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Interactions between Schistosoma intercalatum (Zaire strain) and S. mansoni

Published online by Cambridge University Press:  12 April 2024

C.L. Cosgrove
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, The Natural History Museum, Cromwell Road, South Kensington, London, SW7 5BD, UK
V.R. Southgate*
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, The Natural History Museum, Cromwell Road, South Kensington, London, SW7 5BD, UK
*
*Author for correspondence Fax: +44 942 5518 E-mail: V.Southgate@nhm.ac.uk

Abstract

Schistosoma mansoni and S. intercalatum, two schistosomes from different evolutionary lineages, are parasitic in humans and therefore able to co-infect the same host where they occur sympatrically in Africa. Previous studies of mating interactions between these species in mice, using the Lower Guinea strain of S. intercalatum, have demonstrated the competitive dominance of S. mansoni over S. intercalatum in terms of pairing ability, which is potentially an important mechanism restricting the distribution of S. intercalatum in Africa. The study presented here examines the mating interactions in mice between S. mansoni and the Zaire (Democratic Republic of Congo) strain of S. intercalatum, which differs from the Lower Guinea strain in many biological characteristics. Analysis of the data showed a preponderance of intraspecific pairs over interspecific, demonstrating a specific mate preference system for both species. Mating competition between these species and the ability of males of both species to effect a change of mate by pulling paired females away from their partners was indicated. Comparisons are made between the competitive mating abilities of both strains of S. intercalatum relative to those of S. mansoni, with the data suggesting that S. mansoni is competitively dominant to S. intercalatum (Zaire) in sequential infections but to a lesser extent than for S. intercalatum (Lower Guinea). Additional factors which may contribute to the confinement of S. intercalatum (Zaire) to the Democratic Republic of Congo are discussed.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2003

