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Development and application of an ethically and epidemiologically advantageous assay for the multi-locus microsatellite analysis of Schistosoma mansoni

  • C. M. GOWER (a1) (a2), J. SHRIVASTAVA (a1), P. H. L. LAMBERTON (a1), D. ROLLINSON (a2), B. L. WEBSTER (a2), A. EMERY (a2), N. B. KABATEREINE (a3) and J. P. WEBSTER (a1)
  • DOI:
  • Published online: 13 November 2006

Non-availability of adult worms from living hosts remains a key problem in population genetic studies of schistosomes. Indirect sampling involving passage through laboratory animals presents significant ethical and practical drawbacks, and may result in sampling biases such as bottlenecking processes and/or host-induced selection pressures. The novel techniques reported here for sampling, storage and multi-locus microsatellite analysis of larval Schistosoma mansoni, allowing genotyping of up to 7 microsatellite loci from a single larva, circumvent these problems. The utility of these assays and the potential problems of laboratory passage, were evaluated using 7 S. mansoni population isolates collected from school-children in the Hoima district of Uganda, by comparing the associated field-collected miracidia with adult worms and miracidia obtained from a single generation in laboratory mice. Analyses of laboratory-passaged material erroneously indicated the presence of geographical structuring in the population, emphasizing the dangers of indirect sampling for population genetic studies. Bottlenecking and/or other sampling effects were demonstrated by reduced variability of adult worms compared to their parent field-collected larval samples. Patterns of heterozygote deficiency were apparent in the field-collected samples, which were not evident in laboratory-derived samples, potentially indicative of heterozygote advantage in establishment within laboratory hosts. Genetic distance between life-cycle stages in the majority of isolates revealed that adult worms and laboratory-passaged miracidia clustered together whilst segregating from field miracidia, thereby further highlighting the utility of this assay.

Corresponding author
Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College (St Mary's Campus), Norfolk Place, London W2 1PG, UK. Tel: +44 (0) 20 7594 3819. Fax: +44 (0) 207 402 3927. E-mail:
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Blair, L., Webster, J. P. and Barker, G. C. ( 2001). Isolation and characterisation of polymorphic microsatellite markers in Schistosoma mansoni from Africa. Molecular Ecology Notes1, 9395.

Brouwer, K. C., Ndhlovu, P., Munatsi, A. and Shiff, C. J. ( 2001). Genetic diversity of a population of Schistosoma haematobium derived from schoolchildren in east central Zimbabwe. Journal of Parasitology87, 762769.

Chitsulo, L., Engels, D., Montressor, A. and Savioli, L. ( 2000). The global status of schistosomiasis and its control. Acta Tropica77, 4151.

Cohen, L. M. and Eveland, L. K. ( 1988). Schistosoma mansoni: characterisation of clones maintained by the microsurgical transplantation of sporocysts. Journal of Parasitology74, 963969.

Curtis, J. and Minchella, D. J. ( 2000). Schistosome population genetic structure: when clumping worms is not just splitting hairs. Parasitology Today16, 6871.

Curtis, J., Sorensen, R. E. and Minchella, D. J. ( 2002). Schistosome genetic diversity: the implications of population structure as detected with microsatellite markers. Parasitology125, S51S59.

Curtis, J., Sorensen, R. E., Page, L. K. and Minchella, D. J. ( 2001). Microsatellite loci in the human blood fluke Schistosoma mansoni and their utility for other schistosome species. Molecular Ecology Notes1, 143145.

Davies, C. M., Webster, J. P., Kruger, O., Munatsi, A., Ndamba, J. and Woolhouse, M. E. J. ( 1999). Host-parasite population genetics: a cross-sectional comparison of Bulinus globosus and Schistosoma haematobium. Parasitology119, 295302.

Davies, C. M., Webster, J. P. and Woolhouse, M. E. ( 2001). Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite. Proceedings of the Royal Society of London, B268, 251257.

Durand, P., Sire, C. and Theron, A. ( 2000). Isolation of microsatellite markers in the digenetic trematode Schistosoma mansoni from Guadeloupe island. Molecular Ecology9, 997998.

Guo, S. and Thompson, E. ( 1992). Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics48, 361372.

Kumar, S., Tamura, K. and Nei, M. ( 2004). MEGA3: integrated software for Molecular Evolutionary Genetic Analysis and sequence alignment. Briefings in Bioinformatics5, 150163.

Loverde, P. T., Dewald, J., Minchella, D. J., Bosshardt, S. C. and Damian, R. T. ( 1985). Evidence for host-induced selection in Schistosoma mansoni. Journal of Parasitology71, 297301.

Manning, S. D., Woolhouse, M. E. J. and Ndamba, J. ( 1995). Geographic compatibility of the freshwater snail Bulinus globusus and schistosomes from the Zimbabwe Highveld. International Journal for Parasitology25, 3742.

Morand, S., Manning, S. D. and Woolhouse, M. E. J. ( 1996). Parasite-host coevolution and geographic patterns of parasite infectivity and host susceptibility. Proceedings of the Royal Society of London, B263, 119128.

Prugnolle, F., De Meeus, T., Durand, P., Sire, C. and Theron, A. ( 2002). Sex-specific genetic structure in Schistosoma mansoni: evolutionary and epidemiological implications. Molecular Ecology11, 12311238.

Prugnolle, F., Choisy, M., Theron, A., Durand, P. and De Meeus, T. ( 2004). Sex-specific correlation between heterozygosity and clone size in the trematode Schistosoma mansoni. Molecular Ecology13, 28592864.

Rodrigues, N. B., Filho, P. C., Souza, C. P., Passos, L. K. J., Dias-Neto, E. and Romanha, A. J. ( 2002). Population structure of Schistosoma mansoni assessed by DNA microsatelites. International Journal for Parasitology32, 843851.

Rollinson, D. and Johnston, D. A. ( 1996). Schistosomiasis: a persistent parasitic disease. Interdisciplinary Science Reviews21, 140154.

RosenbergN. A., Pritchard, J. K., Weber, J. L., Cann, H. M., Kidd, K. K., Zhivotovsky, L. A. and Feldman, M. W. ( 2002). Genetic structure of human populations. Science298, 23812383.

Shrivastava, J., Barker, G. C., Johansen, M. V., Xiaonong, Z., Aligui, G. D., Mcgarvey, S. T. and Webster, J. P. ( 2003). Isolation and characterisation of polymorphic DNA microsatellite markers from Schistosoma japonicum. Molecular Ecology Notes3, 406408.

Sire, C., Durand, P., Pointier, J. P. and Theron, 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 Parasitology85, 436441.

Sire, C., Durand, P., Pointier, J. P. and Theron, A. ( 2001). Genetic diversity of Schistosoma mansoni within and among individual hosts (Rattus rattus): infrapopulation differentiation at microspatial scale. International Journal for Parasitology31, 16091616.

Stohler, R. A., Curtis, J. and Minchella, D. J. ( 2004). A comparison of microsatellite polymorphism and heterozygosity among field and laboratory populations of Schistosoma mansoni. International Journal for Parasitology34, 595610.

Thiongo, F. W., Madsen, H., Ouma, J. H., Andreassen, J. and Christensen, N. O. ( 1997). Host-parasite relationships in infections with two Kenyan isolates of Schistosoma mansoni in NMRI mice. Journal of Parasitology83, 330332.

Thompson, J. N. ( 1994). The Coevolutionary Process. Chicago University Press, Chicago.

Webster, J. P., Gower, C. M. and Blair, L. ( 2004). Do hosts and parasites coevolve?: empirical support from the Schistosoma system. American Naturalist164, S33S51.

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