Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-16T07:43:24.656Z Has data issue: false hasContentIssue false
  • English
  • Français

A DNA sequence-based study of the Schistosoma indicum (Trematoda: Digenea) group: population phylogeny, taxonomy and historical biogeography

Published online by Cambridge University Press:  06 September 2007

S. W. ATTWOOD ,
F. A. FATIH ,
M. M. H. MONDAL ,
M. A. ALIM ,
S. FADJAR ,
R. P. V. J. RAJAPAKSE  and
D. ROLLINSON
S. W. ATTWOOD*
Affiliation:
State Key Laboratory of Biotherapy, West China Hospital, West China Medical School, Sichuan University, Chengdu 610041, PRChina Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
F. A. FATIH
Affiliation:
Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
M. M. H. MONDAL
Affiliation:
Department of Parasitology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh
M. A. ALIM
Affiliation:
Department of Parasitology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh
S. FADJAR
Affiliation:
Department of Parasitology and Pathology, Faculty of Veterinary Medicine, Bogor Agricultural University (IPB), Jl. Agathis – Kampus IPB Darmaga, Bogor 16680, Indonesia
R. P. V. J. RAJAPAKSE
Affiliation:
Faculty of Veterinary Medicine and Animal Science, Department of Veterinary Pathobiology, University of Peradeniya, Peradeniya 20400, Sri Lanka
D. ROLLINSON
Affiliation:
Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
*
*Corresponding author: State Key Laboratory of Biotherapy, Gaopeng Street, Keyuan Road 4, Chengdu 610041, China. Tel: +86 28 85164098. Fax: +86 28 85164092. E-mail: swahuaxi@yahoo.com
Get access Rights & Permissions [Opens in a new window]

Summary

Partial (DNA) sequences were collected for 2 mitochondrial loci (Srrna and Lrrna, the rrnS and rrnL rRNA genes respectively) for Schistosoma indicum group species from 4 Southeast Asian countries. The samples included 7 populations, 4 of which were previously unstudied. In 11 cases the combination of locus and population was new. The aim of the study was to provide a phylogeny based on new independent data and multiple populations (earlier studies had mostly used a common set of field samples or laboratory lines) and to examine interrelationships and phylogeography within this species group. Paraphyly of the S. indicum group was confirmed, as was the basal position of Schistosoma incognitum in the Schistosoma phylogeny. Southeast Asian Schistosoma spindale and S. incognitum populations were shown to fall into their respective con-specific cohesive groupings. Estimated divergence times for these taxa were shown to be related to Pleistocene changes in sea level and the radiation of definitive host groups. A revised phylogeographical model is proposed in the light of these findings.

