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Inter-specific parasite competition: mixed infections of Schistosoma mansoni and S. rodhaini in the definitive host

Published online by Cambridge University Press:  24 January 2008

A. J. NORTON*
Affiliation:
Department of Infectious Disease Epidemiology, Imperial College Faculty of Medicine, London W2 1PG, UK Department of Zoology, The Natural History Museum, London SW7 5BD, UK
J. P. WEBSTER
Affiliation:
Department of Infectious Disease Epidemiology, Imperial College Faculty of Medicine, London W2 1PG, UK
R. A. KANE
Affiliation:
Department of Zoology, The Natural History Museum, London SW7 5BD, UK
D. ROLLINSON
Affiliation:
Department of Zoology, The Natural History Museum, London SW7 5BD, UK
*
*Corresponding author: Department of Infectious Disease Epidemiology, Imperial College Faculty of Medicine, London W2 1PG, UK. Tel: +0207 594 3819. Fax: +0207 402 3927. E-mail: alice.norton@imperial.ac.uk

Summary

Competition between parasite species has been predicted to be an important force shaping parasite and host ecology and evolution, although empirical data are often lacking. Using the Mus musculus-Schistosoma mansoni and Schistosoma rodhaini host-parasite systems we characterized mate choice and inter-specific competition between these two schistosome species. Simultaneous infections revealed species-specific mate preferences for both species as well as suggesting mating competition, with male S. rodhaini appearing dominant over male S. mansoni. S. rodhaini homologous pairs were also shown to have increased reproduction per paired female in the presence of a competitor in simultaneous infections. Overall total reproductive success was, however, similar between the two species under conditions of direct competition due to the greater initial infectivity of S. mansoni in comparison to S. rodhaini. Inter-specific competition was also implicated as increased parasite virulence to the host. The potential effects of such interactions on parasite and host ecology and evolution in nature are discussed.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2008

