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A phylogeny based on three mitochondrial genes supports the division of Schistosoma intercalatum into two separate species

Published online by Cambridge University Press:  09 October 2003

R. A. KANE
Affiliation:
Biomedical Parasitology Division, Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD
V. R. SOUTHGATE
Affiliation:
Biomedical Parasitology Division, Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD
D. ROLLINSON
Affiliation:
Biomedical Parasitology Division, Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD
D. T. J. LITTLEWOOD
Affiliation:
Parasitic Worms Division, Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD
A. E. LOCKYER
Affiliation:
Parasitic Worms Division, Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD
J. R. PAGÈS
Affiliation:
Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne (UMR 5555 du CNRS), Université de Perpignan, Av. De Villeneuve, 66860 Perpignan Cedex, France
L. A. TCHUEM TCHUENTÉ
Affiliation:
Laboratoire de Biologie Générale, Faculté des Sciences, Université de Yaoundé I, B.P. 812 Yaoundé, Cameroun
J. JOURDANE
Affiliation:
Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne (UMR 5555 du CNRS), Université de Perpignan, Av. De Villeneuve, 66860 Perpignan Cedex, France

Abstract

Two recognized strains of Schistosoma intercalatum, one from the Democratic Republic of Congo (DRC), formerly Zaire, and the other from Cameroon, have been investigated using DNA sequences from 3 mitochondrial genes, cytochrome oxidase subunit 1 (cox1), NADH dehydrogenase subunit 6 (nad6) and the small ribosomal RNA gene (rrnS). In addition, partial DNA sequences from the nuclear large subunit ribosomal RNA gene (lsrDNA) were included within the study. Although partial lsrDNA alone reveals little taxonomic information, phylogenetic analysis of the mitochondrial data demonstrates a clear dichotomy between the 2 purported strains and it is proposed that they should be treated as distinct taxa. The ‘original’ S. intercalatum now falls relatively basal in the S. haematobium group, while the proposed new species is more derived and sister taxon to S. bovis and S. curassoni.

Type
Research Article
Copyright
2003 Cambridge University Press

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References

REFERENCES

BJØRNEBOE, A. & FRANDSEN, F. (1979). A comparison of the characteristics of two strains of Schistosoma intercalatum Fisher, 1934 in mice. Journal of Helminthology 53, 195203.CrossRefGoogle Scholar
BROWN, D. S., SARFATI, C., SOUTHGATE, V. R. & KNOWLES, R. J. (1984). Observations on Schistosoma intercalatum in south–east Gabon. Zeitschrift für Parasitenkunde 70, 243253.CrossRefGoogle Scholar
CUNNINGHAM, C. W. (1997). Can three incongruence tests predict when data should be combined? Molecular Biology and Evolution 14, 733740.Google Scholar
FARRIS, J. S., KALLERSJO, M., KLUGE, A. G. & BULT, C. (1995). Constructing a significance test for incongruence. Systematic Biology 44, 570572.CrossRefGoogle Scholar
FISHER, A. C. (1934). A study of the schistosomiasis of the Stanleyville district of the Belgium Congo. Transactions of the Royal Society of Tropical Medicine and Hygiene 28, 277306.CrossRefGoogle Scholar
FRANDSEN, F. (1978). Hybridization between different strains of Schistosoma intercalatum Fisher, 1934 from Cameroun and Zaire. Journal of Helminthology 52, 1122.CrossRefGoogle Scholar
HUELSENBECK, J. P., BULL, J. J. & CUNNINGHAM, C. W. (1996). Combining data in phylogenetic analysis. Trends in Ecology and Evolution 11, 152158.CrossRefGoogle Scholar
JEANMOUGIN, F., THOMPSON, J. D., GOUY, M., HIGGINS, D. G. & GIBSON, T. J. (1998). Multiple sequence alignment with Clustal X. Trends in Biochemical Sciences 23, 403405.CrossRefGoogle Scholar
KUMAR, S., TAMURA, K., JAKOBSEN, I. B. & NEI, M. (2001). MEGA2: Molecular Evolutionary Genetics Analysis software. Bioinformatics 17, 12441245.CrossRefGoogle Scholar
LEE, M. S. Y. (2001). Uninformative characters and apparent conflict between molecules and morphology. Molecular Biology and Evolution 18, 676680.CrossRefGoogle Scholar
LITTLEWOOD, D. T. J. & JOHNSTON, D. A. (1995). Molecular phylogenetics of the four Schistosoma species groups determined with partial 28S ribosomal RNA gene sequences. Parasitology 111, 167175.CrossRefGoogle Scholar
LOCKYER, A. E., OLSON, P. D., ØSTERGAARD, 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. & 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 Scholar
MADDISON, W. P. & MADDISON, D. R. (2000). MacClade. Version 4. Sinauer Associates, Sunderland, Massachusetts.
MUTANI, A., CHRISTENSEN, N. Ø. & FRANDSEN, F. (1985). A study of the biological characteristics of a hybrid line between male Schistosoma haematobium (Dar es Salaam, Tanzania) and female S. intercalatum (Edea, Cameroun). Acta Tropica 42, 319331.Google Scholar
PAGÈS, J. R., DURAND, P., SOUTHGATE, V. R., TCHUEM TCHUENTÉ, L. A. & JOURDANE, J. (2001 a). Molecular arguments for splitting of Schistosoma intercalatum into two distinct species. Parasitology Research 87, 5762.Google Scholar
PAGÈS, J. R., SOUTHGATE, V. R., TCHUEM TCHUENTÉ, L. A. & JOURDANE, J. (2001 b). Lack of prezygotic isolation by assortative mating between the two cryptic species of the polytypic Schistosoma intercalatum taxon. Parasitology Research 87, 888890.Google Scholar
PAGÈS, J. R., SOUTHGATE, V. R., TCHUEM TCHUENTÉ, L. A. & JOURDANE, J. (2002). Experimental evidence of hybrid breakdown between the two geographical strains of Schistosoma intercalatum. Parasitology 124, 169175.CrossRefGoogle Scholar
POSADA, D. & CRANDALL, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle Scholar
SHIMODAIRA, H. & HASEGAWA, M. (1999). Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 11141116.CrossRefGoogle Scholar
SOUTHGATE, V. R., ROLLINSON, D., KAUKAS, A., ALMEDA, J., SOUSA, A. M., CASTRO, F., SOARES, E. & CORACHAN, M. (1994). Schistosomiasis in the Republic of São Tomé and Principe: characterization of Schistosoma intercalatum. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 479486.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.Google Scholar
SWOFFORD, D. L. (2002). PAUP*. (Phylogenetic Analysis Using Parsimony* and Other Methods). Sinauer Associates, Sunderland, Massachusetts.
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, 263259.CrossRefGoogle Scholar
TELFORD, M. J., HERNIOU, E. A., RUSSELL, R. B. & LITTLEWOOD, D. T. J. (2000). Changes in mitochondrial genetic codes as phylogenetic characters: Two examples from the flatworms. Proceedings of the National Academy of Sciences, USA 97, 1135911364.CrossRefGoogle Scholar
WALKER, T. K., ROLLINSON, D. & SIMPSON, A. J. G. (1986). Differentiation of Schistosoma haematobium from related species using cloned ribosomal RNA gene probes. Molecular and Biochemical Parasitology 20, 123131.CrossRefGoogle Scholar
WRIGHT, C. A. & ROSS, G. C. (1980). Hybrids between Schistosoma haematobium and S. mattheei and their identification by isoelectric focusing of enzymes. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 326332.Google Scholar
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.Google Scholar
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 Scholar