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Molecular phylogenetics of the four Schistosoma species groups determined with partial 28S ribosomal RNA gene sequences

Published online by Cambridge University Press:  06 April 2009

D. T. J. Littlewood
Affiliation:
Department of Biology, King's College London, Campden Hill Road, London W8 7AH and Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD
D. A. Johnston
Affiliation:
Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD

Summary

Partial 28S ribosomal RNA (rRNA) gene sequences, including the variable domains D1, D2 and D3, were determined for representative species from the 4 Schistosoma species groups. On an alignment of 1345 bp from S. mansoni, S. haematobium, S. spindale and S. japonicum (with Heterobilharzia americana chosen as an outgroup), both maximum likelihood and maximum parsimony analyses provide a robust molecular phytogeny for the genus; ((((S. haematobium, S. spindale), S. mansoni), S. japonicum), H. americana). When analysed separately, both domain D1 and domain D2 yielded similarly informative data whereas D3 failed to resolve the phylogeny. These results confirm a phylogeny previously suggested by 18S rRNA gene sequences, corroborating the status of S. spindale as a sister taxon to S. haematobium, and demonstrate the utility of 28S rRNA gene sequence data for resolving phylogenies within the Schistosomatidae.

Note: nucleotide sequence data reported in this paper are available in the EMBL database under the accession numbers Z46503/04/05/06/21.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

