Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-28T19:24:09.417Z Has data issue: false hasContentIssue false

Parasite (Schistosoma mansoni) and host (Biomphalaria glabrata) genetic diversity: population structure in a fragmented landscape

Published online by Cambridge University Press:  07 August 2001

C. SIRE
Affiliation:
Laboratoire de Biologie Animale, UMR CNRS-UP 5555, Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, 52 Av. de Villeneuve, 66860 Perpignan Cedex, France
J. LANGAND
Affiliation:
Laboratoire de Biologie Animale, UMR CNRS-UP 5555, Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, 52 Av. de Villeneuve, 66860 Perpignan Cedex, France
V. BARRAL
Affiliation:
Laboratoire de Biologie Animale, UMR CNRS-UP 5555, Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, 52 Av. de Villeneuve, 66860 Perpignan Cedex, France
A. THÉRON
Affiliation:
Laboratoire de Biologie Animale, UMR CNRS-UP 5555, Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, 52 Av. de Villeneuve, 66860 Perpignan Cedex, France

Abstract

Random amplified polymorphic DNA (RAPD) markers were used to quantify genetic diversity within and between 5 populations of Schistosoma mansoni within its definitive host (Rattus rattus) and the 5 corresponding populations of the snail intermediate host (Biomphalaria glabrata) from a limited endemic area of murine schistosomiasis on the island of Guadeloupe. Analysis of molecular variance (AMOVA) and canonical correspondence analysis (CCA) were used to test the significance of genetic differentiation between populations. Both methods gave similar results. Of total gene diversity, 15.1% (AMOVA) and 18.8% (CCA) was partitioned between localities for S. mansoni with an absence of association between genetic and geographical distances. Geographical localities accounted for 20.5% (CCA) of the total diversity for B. glabrata populations. The genetic distances between pairs of parasite populations were not correlated with the genetic distances between the corresponding pairs of snail host populations. Such strong patterns of local differentiation of both parasite and snail populations are consistent with predictions based on metapopulation dynamics and may have implications on host–parasite susceptibility relationship through local adaptation processes.

Type
Research Article
Copyright
2001 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