Keywords

Schistosoma indicum groupphylogeographypopulation phylogenytaxonomy
Type
Research Article
Information
Parasitology , Volume 134 , Issue 14 , December 2007 , pp. 2009 - 2020
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Agatsuma, T., Iwagami, M., Liu, C. X., Rajapakse, R. P. V. J., Mondal, M. M. H., Kitikoon, V., Ambu, S., Agatsuma, Y., Blair, D. and Higuchi, T. (2002). Affinities between Asian non-human Schistosoma species, the S. indicum group, and the African human schistosomes. Journal of Helminthology 76, 7–19.Google Scholar
Attwood, S. W., Upatham, E. S., Meng, X. H., Qiu, D.-C. and Southgate, V. R. (2002). The phylogeography of Asian Schistosoma (Trematoda: Schistosomatidae). Parasitology 125, 1–13.Google Scholar
Barker, S. C. and Blair, D. (1996). Molecular phylogeny of Schistosoma species supports traditional groupings within the genus. Journal of Parasitology 82, 292–298.Google Scholar
Batchelor, B. C. (1979). Discontinuously rising late Cainozoic eustatic sea-levels, with special reference to Sundaland, Southeast Asia. Geologie en Mijnbouw 58, 1–20.Google Scholar
Bednarik, R. G. (1995). Seafaring Homo erectus. The Artefact 18, 91–92.Google Scholar
Chandler, A. C. (1926). A new schistosome infection of man, with notes on other human fluke infections in India. Indian Journal of Medical Research 14, 179–183.Google Scholar
Chitsulo, L., Engels, D., Montresor, A. and Savioli, L. (2000). The global status of schistosomiasis and its control. Acta Tropica 77, 41–51.Google Scholar
Clackson, T., Güssow, D. and Jones, P. T. (1991). General applications of PCR to gene cloning and manipulation. In PCR: A Practical Approach, Vol. 1 (ed. McPherson, M. J., Quirke, P. and Taylor, G. R.), pp. 187–214. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Combes, C., Albaret, J.-L., Arvy, L., Durette-Desset, M.-C., Gabrion, C., Jourdane, J., Lambert, A., Leger, N., Maillard, C., Matricon, M., Nassi, H., Prevot, G., Richard, J. and Theron, A. (1980). Atlas Mondiales des Cercaires. Mémoires du Muséum National D'Histoire Naturelle A115, 1–235.Google Scholar
Dejong, R. J., Morgan, J. A. T., Wilson, W. D., Al-Jaser, M. H., Appleton, C. C., Coulibaly, G., Doenhoff, M. J., Haas, W., Idris, M. A., Magalhaes, L. A., Mone, H., Mouahid, G., Mubila, L., Pointier, J.-P., Webster, J. P., Zanotti-Magalhaes, E. M., Paraense, W. L., Mkoji, G. M. and Loker, E. S. (2003). Phylogeography of Biomphalaria glabrata and B. pfeifferi, the two most important hosts of Schistosoma mansoni in the New and Old World tropics. Molecular Ecology 12, 3041–3056.Google Scholar
Desalle, R., Freedman, T., Prager, E. M. and Wilson, A. C. (1987). Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. Journal of Molecular Evolution 26, 157–164.CrossRefGoogle ScholarPubMed
Despres, L., Imbert-Establet, D., Combes, C. and Bonhomme, F. (1992). Molecular evidence linking hominid evolution to recent radiation of schistosomes (Platyhelminthes: Trematoda). Molecular Phylogenetics and Evolution 1, 295–304.Google Scholar
Duvall, R. H. and DeWitt, W. B. (1967). An improved perfusion technique for recovering adult schistosomes from laboratory animals. American Journal of Tropical Medicine and Hygiene 16, 483–486.Google Scholar
Edwards, S. V. and Beerli, P. (2000). Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54, 1839–1854.Google Scholar
Farris, J. S., Kallersjo, M., Kluge, A. G. and Bult, C. (1995). Constructing a significance test for incongruence. Systematic Biology 44, 570–572.Google Scholar
Felsenstein, J. (1988). Phylogenies from molecular sequences: inference and reliability. Annual Reviews of Genetics 22, 521–565.Google Scholar
Fenwick, A., Rollinson, D. and Southgate, V. R. (2006). Implementation of human schistosomiasis control: challenges and prospects. Advances in Parasitology 61, 568–623.Google Scholar
Foster, P. G. (2004). Modelling compositional heterogeneity. Systematic Biology 53, 485–495.CrossRefGoogle ScholarPubMed
Hebert, P. D. N., Ratnasingham, S. and Dewaard, J. R. (2003). Barcoding animal life: cytochrome c oxidase subunit divergences among closely related species. Proceedings of the Royal Society of London, B 270, S96–S99.Google Scholar
Holder, M. and Lewis, P. O. (2003). Phylogeny estimation: traditional and Bayesian approaches. Nature Reviews: Genetics 4, 275–284.Google Scholar
Huelsenbeck, J. P., Ronquist, F. and Hall, B. (2000). MrBayes: Bayesian Inference of Phylogeny; the Manual. Department of Biology, University of Rochester, Rochester, USA.Google Scholar
Kane, R. A., Southgate, V. R., Rollinson, D., Littlewood, D. T. J., Lockyer, A. E., Pages, J. R., Tchuem Tchuenté, L.-A. and Jourdane, J. (2003). A phylogeny based on three mitochondrial genes supports the division of Schistosoma intercalatum into two separate species. Parasitology 127, 131–137.Google Scholar
Kolaczkowski, B. and Thornton, J. W. (2006). Is there a star tree paradox? Molecular Biology and Evolution 23, 1819–1823.Google Scholar
Le, T. H., Blair, D., Agatsuma, T., Iwagami, M., Humair, P.-F., Campbell, N. J. H., Littlewood, D. T. J., Peacock, B., Johnston, D. A., Bartley, J., Rollinson, D., Herniou, E. A., Zarlenga, D. S. and McManus, D. P. (2000 a). Phylogenies inferred from mitochondrial gene orders – a cautionary tale from the parasitic flatworms. Molecular Biology and Evolution 17, 1123–1125.Google Scholar
Le, T. H., Blair, D. and McManus, D. P. (2000 b). Mitochondrial genomes of human helminths and their use as markers in population genetics and phylogeny. Acta Tropica 77, 243–256.Google Scholar
Lee, M. S. Y. (2001). Uninformative characters and apparent conflict between molecules and morphology. Molecular Biology and Evolution 18, 676–680.Google Scholar
Lewis, P. O., Holder, M. E. and Holsinger, K. E. (2005). Polytomies and Bayesian phylogenetic inference. Systematic Biology 54, 241–253.Google Scholar
Littlewood, D. T. J., