estimate of the true heterozygosity in this allotetraploid species, we analyse independently the two diploid loci at each tetraploid locus. Our study indicates (i) an extremely low intrapopulation polymorphism with most alleles fixed and the total absence of heterozygotes and (ii) low differentiation between populations. These results indicate high gene flow between populations. However, the existence of private alleles sometimes at high frequency, the low polymorphism and the lack of heterozygotes point to the role of both genetic drift and self-fertilization, the second amplifying the genetic consequences of the first.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

References

Allard, R. W., & Kahler, A. L., (1971). Allozyme polymorphism in plant populations, Stadler. Symposia University of Missouri 3, 924.Google Scholar
Allendorf, F. W., & Thorgaard, G. H., (1984). Tetraploidy and the evolution of Salmonid fishes In Evolutionary Genetics of Fishes (ed. Turner, B. J.), pp. 153. Plenum Publishing Corporation.Google Scholar
Arru, E., Nascetti, G., Orecchia, P., & Paggi, L., (1980). Studi morfologici e genetici su alcune popolazioni di Mandahl-barthia truncata (Gastropoda: Planorbidae) della Sar-degna. Parassitologia 22, 275279.Google Scholar
Bandoni, S. M., Mulvey, M., Koech, D. K., & Locker, E. S., (1990). Genetic structure of Kenyan populations of Biomphalaria pfeifferi (Gastropoda: Planorbidae). Journal of Molluscan Studies 56, 383391.CrossRefGoogle Scholar
Benzecri, J. P., (1973). L' Analyse des Données. Tome 2: l' Analyse des Correspondances. Paris: Dunod.Google Scholar
Berrebi, P., Lévêque, C., Cattaneo-Berrebi, G., Agnèse, J. F., Gueguan, J. F., & Machordon, A., (1990). Diploid and tetraploid African Barbus (Osteichthyes, Cyprinidae): on the coding of differential gene expression. Aquatic Living Resources 3, 313323.CrossRefGoogle Scholar
Betterton, C., (1984). Ecological studies on the snail hosts of schistosomiasis in the South Chad Irrigation project area, Borno state, northern Nigeria. Journal of Arid Environment 7, 4357.CrossRefGoogle Scholar
Boag, D. A., (1986). Dispersal in pond snails: potential role of waterfowl. Canadian Journal of Zoology 64, 904909.CrossRefGoogle Scholar
Brown, A. H. D., (1989). Genetic characterization of plant mating systems In Plant Population Genetics, Breeding, and Genetic Resources (ed. Brown, A. H. D., Clegg, M. T., Kahler, A. L. and Weir, B. S.), pp. 145162. Sunderland, Mass.: Sinauer Associates Inc.Google Scholar
Brown, K. M., & Richardson, T. D., (1988). Genetic polymorphism in gastropods: a comparison of methods and habitat scales. American Malacological Bulletin 6, 917.Google Scholar
Brown, D. S., (1976). A tetraploid freshwater snail (Planorbidae: Bulinus) in the highlands of Kenya. Journal of Natural History 10, 257267.CrossRefGoogle Scholar
Brown, D. S., (1980). Freshwater Snails of Africa and their Medical Importance. London: Taylor & Francis Ltd.Google Scholar
Brown, D. S., & Wright, C. A., (1972). On a polyploid complex of freshwater snails (Planorbidae: Bulinus) in Ethiopia. Journal of Zoology, London 167, 97132.CrossRefGoogle Scholar
Doumenge, J. P., Mott, K. E., Cheung, C., Villenav, D., Chapuis, C., Perrin, M. F., & Reaud-Thomas, G., (1987). Atlas of the Global Distribution of Schistosomiasis. Centre d' Etudes de Géographie Tropicale (CNRS) World Health Organization. Talence: Presses Universitaires de Bordeaux.Google Scholar
Goldman, M. A., LoVerde, P. T., & Chrisman, C. L., (1983). Hybrid origin of polyploidy in freshwater snails of the genus Bulinus (Mollusca: Planorbidae). Evolution 37, 592600.CrossRefGoogle ScholarPubMed
Hamrick, J. L., & Godt, J. W., (1989). Allozymes diversity in plant species In Plant Population Genetics Breeding, and Genetic Resources (ed. Brown, A. H. D., Clegg, M. T., Kahler, A. L. and Weir, B. S.), pp. 4363. Sunderland, Mass.: Sinauer Associates Inc.Google Scholar
Hartl, D. L., (1980). Principles of Population Genetics. Sunderland, Mass.: Sinauer Associates Inc.Google Scholar
Hedrick, P. W., Hutchinson, E. S., Mesler, M., (1991). Estimation of self-fertilization rate and allelic frequencies in diploidized tetraploids. Heredity 67, 259264.CrossRefGoogle Scholar
Jarne, P., & Delay, B., (1990). Population genetics of Lymnaea peregra (Müller) (Gastropoda: Pulmonata) in Lake Geneva. Journal of Molluscan Studies 56, 317321.CrossRefGoogle Scholar