Barker, S. C., Blair, D., Garrett, A. R. & Cribb, T. H. (1993). Utility of the D1 domain of nuclear 28S rRNA for phylogenetic inference in the Digenea. Systematic Parasitology 26, 181–8.CrossRefGoogle Scholar
Barral, V., This, P., Imbert-Establet, D., Combes, C. & Delseny, M. (1993). Genetic variability and evolution of the Schistosoma genome analysed by using random amplified polymorphic DNA markers. Molecular and Biochemical Parasitology 59, 211–22.CrossRefGoogle ScholarPubMed
Basch, P. F. (1991). Schistosomes. Development, Reproduction and Host Relations. Oxford: Oxford University Press.Google Scholar
Blair, D. & Barker, S. C. (1993). Affinities of the Glyiauchenidae: utility of the 18S rRNA gene for phylogenetic inference in the Digenea (Platyhelminthes). International Journal for Parasitology 23, 527–32.CrossRefGoogle Scholar
Bowles, J., Hope, M., Tiu, W. U., Liu, X. & McManus, D. P. (1993). Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Tropica 55, 217–29.CrossRefGoogle ScholarPubMed
Cabot, E. L. & Beckenbach, A. T. (1989). Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Computer Applications in the Biosciences 5, 233–4.Google ScholarPubMed
Christen, R. (1993). VSMI6s – Databasefor rRNA Sequence Information. Distributed by the author. Villefranche-sur-Mer, France: Observatoire Océanologique, F06230.Google Scholar
Davis, G. M. (1980). Snail hosts of Asian Schistosoma infecting man: evolution and coevolution. In Malacological Review, Suppl. 2 – The Mekong Schistosome (ed. Bruce, J. I. & Sornami, S.), pp. 195238. Whitmore Lake, Michigan: Malacological Review.Google Scholar
Davis, G. M. (1982). Historical and ecological factors in the evolution, adaptive radiation, and biogeography of freshwater mollusks. American Zoologist 22, 375–95.CrossRefGoogle Scholar
Degnan, B. M., Yan, J., Hawkins, C. J. & Lavin, M. (1990). rRNA genes from the lower chordate Herdmania momus: structural similarity with higher eukaryotes. Nucleic Acids Research 18, 7063–70.CrossRefGoogle ScholarPubMed
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 1, 295304.CrossRefGoogle ScholarPubMed
Desprès, L., Imbert-Establet, D. & Monnerot, M. (1993). Molecular characterization of mitochondrial DNA provides evidence for the recent introduction of Schistosoma mansoni into America. Molecular and Biochemical Parasitology 60, 221–30.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1993). PHYLIP: Phytogeny Inference Package v.3.5c. Distributed by the author. Seattle: Department of Genetics, University of Washington.Google Scholar
Fletcher, M., Woodruff, D. S., Loverde, P. T. & Asch, H. L. (1980). Genetic differentiation between Schistosoma mekongi and S. japonicum: an electrophoretic study. In Malacological Review Suppl. 2 – The Mekong Schistosome (ed. Bruce, J. I. & Sornami, S.), pp. 113122. Whitmore Lake, Michigan: Malacological Review.Google Scholar
Gill, L. L., Hardman, N., Chappell, L., Qu, L. H., Nicoloso, M. & Bachellerie, J.-P. (1988). Phylogeny of Onchocerca volvulus and related species deduced from rRNA sequence comparisons. Molecular and Biochemical Parasitology 28, 6976.CrossRefGoogle ScholarPubMed
Hassouna, N., Michot, B. & Bachellerie, J.-P. (1984). The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Research 12, 3563–83.CrossRefGoogle ScholarPubMed
Haszprunar, G. (1988). On the origin and evolution of major gastropod groups, with special reference to the Streptoneura. Journal of Molluscan Studies 54, 367441.CrossRefGoogle Scholar
Hillis, D. M. & Dixon, M. T. (1991). Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology 66, 411–53.CrossRefGoogle ScholarPubMed
Hubendick, B. (1948). Studies on Bulinus. Arkiv foer Zoologi 40A, 163.Google Scholar
Hubendick, B. (1955). Phylogeny in the Planorbidae. Transactions of the Zoological Society of London 28, 453542.CrossRefGoogle Scholar
Johnston, D. A., Kane, R. A. & Rollinson, D. (1993 a). Small submit (18S) ribosomal RNA gene divergence in the genus Schistosoma. Parasitology 107, 147–56.CrossRefGoogle Scholar
Johnston, D. A., Dias, Neto E., Simpson, A. J. G. & Rollison, D. (1993 b). Opening the can of worms: Molecular analysis of schistosome populations. Parasitology Today 9, 286–91.CrossRefGoogle Scholar
Kane, R. A. & Rollinson, D. (1993). Repetitive sequences in the ribosomal DNA internal transcribed spacer of Schistosoma haematobium, Schistosoma intercalatum and Schistosoma mattheei. Molecular and Biochemical Parasitology 63, 153–6.CrossRefGoogle Scholar