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References

Browne, S.G. (1969)In: discussion of Webbe,G. (1969) Progress in the control of schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 63(Suppl.4), 82.Google Scholar
Chesterman, C.C. (1923)Note sur la bilharziose de la région de Stanleyville (Congo Belge). Annales de la Société Belge de Médecine Tropicale 3, 73 Google Scholar
Clapier, P. (1923) Schistososoma hematobium in Libreville, Gabon. Ectopic bilharziasis. Bulletin de la Société de Pathologie Exotique 16, 559 Google Scholar
Cosgrove, C.L. & Southgate, V.R. (2002) Mating interactions between. Schistosoma mansoniandS. margrebowiei . Parasitology 125, 233243.CrossRefGoogle ScholarPubMed
De Clercq, D. (1987) La situation malacologique à Kinshasa et description d'un foyer autochtone de schistosomiase à.Schistosoma intercalatum . Annales de la Société Belge de Médecine Tropicale 67, 345352.Google ScholarPubMed
Deschiens, R. & Delas, A. (1969) L'extension geographique de la bilharziose à Schistosoma intercalatum en Afrique tropicale. Transactions of the Royal Society of Tropical Medicine and Hygiene 63(suppl. 4), 5765.CrossRefGoogle Scholar
Desprès, L., Imbert-Establet, D., Combes, C. & Bonhomme, F. (1992) Molecular evidence linking hominid evolution to recent radiation of schistosomes (Platyhelminthes: Trematoda). Molecular Phylogenetics and Evolution 4, 295304.CrossRefGoogle Scholar
Fisher, A.C. (1934) A study of the schistosomiasis of the Stanleyville District of the Belgian Congo. Transactions of the Royal Society of Tropical Medicine and Hygiene 28, 277306.CrossRefGoogle Scholar
Fletcher, M., LoVerde, P.T. & Woodruff, D.S. (1981) Genetic variation inSchistosoma mansoni: enzyme polymorphisms in populations from Africa, Southwest Asia, South America, and the West Indies. American Journal of Tropical Medicine and Hygiene 30, 406421.CrossRefGoogle Scholar
Frandsen, F. (1977) Investigations of the unimiracidial infection of Schistosoma intercalatum in snails and the infection of the final host using cercariae of one sex. Journal of Helminthology 51, 510.CrossRefGoogle ScholarPubMed
Frandsen, F. (1978) Hybridization between different strains of Schistosoma intercalatum Fisher, 1934 from Cameroun and Zaire. Journal of Helminthology 52, 1122.CrossRefGoogle ScholarPubMed
Frandsen, F. (1979) Studies of the relationships between Schistosoma and their intermediate hosts. I. The genus Bulinus and Schistosoma haematobium from Egypt. Journal of Helminthology 53, 1529.CrossRefGoogle ScholarPubMed
Frandsen, F. (1979) Studies of the relationships between Schistosoma and their intermediate hosts. II. The genus Bulinus and Schistosoma haematobium from Sudan, Zaire and Zambia. Journal of Helminthology 53, 205212.CrossRefGoogle ScholarPubMed
Frandsen, F. (1979) Further studies on the compatibility between Schistosoma intercalatum from Cameroun and Zaire and species of Bulinus . Zeitschrift für Parasitenkunde 58, 161167.CrossRefGoogle ScholarPubMed
Frandsen, F., Bennike, R. & Cridland, C.C. (1978) Studies on Schistosoma intercalatum Fisher, 1934 and its intermediate host in the Kisangani area, Zaire. Annales de la Société Belge de Médecine Tropicale 58, 2131.Google ScholarPubMed
Jourdane, J., Southgate, V.R., Pagès, J.R., Durand, P. & Tchuem Tchuenté, L.A. (2001) Recent studies on Schistosoma intercalatum: taxonomic status, puzzling distribution and transmission foci revisited. Memorias do Instituto Oswaldo Cruz 96(Suppl.), 4548.CrossRefGoogle ScholarPubMed
Khalil, S.B. & Mansour, N.S. (1995) Worm development in hamsters infected with unisex and cross-mated with Schistosoma mansoni and Schistosoma haematobium . Journal of Parasitology 81, 811.CrossRefGoogle ScholarPubMed
Liberatos, J.D. (1987) Schistosoma mansoni: male-biased sex ratios in snails and mice. Experimental Parasitology 64, 165177.CrossRefGoogle ScholarPubMed
Loker, E.S. (1983) A comparative study of the life-histories of mammalian schistosomes. Parasitology 87, 343369.CrossRefGoogle ScholarPubMed
Mantel, N. & Haenszel, W. (1959) Statistical aspects of analysis of data from retrospective studies of disease. Journal of the National Cancer Institute 22, 719748.Google ScholarPubMed
Mitchell, G.F., Garcia, E.G., Wood, S.M., Diasanta, R., Almonte, R., Calica, E., Davern, K.M. & Tiu, W.U. (1990) Studies on the sex ratio of worms in schistosome infections. Parasitology 101, 2734.CrossRefGoogle ScholarPubMed
Pagès, J.R. & Théron, A. (1990) Schistosoma intercalatum from Cameroon and Zaire–chronobiological differentiation of cercarial emergence. Journal of Parasitology 76, 743745.CrossRefGoogle ScholarPubMed