Jarne, P., & Delay, B., (1991). Population genetics of freshwater snails Trends in Ecology and Evolution 6, 383386.CrossRefGoogle ScholarPubMed
Jarne, P., Finot, L., Bellec, C., & Delay, B., (1992). Aphally versus euphally in selfing hermaphrodite snails from the species Bulinus truncatus (Pulmonata: Planorbidae). American Naturalist 139, 424432.CrossRefGoogle Scholar
Jarne, P., Vianey-Liaud, M., & Delay, B., (1993). Selfing and outcrossing in hermaphrodite freshwater gastropods (Basommatophoran): where, when and why Biological Journal of the Linnaean Society (inthe press).CrossRefGoogle Scholar
Jelnes, J. E., (1978). Experimental taxonomy of Bulinus (Gastropoda: Planorbidae). I. Electrophoretic studies on esterases and phosphoglucose isomerase of Bulinus truncatus. Archiv für Molluskenkunde 109, 237248.Google Scholar
Jelnes, J. E., (1979). Experimental taxonomy of Bulinus (Gastropoda: Planorbidae). II. Recipes for horizontal starch gel electrophoresis of ten enzymes in Bulinus and description of internal standard systems and of two new species of the Bulinus forskalii complex. Journal of Chromatography 170, 403411.Google Scholar
Jelnes, J. E., (1986). Experimental taxonomy of Bulinus (Gastropoda: Planorbidae): the West and North African species reconsidered based on an electrophoretic study of several enzymes per individual. Zoological Journal of the Linnaean Society 87, 126.CrossRefGoogle Scholar
Larambergue, M. de, (1939). Etude de léautofécondation chez les gastéropodes pulmonés. Recherche sur l'aphallie et la fécondation chez Bulinus (Isidora) contortus Michaux. Bulletin Biologique de la France et de la Belgique 73, 19231.Google Scholar
Lande, R., & Schemske, D. W., (1985). The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39, 2440.Google ScholarPubMed
Lewontin, R. C., (1974). The Genetic Basis of Evolutionary Change. New York: Columbia University Press.Google Scholar
McCauley, D. E., (1991). Genetic consequences of local population extinction and recolonization. Trends in Ecology and Evolution 6, 58.CrossRefGoogle ScholarPubMed
Mandahl-Barth, G., (1957). Intermediate hosts of Schistosoma. African Biomphalaria and Bulinus. 2. Bulletin of the World Health Organization 17, 135.Google Scholar
Marti, H. P., & Tanner, M., (1988). Field observations on the influence of low velocities on drifting of Bulinus globosus. Hydrobiologia 157, 119123.CrossRefGoogle Scholar
Mimpfoundi, R., & Greer, G. J., (1989). Allozyme comparison among species of the Bulinus forskalii group (Gastropoda: Planorbidae) in Cameroun. Journal of Molluscan Studies 55, 405410.CrossRefGoogle Scholar
Mimpfoundi, R., & Greer, G. J., (1990 a). Allozyme variation among populations of Bulinus forskalii (Ehrenberg, 1831) (Gastropoda: Planorbidae) in Cameroon. Journal of Molluscan Studies 56, 363371.CrossRefGoogle Scholar
Mimpfoundi, R., & Greer, G. J., (1990 b). Allozyme variation among populations of Biomphalaria pfeifferi (Krauss, 1848) (Gastropoda: Planorbidae) in Cameroon. Journal of Molluscan Studies 56, 461467.CrossRefGoogle Scholar
Mimpfoundi, R., & Greer, G. J., (1990 c). Allozyme variation among populations of Biomphalaria camerounensis (Boettger, 1941) (Gastropoda: Planorbidae) in Cameroun. Journal of Molluscan Studies 56, 373381.CrossRefGoogle Scholar
Mimpfoundi, R., & Greer, G. J., (1990 da). Allozyme comparison and ploidy levels among species of the Bulinus truncatus/tropicus complex (Gastropoda: Planorbidae). Journal of Molluscan Studies 56, 6368.CrossRefGoogle Scholar
Mulvey, M., & Vrijenhoek, R. C., (1982). Population structure in Biomphalaria glabrata: examination of an hypothesis for the patchy distribution of susceptibility to schistosomes. American Journal of Tropical Medicine and Hygiene 31, 11951200.CrossRefGoogle ScholarPubMed
Mulvey, M., Newman, M. C., & Woodruff, D. S., (1988). Genetic differentiation among West Indian populations of the schistosome-transmitting snail Biomphalaria glabrata. Malacologia 29, 309317.Google Scholar
Nascetti, G., & Bullini, L., (1980). Genetic differentiation in the Mandahlbarthia truncata complex (Gastropoda: Planorbidae). Parassitologia 22, 269274.Google Scholar
Nei, M., (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583590.CrossRefGoogle ScholarPubMed
Njiokou, F., Bellec, C., Jarne, P., Finot, L., & Delay, B., (1993). Mating system analysis using electrophoresis in the self-fertile hermaphrodite species Bulinus truncatus (Gastropoda: Planorbidae). Journal of Molluscan Studies 59, 125133.CrossRefGoogle Scholar