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References

REFERENCES

Bremond, P., Theron, A. and Rollinson, D. (1989). Hybrids between Schistosoma mansoni and S. rodhaini: characterization by isoelectric focusing of six enzymes. Parasitology Research 76, 138145.CrossRefGoogle ScholarPubMed
Cosgrove, C. L. and Southgate, V. R. (2002). Mating interactions between Schistosoma mansoni and S. margrebowiei. Parasitology 125, 233243.Google ScholarPubMed
Cosgrove, C. L. and Southgate, V. R. (2003 a). Competitive mating interactions between Schistosoma haematobium and S. intercalatum (Lower Guinea strain). Parasitology Research 89, 238241.CrossRefGoogle ScholarPubMed
Cosgrove, C. L. and Southgate, V. R. (2003 b). Interactions between Schistosoma intercalatum (Zaire strain) and S. mansoni. Journal of Helminthology 77, 209218.CrossRefGoogle ScholarPubMed
Davies, C. M., Webster, J. P. and Woolhouse, M. E. J. (2001). Trade-offs in the evolution of virulence of schistosomes-macroparasites with an indirect life-cycle. Proceedings of the Royal Society of London, B 268, 17.CrossRefGoogle Scholar
Gentile, R., Costa-Neto, S. F., Goncalves, M. L., Bonecker, S. T., Fernandes, F. A., Garcia, J. S., Barreto, M. G. M., Soares, M. S., D'andrea, P. S., Peralta, J. M. and Rey, L. (2006). An ecological field study of the water-rat Nectomys squamipes as a wild reservoir indicator of Schistosoma mansoni transmission in an endemic area. Memórias do Instituto Oswaldo Cruz 101, 111117.Google Scholar
Gower, C. M., Shrivastava, J., Lamberton, P. H., Rollinson, D., Webster, B. L., Emery, A., Kabetereine, B. and Webster, J. P. (2007). Development and application of an ethically and epidemiologically advantageous assay for the multi-locus microsatellite analysis of Schistosoma mansoni. Parasitology 134, 523536.CrossRefGoogle ScholarPubMed
Gower, C. M. and Webster, J. P. (2005). Intraspecific competition and the evolution of virulence in a parasitic trematode. Evolution; International Journal of Organic Evolution 59, 544553.Google Scholar
Kane, R. A., Bartley, J., Stothard, R. J., Vercruysee, J., Rollinson, D. and Southgate, V. R. (2002). Application of single strand conformational polymorphism (SSCP) analysis with fluorescent primers for differentiation of Schistosoma haematobium group species. Transactions of the Royal Society of Tropical Medicine and Hygiene 96 (Suppl.), 235241.CrossRefGoogle ScholarPubMed
King, C. H., Dickman, K. and Tisch, D. (2005). Reassessment of the cost of chronic helminthic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. The Lancet 365, 15611569.CrossRefGoogle ScholarPubMed
Le Roux, P. L. (1954 a). Hybridisation of Schistosoma mansoni and Schistosoma rodhaini. Transactions of the Royal Society of Tropical Medicine and Hygiene 48, 34.Google Scholar
Le Roux, P. L. (1954 b). Hybridisation of Schistosoma mansoni and Schistosoma rodhaini. Transactions of the Royal Society for Tropical Medicine and Hygiene 48, 34.Google Scholar
Liberatos, J. D. (1987). Schistosoma mansoni: male-biased sex ratios in snails and mice. Experimental Parasitology 64, 165177.CrossRefGoogle ScholarPubMed
Lockyer, A. E., Olson, P. D., Ostergaard, P., Rollinson, D., Johnston, D. A., Attwood, S. W., Southgate, V. R., Horak, P., Snyder, S. D., Le, T. H., Agatsuma, T., McManus, D. P., Carmichael, A. C., Naem, S. and Littlewood, D. T. J. (2003). The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126, 203224.CrossRefGoogle ScholarPubMed
Morgan, J. A., Dejong, R. J., Lwambo, N. J., Mungai, B. N., Mkoji, G. M. and Loker, E. S. (2003 a). First report of a natural hybrid between Schistosoma mansoni and S. rodhaini. Journal of Parasitology 89, 416418.CrossRefGoogle ScholarPubMed
Morgan, J. A. T., Dejong, R. J., Kazibwe, F., Mkoji, G. M. and Loker, E. S. (2003 b). A newly-identified lineage of Schistosoma. International Journal for Parasitology 33, 977985.CrossRefGoogle ScholarPubMed
Pitchford, R. J. (1977). A check list of definitive hosts exhibiting evidence of the genus Schistosoma Weinland, 1858 acquired naturally in Africa and the Middle East. Journal of Helminthology 51, 229252.CrossRefGoogle ScholarPubMed
Smithers, S. R. and Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55, 695700.CrossRefGoogle ScholarPubMed
Southgate, V. R., Jourdane, J. and Tchuente, L. A. (1998). Recent studies on the reproductive biology of the schistosomes and their relevance to speciation in the Digenea. International Journal for Parasitology 28, 11591172.CrossRefGoogle ScholarPubMed
Southgate, V. R., Tchuem Tchuente, L. A., Vercruysse, J. and Jourdane, J. (1995). Mating behaviour in mixed infections of Schistosoma haematobium and S. mattheei. Parasitology Research 81, 651656.CrossRefGoogle ScholarPubMed
Steinauer, M. L., Mkoji, G. M. and Loker, E. S. (2006). Schistosoma mansoni and Schistosoma rodhaini in western Kenya: a study of species boundaries. American Journal of Tropical Medicine and Hygiene 75, 212 (Abstract).Google Scholar
Stothard, J. R. and Rollinson, D. (1997). Partial DNA sequences from the mitochondrial cytochrome oxidase subunit 1 (CO1) gene can differentiate the intermediate snail hosts Bulinus globosus and B. nasutus (Gastropoda: Planorbidae). Journal of Natural History 31, 727737.CrossRefGoogle Scholar
Tchuem Tchuente, L. A., Southgate, V. R., Imbert-Establet, D. and Jourdane, J. (1995). Change of mate and mating competition between males of Schistosoma intercalatum and S. mansoni. Parasitology 110, 4552.CrossRefGoogle ScholarPubMed
Theron, A. (1984 a). Early and late shedding patterns of Schistosoma mansoni cercariae: ecological significance in transmission to human and murine hosts. Journal of Parasitology 70, 652655.CrossRefGoogle ScholarPubMed
Theron, A. (1984 b). Early and late shedding patterns of Schistosoma mansoni cercariae: ecological significance in transmission to human and murine hosts. Journal of Parasitology 70, 652655.CrossRefGoogle ScholarPubMed
Theron, A. (1989). Hybrids between Schistosoma mansoni and S. rodhaini: characterization by cercarial emergence rhythms. Parasitology 99, 225228.CrossRefGoogle ScholarPubMed
Theron, A. and Combes, C. (1995). Asynchrony of infection timing, habitat preference, and sympatric speciation of Schistosome parasites. Evolution 49, 372375.CrossRefGoogle ScholarPubMed
Ulmer, M. J. (1970). Notes on rearing snails in the laboratory. In Experiments and Techniques in Parasitology (ed. MacInnis, A. J. and Voge, M.), W. H. Freeman and Company, San Francisco.Google Scholar
Webster, B. L., Southgate, V. R. and Tchuem Tchuente, L. A. (1999). Mating interactions between Schistosoma haematobium and S. mansoni. Journal of Helminthology 73, 351356.CrossRefGoogle ScholarPubMed
Webster, B. L., Tcheum Tchuente, L. A. and Southgate, V. R. (2007). A single-strand conformation polymorphism (SSCP) approach for investigating genetic interactions of Schistosoma haematobium and Schistosoma guineensis in Loum, Cameroon. Parasitology Research 100, 739745.CrossRefGoogle ScholarPubMed
Woolhouse, M. E. J., Taylor, L. H. and Haydon, D. T. (2001). Population biology of multihost pathogens. Science 292, 11091112.Google ScholarPubMed
Wright, C. A. and Southgate, V. R. (1976). Hybridization of schistosomes and some of its implications. In Genetic Aspects of Host-Parasite Relationships (ed. Taylor, A. E. R. and Muller, R.), pp. 5586. Blackwell Scientific, Oxford.Google Scholar