ANDERSON, T. J. C., BLOUIN, M. S. & BEECH, R. N. (1998). Population biology of parasitic nematodes: application of genetic markers. Advances in Parasitology 41, 219283.CrossRefGoogle Scholar
ANDERSON, T. J. C., ROMERO-ABAL, M. E. & JAENIKE, J. (1993). Genetic structure and epidemiology of Ascaris population: patterns of host affiliation in Guatemala. Parasitology 107, 319334.CrossRefGoogle Scholar
ANDERSON, T. J. C., ROMERO-ABAL, M. E. & JAENIKE, J. (1995). Mitochondrial DNA and Ascaris microepidemiology: the composition of parasite populations from individual hosts, families and villages. Parasitology 110, 221229.CrossRefGoogle Scholar
BARRAL, V., MORAND, S., POINTIER, J. P. & THÉRON, A. (1996). Distribution of schistosome genetic diversity within naturally infected Rattus rattus detected by RAPD markers. Parasitology 113, 511517.CrossRefGoogle Scholar
BARRAL, V., THIS, P., IMBERT-ESTABLET, D., COMBES, C. & DELSENY, M. (1993). Genetic variability and evolution of the Schistosoma genome analysed by using random amplified polymorphic DNA markers. Molecular and Biochemical Parasitology 59, 211222.CrossRefGoogle Scholar
BLOUIN, M. S., DAME, J. B., TARRANT, C. A. & COURTNEY, C. H. (1992). Unusual population genetics of a parasitic nematode: mtDNA variation within and among populations. Evolution 46, 470476.CrossRefGoogle Scholar
BLOUIN, M. S., LIU, J. & BERRY, R. E. (1999). Life cycle variation and the genetic structure of nematode populations. Heredity 83, 253259.CrossRefGoogle Scholar
BLOUIN, M. S., YOWELL, C. A., COURTNEY, C. H. & DAME, J. B. (1995). Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141, 10071014.Google Scholar
BULLINI, L., NASCETTI, G., PAGGI, L., ORECCHIA, P., MATTIUCCI, S. & BERLAND, B. (1986). Genetic variation of ascaridoid worms with different life cycles. Evolution 40, 434440.Google Scholar
BUSH, A. O., CAIRA, J. N., MINCHELLA, D. J., NADLER, S. A. & SEED, J. R. (1995). Parasitology year 2000. Journal of Parasitology 81, 835842.CrossRefGoogle Scholar
CHARBONNEL, N., ANGERS, B., RAZATAVONJIZAY, R., BREMOND, P. & JARNE, P. (2000). Microsatellite variation in the freshwater snail Biomphalaria pfeifferi. Molecular Ecology 9, 1006.CrossRefGoogle Scholar
CHILTON, N. B., BAO-ZHEN, Q., BOGH, H. O. & NANSEN, P. (1999). An electrophoretic comparison of Schistosoma japonicum (Trematoda) from different provinces in the People's Republic of China suggests the existence of cryptic species. Parasitology 119, 375383.CrossRefGoogle Scholar
CURTIS, J. & MINCHELLA, D. J. (2000). Schistosome population genetic structure: when clumping worms is not just splitting hairs. Parasitology Today 16, 6871.CrossRefGoogle Scholar
DABO, A., DURAND, P., MORAND, S., LANGAND, J., IMBERT-ESTABLET, D., DOUMBO, O. & JOURDANE, J. (1997). Dispersion and genetic diversity of Schistosoma haematobium within its Bulinid intermediate hosts in Mali. Acta Tropica 66, 1526.CrossRefGoogle Scholar
DAVIES, C. M., WEBSTER, J. P., KRÜGER, O., MUNATSI, A., NDAMBA, J. & WOOLHOUSE, M. E. J. (1999). Host–parasite population genetics, a cross-sectional comparison of Bulinus globosus and Schistosoma haematobium. Parasitology 119, 295302.CrossRefGoogle Scholar
DELATTRE, P. & LE LOUARN, H. (1981). Dynamique des populations du rat noir, Rattus rattus, en mangrove lacustre. Mammalia 45, 275288.CrossRefGoogle Scholar
DIAS NETO, E., PEREIRA DE SOUZA, C., ROLLINSON, D., KATZ, N., PENA, S. D. J. & SIMPSON, A. J. G. (1993). The random amplification of polymorphic DNA allows the identification of strains and species of schistosomes. Molecular and Biochemical Parasitology 57, 8388.CrossRefGoogle Scholar
DYBDAHL, M. F. & LIVELY, C. M. (1996). The geography of coevolution: comparative population structures for a snail and its trematode parasite. Evolution 50, 22642275.CrossRefGoogle Scholar
DURAND, P., SIRE, C. & THÉRON, A. (2000). Isolation of microsatellite markers in the digenetic trematode Schistosoma mansoni from Guadeloupe island. Molecular Ecology 9, 997998.CrossRefGoogle Scholar
DUVALL, R. H. & DEWITT, W. B. (1967). An improved perfusion technique for recovering adult schistosomes from laboratory animals. American Journal of Tropical Medicine and Hygiene 16, 483486.CrossRefGoogle Scholar
ESCOFFIER, L., SMOUSE, P. E. & QUATTRO, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479491.Google Scholar
FISHER, M. C. & VINEY, M. E. (1998). The population genetic structure of the facultatively sexual parasitic nematode Strongyloides ratti in wild rats. Proceedings of the Royal Society of London, B 265, 703709.CrossRefGoogle Scholar
GABRIELSEN, M., BACHMANN, K., JAKOBSEN, K. S. & BROCHMAN, C. (1997). Glacial survival does not matter: RAPD phylogeography of Nordic Saxifraga oppositifolia. Molecular Ecology 6, 834842.Google Scholar
GANDON, S., CAPOWIEZ, Y., DUBOIS, Y., MICHALAKIS, Y. & OLIVIERI, I. (1996). Local adaptation and gene for gene coevolution in a metapopulation model. Proceedings of the Royal Society of London, B 263, 10031009.CrossRefGoogle Scholar
GANDON, S. & VAN ZANDT, P. A. (1998). Local adaptation and host-parasite interactions. Trends in Ecology and Evolution 13, 214216.CrossRefGoogle Scholar
GASSER, R. B., BAO-ZHEN, Q., NANSEN, P., JOHANSEN, M. V. & BOGH, H. (1996). Use of RAPD for the detection of genetic variation in the human blood fluke, Schistosoma japonicum, from mainland China. Molecular and Cellular Probes 10, 353358.CrossRefGoogle Scholar