Ohno, S., (1970). Evolution by Gene Duplication. New York: Springer-Verlag.CrossRefGoogle Scholar
Paggi, L., Orecchia, P., Bullini, L., Nascetti, G., & Biocca, E., (1978). Studi morfologici, biologici e biochimici su una nuovo specie di Bulinus (Gastropoda: Planorbidae). Parassitologia 20, 16.Google Scholar
Pasteur, N., Pasteur, G., Bonhomme, F., Catalan, J., & Britton-Davidian, J., (1988). Practical Isoenzyme Genetics. New York: Halsted Press.Google Scholar
Rollinson, D., (1985). Biochemical genetics in the study of schistosomes and their intermediate hosts. Parasitology 27, 123139.Google Scholar
Rollinson, D., & Wright, C. A., (1984). Population studies on Bulinus cernicus from Mauritius. Malacologia 25, 447463.Google Scholar
Rollinson, D., Kane, R. A., Warlow, A., Southgate, V. R., & Gopaul, A. R., (1990). Observations on genetic diversity of Bulinus cernicus (Gastropoda: Planorbidae) from Mauritius. Journal of Zoology, London 222, 1926.CrossRefGoogle Scholar
Schrag, S. J., & Read, A. F., (1992). Temperature determination of male outcrossing ability in a simultaneous hermaphrodite. Evolution 46, 16981707.CrossRefGoogle Scholar
Selander, R. K., (1976). Genetic variation in natural populations In Molecular Evolution (ed. Ayala, F.), pp. 2145. Sunderland, Mass.: Sinauer Associates Inc.Google Scholar
Selander, R. K., & Kaufman, D. W., (1973). Self-fertilization and genetic population structure in a colonizing land snail. Proceedings of the National Academy of Science, USA 70, 11861190.CrossRefGoogle Scholar
Selander, R. K., & Ochman, H., (1983). The genetic structure of populations as illustrated by molluscs. In Isozymes: Current Topics in Biology and Medical Research, Genetics and Evolution 10, 93123.Google ScholarPubMed
Sellin, B., & Boudin, C., (1981). Les schistosomiases en Afrique de l' Ouest. Etudes médicates, mars, 187.Google Scholar
She, J. X., Autem, M., Kotulas, G., Pasteur, N., & Bonhomme, F., (1987). Multivariate analysis of genetic exchanges between Solea aegyptica and Solea senegalensis (Teleost: Soleidae). Biological Journal of Linnaean Society 32, 357371.CrossRefGoogle Scholar
Slatkin, M., (1977). Gene flow and genetic drift in a species subjected to frequent local extinction. Theoretical Population Biology 12, 253262.CrossRefGoogle Scholar
Slatkin, M., (1985 a). Gene flow in natural populations. Annual Review of Ecology and Systematics 16, 393430.CrossRefGoogle Scholar
Slatkin, M., (1985 b). Rare alleles as indicators of gene flow. Evolution 39, 5365.CrossRefGoogle ScholarPubMed
Smouse, P. E., Long, J. C., & Sokal, R. R., (1986). Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Systematic Zoology 35, 627632.CrossRefGoogle Scholar
Stebbins, G. L., (1977). Processes of Organic Evolution, 3rd edn. Englewood Cliffs: Prentice-Hall.Google Scholar
Vera, C., Jourdane, J., Sellin, B., & Combes, C., (1990). Genetic variability in the compatibility between Schistosoma haematobium and its potential vectors in Niger. Tropical Medicine and Parasitology 41, 143148.Google ScholarPubMed
Vrijenhoek, R. C., & Graven, M. A., (1992). Population genetics of Egyptian Biomphalaria alexandrina (Gastropoda, Planorbidae). Journal of Heredity 83, 255261.CrossRefGoogle Scholar
Wade, M. J., & McCauley, D. E., (1988). Extinction and recolonisation: their effects on the genetic differentiation of local populations. Evolution 42, 9951005.CrossRefGoogle Scholar
Waples, R. S., (1989). Temporal variation in allele frequencies: testing the right hypothesis. Evolution 43, 12361251.CrossRefGoogle ScholarPubMed
Woolhouse, M. E. J., & Chandiwana, S. K., (1989). Spatial and temporal heterogeneity in the population dynamics of Bulinus globosus and Biomphalaria pfeifferi and in the epidemiology of their infection with schistosomes. Parasitology 98, 2134.CrossRefGoogle ScholarPubMed
Wright, C. A., (1977). Co-evolution of Bulinid snails and African schistosomes In Medicine in a Tropical Environment (ed. Gear, J. H.), pp. 291300. Capetown: Balkema.Google Scholar
Wright, C. A., & Rollinson, D., (1981). Analysis of enzymes in the Bulinus tropicus/truncatus complex (Mollusca: Planorbidae). Journal of Natural History 15, 873885.CrossRefGoogle Scholar
Wurzinger, K. H., & Saliba, E. K., (1979). A cytological and electrophoretic comparison of Jordanian Bulinus with three other tetraploid Bulinus populations. Malacological Review 12, 583591.Google Scholar