Pagès, J.R., Durand, P., Southgate, V.R., Tchuem Tchuenté, L.A. & Jourdane, J. (2001) Molecular arguments for splitting of Schistosoma intercalatum into two distinct species. Parasitology Research 87, 5762.Google ScholarPubMed
Pagès, J.R., Southgate, V.R., Tchuem Tchuenté, L.A. & Jourdane, J. (2001) Lack of prezygotic isolation by assortative mating between the two cryptic species of the polytypic Schistosoma intercalatum taxon. Parasitology Research 87, 888890.Google ScholarPubMed
Southgate, V.R. (1978) On factors possibly restricting the distribution of Schistosoma intercalatum Fisher, 1934. Zeitschrift für Parasitenkunde 56, 183193.CrossRefGoogle ScholarPubMed
Southgate, V.R. & Knowles, R.J. (1975) Observations on Schistosoma bovis Sonsino, 1876. Journal of Natural History 9, 273314.CrossRefGoogle Scholar
Southgate, V.R., van Wijk, H.B. & Wright, C.A. (1976) Schistosomiasis at Loum, Cameroun; Schistosoma haematobium, S.intercalatum and their natural hybrid. Zeitschrift für Parasitenkunde 49, 145159.CrossRefGoogle ScholarPubMed
Southgate, V.R., Rollinson, D., Ross, G.C. & Knowles, R.J. (1982) Mating behaviour in mixed infections of Schistosoma haematobium andS.intercalatum . Journal of Natural History 16, 491496.CrossRefGoogle Scholar
Southgate, V.R., Jourdane, J. & Tchuem Tchuenté, 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
Tchuem Tchuenté, L.A., Imbert-Establet, D., Delay, B. & Jourdane, J. (1993) Choice of mate, a reproductive isolating mechanism between Schistosoma intercalatum and S.mansoni in mixed infections. International Journal for Parasitology 23, 179185.CrossRefGoogle Scholar
Tchuem Tchuenté, L.A., Imbert-Establet, D., Southgate, V.R. & Jourdane, J. (1994) Interspecific stimulation of parthenogenesis in Schistosoma intercalatum and S.mansoni . Journal of Helminthology 68, 167173.CrossRefGoogle Scholar
Tchuem Tchuenté, L.A., Southgate, V.R., Imbert-Establet, D. & Jourdane, J. (1995) Change of mate and mating competition between males of Schistosoma intercalatum and S.mansoni . Parasitology 110, 4552.CrossRefGoogle ScholarPubMed
Tchuem Tchuenté, L.A., Morand, S., Imbert-Establet, D., Delay, B. & Jourdane, J. (1996) Competitive exclusion in human schistosomes: the restricted distribution of Schistosoma intercalatum . Parasitology 113, 129136.CrossRefGoogle ScholarPubMed
Tchuem Tchuenté, L.A., Southgate, V.R., Vercruysse, J., Kaukas, A., Kane, R., Mulumba, M.P., Pagès, J.R. & Jourdane, J. (1997) Epidemiological and genetic observations on human schistosomiasis in Kinshasa, Zaire. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 263269.CrossRefGoogle ScholarPubMed
Tchuem Tchuenté, L.A., Southgate, V.R., Njiokou, F., Njine, T., Kouemeni, L.E. & Jourdane, J. (1997) The evolution of schistosomiasis at Loum, Cameroon: replacement of Schistosoma intercalatum by S. haematobium through introgressive hybridization. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 664665.CrossRefGoogle Scholar
Webster, B.L., Southgate, V.R. & Tchuem Tchuenté, L.A.(1999) Mating interactions between Schistosoma haematobium and S. mansoni . Journal of Helminthology 73, 351356.CrossRefGoogle ScholarPubMed
Wright, C.A. & Bennett, M.S. (1967) Studies on Schistosoma haematobium in the laboratory.I. A strain from Durban, Natal, South Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 61, 221227.CrossRefGoogle ScholarPubMed
Wright, C.A. & Knowles, R.J. (1972) Studies on Schistosoma haematobium in the laboratory. III. Strains from Iran, Mauritius and Ghana. Transactions of the Royal Society of Tropical Medicine and Hygiene 66, 108118.CrossRefGoogle Scholar
Wright, C.A. & Southgate, V.R. (1976) Hybridization of schistosomes and some of its implications.pp 5586in Taylor, A.E.R. & Muller, R. (Eds) Genetic aspects of host–parasite relationships. Oxford: Blackwell Scientific Publishers.Google Scholar
Wright, C.A. & Ross, G.C. (1983) Enzyme analysis of Schistosoma haematobium . Bulletin of the World Health Organization 61, 307316.Google ScholarPubMed
Wright, C.A., Southgate, V.R. & Knowles, R.J. (1972) What is Schistosoma intercalatum Fisher, 1934?. Transactions of the Royal Society of Tropical Medicine and Hygiene 66, 2864.CrossRefGoogle ScholarPubMed
Wright, C.A., Southgate, V.R., van Wijk, H.B. & Moore, P.J. (1974) Hybrids between Schistosoma haematobium and S. intercalatum in Cameroon. Transactions of the Royal Society of Tropical Medicine and Hygiene 68, 413414.CrossRefGoogle ScholarPubMed
Wright, C.A., Southgate, V.R. & Ross, G.C. (1979) Enzymes in Schistosoma intercalatum and the relative status of the lower Guinea and Zaire strains of the parasite. International Journal for Parasitology 9, 523528.CrossRefGoogle ScholarPubMed