HADRYS, H., BALICK, M. & SCHIERWATER, B. (1992). Application of random amplified polymorphic DNA (RAPD) in molecular ecology. Molecular Ecology 1, 5563.CrossRefGoogle Scholar
HANSKI, I. & GILPIN, M. (1997). Metapopulation Biology:Ecology, Genetics and Evolution. Academic Press, London.
HASTINGS, A. & HARRISON, S. (1994). Metapopulation dynamics and genetics. Annual Review of Ecology and Systematics 25, 167188.CrossRefGoogle Scholar
HUFF, D. R., PEAKALL, R. & SMOUSE, P. E. (1993). RAPD variation within and among natural populations of outcrossing buffalograss (Buchlöe dactyloides (Nutt.) Englem.). Theoretical and Applied Genetics 86, 927934.Google Scholar
JARNE, P. & LAGODA, P. J. L. (1996). Microsatellites, from molecules to populations and back. Trends in Ecology and Evolution 11, 424429.CrossRefGoogle Scholar
JOBET, E., DURAND, P., LANGAND, J., MÜLLER-GRAF, C. D. M., HUGOT, J-P., BOUGNOUX, M-E., RIVAULT, C., COAREC, A. & MORAND, S. (2000). Comparative genetic diversity of parasites and their host: population structure of an urban cockroach and its haplo-diploid parasite (oxyuroid nematode). Molecular Ecology 9, 481486.CrossRefGoogle Scholar
JONES, C. S., LOCKYER, A. E., ROLLINSON, D., PIERTNEY, S. B. & NOBLE, L. R. (1999). Isolation and characterization of microsatellite loci in the freshwater gasteropode, Biomphalaria glabrata, an intermediate host for Schistosoma mansoni. Molecular Ecology 8, 21492151.CrossRefGoogle Scholar
LANGAND, J., THÉRON, A., POINTIER, J. P., DELAY, B. & JOURDANE, J. (1999). Population structure of Biomphalaria glabrata, intermediate host of Schistosoma mansoni in Guadeloupe Island, using RAPD markers. Journal of Molluscan Studies 65, 425433.CrossRefGoogle Scholar
LESLIE, J. F., CAIN, G. G., MEFFE, G. K. & VRIJENHOEK, R. C. (1982). Enzyme polymorphism in Ascaris suum (Nematoda). Journal of Parasitology 68, 576587.CrossRefGoogle Scholar
LYDEARD, C., MULVEY, M., AHO, J. M. & KENNEDY, P. K. (1989). Genetic variability among natural populations of the liver fluke, Fascioloides magna, in the white-tailed deer, Odocoileus virginianus. Canadian Journal of Zoology 67, 20212025.CrossRefGoogle Scholar
MANNING, S. D., WOOLHOUSE, M. E. J. & NDAMBA, J. (1995). Geographic compatibility of the freshwater snail Bulinus globosus and schistosomes from the Zimbabwe highveld. International Journal for Parasitology 25, 3742.CrossRefGoogle Scholar
MCCUTCHAN, T. F., SIMPSON, A. J., MULLINS, J. A., SHER, A., NASH, T. E., LEWIS, F. & RICHARDS, C. (1984). Differenciation of schistosomes by species, strain, and sex by using coled DNA markers. Proceedings of the National Academy of Sciences, USA 81, 889893.CrossRefGoogle Scholar
MINCHELLA, D. J., LEWIS, F. A., SOLLENBERGER, K. M. & WILLIAMS, J. A. (1994). Genetic diversity of Schistosoma mansoni. Molecular and Biochemical Parasitology 68, 307313.CrossRefGoogle Scholar
MINCHELLA, D. J., SOLLENBERGER, K. M. & PEREIRA DESOUSA, C. (1995). Distribution of schistosome genetic diversity within molluscan intermediate hosts. Parasitology 111, 217220.CrossRefGoogle Scholar
MULVEY, M., AHO, J. M., LYDEARD, C., LEBERG, P. L. & SMITH, M. H. (1991). Comparative population genetic structure of a parasite (Fascioloides magna) and its definitive host. Evolution 45, 16281640.Google Scholar
NADLER, S. A. (1990). Molecular approaches to studying helminth population genetics and phylogeny. International Journal for Parasitology 20, 1129.CrossRefGoogle Scholar
NADLER, S. A., LINDQUIST, R. L. & NEAR, T. J. (1995). Genetic structure of midwestern Ascaris suum populations: a comparison of isoenzyme and RAPD markers. Journal of Parasitology 81, 385394.CrossRefGoogle Scholar
NADLER, S. A. (1995). Microevolution and the genetic structure of parasite populations. Journal of Parasitology 81, 395403.CrossRefGoogle Scholar
NADLER, S. A. (1996). Microevolutionary patterns and molecular markers: the genetics of geographic variation in Ascaris suum. Journal of Nematology 28, 277285.Google Scholar
RAYMOND, M. & ROUSSET, F. (1995). GENEPOP v1.2, a population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248249.Google Scholar
SIMPSON, A. J. G., DIAS NETO, E., JOHNSTON, D. A., KAUKAS, A. & ROLLINSON, D. (1993). Recent molecular approach to the study of schistosome genetics. Experimental Parasitology 77, 376379.CrossRefGoogle Scholar
SIRE, C., DURAND, P., POINTIER, J. P. & THÉRON, A. (1999). Genetic diversity and recruitment pattern of Schistosoma mansoni in a Biomphalaria glabrata snail population: a field study using random-amplified polymorphic DNA markers. Journal of Parasitology 85, 436441.CrossRefGoogle Scholar
TER BRAAK, C. J. F. (1990). CANOCO – a FORTRAM program for canonical community ordination by [partial] [detrended] [canonical] correspondence analysis, principal components analysis and redundancy analysis. Microcomputer Power, Ithaca, New York.
THÉRON, A., POINTIER, J. P., MORAND, S., IMBERT-ESTABLET, D. & BOREL, G. (1992). Long-term dynamics of natural populations of Schistosoma mansoni among Rattus rattus in patchy environment. Parasitology 104, 291298.CrossRefGoogle Scholar
VIEIRA, L. Q., CORREA-OLIVEIRA, R., KATZ, N., DE SOUZA, C. P., CARVALHO, O. S., ARAUJO, N., SHER, A. & BRINDLEY, P. J. (1991). Genomic variability in field populations of S. mansoni in Brazil as detected with a ribosomal gene probe. American Journal of Tropical and Medical Hygiene 44, 6978.Google Scholar