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Schistosome genetic diversity: the implications of population structure as detected with microsatellite markers

Published online by Cambridge University Press:  15 March 2004

J. CURTIS
Affiliation:
Biology/Chemistry Section, Purdue University North Central, Westville, IN 46391, USA
R. E. SORENSEN
Affiliation:
Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USA
D. J. MINCHELLA
Affiliation:
Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USA

Abstract

Blood flukes in the genus Schistosoma are important human parasites in tropical regions. A substantial amount of genetic diversity has been described in populations of these parasites using molecular markers. We first consider the extent of genetic variation found in Schistosoma mansoni and some factors that may be contributing to this variation. Recently, though, attempts have been made to analyze not only the genetic diversity but how that diversity is partitioned within natural populations of schistosomes. Studies with non-allelic molecular markers (e.g. RAPDs and mtVNTRs) have indicated that schistosome populations exhibit varying levels of gene flow among component subpopulations. The recent characterization of microsatellite markers for S. mansoni provided an opportunity to study schistosome population structure within a population of schistosomes from a single Brazilian village using allelic markers. Whereas the detection of population structure depends strongly on the type of analysis with a mitochondrial marker, analyses with a set of seven microsatellite loci consistently revealed moderate genetic differentiation when village boroughs were used to define parasite subpopulations and greater subdivision when human hosts defined subpopulations. Finally, we discuss the implications that such strong population structure might have on schistosome epidemiology.

Type
Research Article
Copyright
© 2002 Cambridge University Press

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References

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
BIEBERICH, A. A. & MINCHELLA, D. J. (2001). Mitochondrial inheritance in Schistosoma mansoni: mtVNTR mutation produces noise on top of the signal. Journal of Parasitology 87, 10111015.CrossRefGoogle Scholar
BIRKY, C. W. JR., FUERST, P. & MARUYAMA, T. (1989). Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121, 613627.Google Scholar
BRINDLEY, P. J., LEWIS, F. A., MCCUTCHAN, T. F., BUEDING, E. & SHER, A. (1989). A genomic change associated with the development of resistance to hycanthone in Schistosoma mansoni. Molecular and Biochemical Parasitology 36, 243252.CrossRefGoogle Scholar
BROUWER, K. C., NDHLOVU, P., MUNATSI, A. & SHIFF, C. J. (2001). Genetic diversity of a population of Schistosoma haematobium derived from schoolchildren in east central Zimbabwe. Journal of Parasitology 87, 762769.CrossRefGoogle Scholar
CURTIS, J., FRAGA, L. A., DE SOUZA, C. P., CORREA-OLIVEIRA, R. & MINCHELLA, D. J. (2001a). Widespread heteroplasmy in schistosomes makes a mtVNTR marker ‘nearsighted’. Journal of Heredity 92, 248253.Google 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
CURTIS, J., SORENSEN, R. E., PAGE, L. K. & MINCHELLA, D. J. (2001b). Microsatellite loci in the human blood fluke Schistosoma mansoni and their utility for other schistosome species. Molecular Ecology Notes 1, 143145.Google Scholar
DABO, A., DURAND, P., MORAND, S., DIAKITE, M., LANGAND, J., IMBERT-ESTABLET, D., DOUMBO, O. & JOURDANE, J. (1997). Distribution 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., KRUGER, 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
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
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
EPPERT, A., LEWIS, F. A., GRZYWACZ, C., COURA-FILHO, P. & MINCHELLA, D. J. (2002). Distribution of schistosome infections in molluscan hosts at different levels of parasite prevalence. Journal of Parasitology 88, 232236.CrossRefGoogle Scholar
ESTOUP, A. & CORNUET, J. (1999). Microsatellite evolution: inferences from population data. In Microsatellites: Evolution and Applications (ed. GOLDSTEIN, D. B. & SCHLÖTTERER, C.), pp. 4965.
FENG, Z., CURTIS, J. & MINCHELLA, D. J. (2001). The influence of drug treatment on the maintenance of schistosome genetic diversity. Journal of Mathematical Biology 43, 5268.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
LEWONTIN, R. C. (1972). The apportionment of human diversity. Evolutionary Biology 6, 381398.CrossRefGoogle Scholar
LOUGHEED, S. C., GIBBS, H. L., PRIOR, K. A. & WEATHERHEAD, P. J. (2000). A comparison of RAPD versus microsatellite DNA markers in population studies of the massasauga rattlesnake. Journal of Heredity 91, 458463.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
MICHALAKIS, Y. & EXCOFFIER, L. (1996). A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142, 10601064.Google Scholar
MINCHELLA, D. J., LEWIS, F. A., SOLLENBERGER, K. M. & WILLIAMS, J. A. (1994). Genetic diversity of Schistosoma mansoni: quantifying strain heterogeneity using a polymorphic DNA element. Molecular and Biochemical Parasitology 68, 307313.CrossRefGoogle Scholar
MINCHELLA, D. J., SOLLENBERGER, K. M. & DE SOUZA, C. P. (1995). Distribution of schistosome genetic diversity within molluscan intermediate hosts. Parasitology 111, 217220.CrossRefGoogle Scholar
NADLER, S. (1995). Microevolution and the genetic structure of parasite populations. Journal of Parasitology 81, 395403.CrossRefGoogle Scholar
ROLLINSON, D. (1986). Schistosoma mansoni from naturally infected Rattus rattus in Guadeloupe: identification, prevalence and enzyme polymorphism. Parasitology 93, 3953.CrossRefGoogle Scholar
ROUSSET, F. & RAYMOND, M. (1995). Testing heterozygote excess and deficiency. Genetics 140, 14131419.Google Scholar
SAMBROOK, J., FRITSCH, E. F. & MANIATIS, T. (1989). Molecular Cloning: A Laboratory Manual.
SENE, M., BRÉMOND, P., HERVE, J. P., SOUTHGATE, V. R., SELLIN, B., MARCHAND, B. & DUPLANTIER, J. M. (1997). Comparison of human and murine isolates of Schistosoma mansoni from Richard-Toll, Senegal, by isoelectric focusing. Journal of Helminthology 71, 175181.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
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, 545554.CrossRefGoogle Scholar
SLATKIN, M. (1985). Rare alleles as indicators of gene flow. Evolution 39, 5365.CrossRefGoogle Scholar
SLATKIN, M. (1995). Gene flow and the geographic structure of natural populations. Science 236, 787792.Google Scholar
SORENSEN, R. E., CURTIS, J. & MINCHELLA, D. J. (1998). Intraspecific variation in the rDNA ITS loci of 37-collar-spined echinostomes from North America: implications for sequence-based diagnoses and phylogenetics. Journal of Parasitology 84, 992997.CrossRefGoogle Scholar
SPOTILA, L. D., REKOSH, D. M. & LOVERDE, P. T. (1991). Polymorphic repeated DNA element in the genome of Schistosoma mansoni. Molecular and Biochemical Parasitology 48, 117120.CrossRefGoogle Scholar
VAN VALEN, L. (1973). A new evolutionary law. Evolutionary Theory 1, 130.Google Scholar
WEIR, B. S. & COCKERHAM, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 13581370.Google Scholar
WRIGHT, S. (1969). Evolution and the Genetics of Populations, Volume 2. The Theory of Gene Frequencies.
WRIGHT, S. (1978). Evolution and the Genetics of Populations, Volume 4. Variability Within and Among Natural Populations.