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Molecular ecology of Schistosoma mansoni transmission inferred from the genetic composition of larval and adult infrapopulations within intermediate and definitive hosts

Published online by Cambridge University Press:  05 October 2004

A. THERON
Affiliation:
Parasitologie Fonctionnelle et Evolutive, UMR 5555 CNRS-UP, CBETM, Université, 52 Av. Paul Alduy, 66860 Perpignan Cedex, France
C. SIRE
Affiliation:
Parasitologie Fonctionnelle et Evolutive, UMR 5555 CNRS-UP, CBETM, Université, 52 Av. Paul Alduy, 66860 Perpignan Cedex, France
A. ROGNON
Affiliation:
Parasitologie Fonctionnelle et Evolutive, UMR 5555 CNRS-UP, CBETM, Université, 52 Av. Paul Alduy, 66860 Perpignan Cedex, France
F. PRUGNOLLE
Affiliation:
Centre d'Etude du Polymorphisme des Micro-organismes, Equipe ESS, UMR 9926 CNRS-IRD, 911 av. Agropolis, BP 5045, 34032 Montpellier, France
P. DURAND
Affiliation:
Centre d'Etude du Polymorphisme des Micro-organismes, Equipe ESS, UMR 9926 CNRS-IRD, 911 av. Agropolis, BP 5045, 34032 Montpellier, France

Abstract

We investigated the genotypic composition of the digenetic parasite Schistosoma mansoni for its adult stages within the definitive host (the wild rat, Rattus rattus) and for the larval stages within the intermediate host (the snail, Biomphalaria glabrata) both collected at the same transmission site. Our analyses are based upon the recognition and distribution of 200 different multilocus genotypes generated by RAPD markers. While intramolluscan larval infrapopulations are characterized by a low infection rate (0·6% on average) and low intra-host genetic diversity (1·1 genotype on average per infected snail), adult infrapopulations within rats showed a high infection rate (94%) and a substantial intra-host genetic diversity (34 genotypes on average) linked to high intensities (160 worms per host on average). A single definitive host bearing 105 different genotypes harboured 52% of the total genetic diversity detected within the whole parasite population. Analysis of the genetic data allowed the identification of various ecological, behavioural and immunological factors which are likely to enhance transmission of multiple parasite genotypes towards the vertebrate hosts. From the distribution of repeated identical multilocus genotypes within the parasite population and among the hosts, we have inferred different parameters of the cercarial transmission efficiency as well as patterns and processes by which vertebrate hosts acquire infection in the field.

Type
Research Article
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

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
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
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
BROUWER, K. C., NDHLOVU, P., MUNATSI, A. & SHIFF, C. J. ( 2001). Genetic diversity of a population of Schistosoma haematobium derived from school children in East Central Zimbabwe. Journal of Parasitology 84, 762769.CrossRefGoogle Scholar
CURTIS, J. & MINCHELLA, D. J. ( 2000). Schistosome population genetic structure: When clumping worms is not just splitting hairs. Parasitology Today 16, 7073.CrossRefGoogle Scholar
CURTIS, J., SORENSEN, R. E. & MINCHELLA, D. J. ( 2002). Schistosome genetic diversity: the implications of population structure as detected with microsatellite markers. Parasitology 125, S51S59.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
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
EPPERT, A., LEWIS, F. A., GRZYWACZ, C., COURA-FILHO, P., CALDAS, I. & MINCHELLA, D. J. ( 2002). Distribution of schistosome infections in molluscan hosts at different levels of parasite prevalence. Journal of Parasitology 88, 232236.CrossRefGoogle Scholar
MINCHELLA, D. J., SOLLENBERGER, K. M. & PEREIRA DE SOUZA, 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. ( 1995). Microevolution and the genetic structure of parasite populations. Journal of Parasitology 81, 395403.CrossRefGoogle Scholar
PATERSON, S., FISHER, M. C. & VINEY, M. E. ( 2000). Inferring infection processes of a parasitic nematode using population genetics. Parasitology 120, 185194.CrossRefGoogle Scholar
POINTIER, J.-P. & THERON, A. ( 1979). La schistosomose intestinale dans les forêts marécageuses à Pterocarpus de Guadeloupe: Ecologie du mollusque vecteur Biomphalaria glabrata et de son parasite Schistosoma mansoni. Annales de Parasitologie 54, 4356.CrossRefGoogle Scholar
POULIN, R. ( 1993). The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23, 937944.CrossRefGoogle Scholar
POULIN, R. ( 1998). Evolutionary Ecology of Parasites. Chapman and Hall, London.
PRUGNOLLE, F., DE MEEUS, T., DURAND, P., SIRE, C. & THÉRON, A. ( 2002). Sex-specific structure in Schistosoma mansoni: evolutionary and epidemiological implications. Molecular Ecology 11, 12311238.CrossRefGoogle Scholar
SIRE, C., ROGNON, A. & THERON, A. ( 1998). Failure of Schistosoma mansoni to reinfect Biomphalaria glabrata snails: acquired humoral resistance or intra-specific larval antagonism? Parasitology 117, 117122.Google 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., DURAND, P., POINTIER, J.-P. & THÉRON, A. ( 2001 a). Genetic diversity of Schistosoma mansoni within and between individual hosts (Rattus rattus): infrapopulation differentiation at microspatial scale. International Journal for Parasitology 31, 16091616.Google Scholar
SIRE, C., LANGAND, J., BARRAL, V. & THÉRON, A. ( 2001 b). Parasite (Schistosoma mansoni) and host (Biomphalaria glabrata) genetic diversity: population structure in a fragmented landscape. Parasitology 122, 545554.Google Scholar
THÉRON, A., PAGÈS, J. R. & ROGNON, A. ( 1997). Schistosoma mansoni: distribution patterns of miracidia among Biomphalaria glabrata snail hosts as related to host susceptibility and sporocyst regulation process. Experimental Parasitology 85, 19.Google Scholar
THÉRON, A. & POINTIER, J.-P. ( 1995). Ecology, dynamics, genetics and divergence of trematode populations in heterogenous environments: the model of Schistosoma mansoni in the insular focus of Guadeloupe. Research and Review in Parasitology 55, 4964.Google Scholar