Kaukas, A., Dias, Neto E., Simpson, A. J. G., Southgate, V. R. & Rollinson, D. (1994). A Phylogenetic analysis of Schistosoma haematobium group species based on randomly amplified polymorphic DNA. International Journal for Parasitology 24, 285–90.CrossRefGoogle ScholarPubMed
Larsen, N., Olsen, J. G., Maidak, B. L., McCaughley, M. J., Overbeek, R., Macke, T. J., Marsh, T. L. & Woese, C. R. (1993). The ribsomal database project. Nucleic Acids Research 21 (Suppl.), 3021–3.CrossRefGoogle Scholar
Lenaers, G., Maroteauz, L., Michot, B. & Herzog, M. (1989). Dinoflagellates in evolution. A molecular phylogenetic analysis of large subunit ribosonal RNA. Journal of Molecular Evolution 29, 4051.CrossRefGoogle Scholar
Littlewood, D. T. J. (1995). Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Molecular Phylogenetics and Evolution (in the press).Google Scholar
Medlin, L., Elwood, H. J., Stickel, S. & Sogin, M. L. (1988). The characterization of enzymatically amplified 16S-like rRNA-coding regions. Gene 71, 491–9.CrossRefGoogle ScholarPubMed
Michot, B., Qu, L. -H. & Bachellerie, J. -P. (1990). Evolution of large-subunit rRNA structure. European Journal of Biochemistry 188, 219–29.CrossRefGoogle ScholarPubMed
Michot, B., Desprès, L., Bonhomme, F. & Bachellerie, J. -P. (1993). Conserved secondary structures in the ITS2 of trematode pre-rRNA. FEBS Letters 316, 247–52.CrossRefGoogle ScholarPubMed
Olsen, G. J. & Woese, C. R. (1993). Ribosomal RNA: a key to phylogeny. FASEB Journal 7, 113–23.CrossRefGoogle ScholarPubMed
Qu, L. -H., Hardman, N., Gill, L. L., Chappell, L., Nicoloso, M. & Bachellerie, J. -P. (1986). Phylogeny of helminths determined by rRNA sequence comparison. Molecular and Biochemical Parasitology 20, 93–9.CrossRefGoogle ScholarPubMed
Qu, L. -H., Nicoloso, M. & Bachellerie, J. -P. (1988). Phylogenetic calibration of the 5′ terminal domain of large rRNA achieved by determining twenty eucaryotic sequences. Journal of Molecular Evolution 28, 113–24.CrossRefGoogle ScholarPubMed
Raué, H. A., Klootwijk, J. & Musters, W. (1988). Evolutionary conservation of structure and function of high molecular weight rRNA. Progress in Biophysics and Molecular Biology 51, 77129.CrossRefGoogle Scholar
Raué, H. A., Musters, W., Rutgers, C. A., Van T Riet, J. & Planta, R. J. (1990). rRNA: from structure to function. In The Ribosome: Structure, Function and Evolution (ed. Hill, W. E., Dahlberg, A., Garrett, R. A., Moore, P. B., Schlessinger, D. & Warner, J. R.) pp. 217–35. WashingtonD. C.: American Society for Microbiology.Google Scholar
Rohde, K., Hefford, C., Ellis, J. T., Baverstock, P. R., Johnson, A. M., Watson, N. A. & Ditmann, S. (1993). Contributions to the phylogeny of platyhelminthes based on partial sequencing of 18S ribosomal DNA. International Journal for Parasitology 23, 705–24.CrossRefGoogle Scholar
Rollinson, D. & Southgate, V. R. (1987). The genus Schistosoma: a taxonomic appraisal. In The Biology of Schistosomes – from Genes to Latrines (ed. Rollinson, D. & Simpson, A. J. G.), pp. 149. London: Academic Press.Google Scholar
Simpson, A. J. G. (1987). Schistosome molecular biology. In The Biology of Schistosomes – from Genes to Latrines (ed. Rollinson, D. & Simpson, A. J. G.) pp. 147–61. London: Academic Press.Google Scholar
Simpson, A. J. G., Dame, J. B., Lewis, F. A. & McCutchan, T. F. (1984). The arrangement of ribosomal genes in Schistosoma mansoni: identification of polymorphic structural variants. European Journal of Biochemistry 139, 41–5.CrossRefGoogle ScholarPubMed
Smith, A. B.Lafay, B. & Cristen, R. (1992). Comparative variation of morphological and molecular evolution through geologic time: 28S ribosomal RNA versus morphology in echinoids. Philosophical Transactions of the Royal Society of London, B 338, 365–82.Google ScholarPubMed
Sokal, R. R. & Rohlf, F. J. (1981). Biometry. 2nd Edn.San Francisco: W. H. Freeman and Co.Google Scholar
Swofford, D. L. (1993). PAUP: Phylogenetic Analysis Using Parsimony v.3.1.1. Distributed by the author. Washington, D. C.: Smithsonian Institution.Google Scholar
Taylor, D. W. (1988). Aspects of freshwater mollusc ecological biogeography. Palaeogeography, palaeoclimatology and palaeoecology 62, 511–76.CrossRefGoogle Scholar
Zharkikh, A. & Rzhetsky, A. (1990). VOSTORG: Phylogenetic Reconstruction and Tree Building Programs v.3.0. Distributed by the authors. Novosibirsk: USSR Academy of Science.Google Scholar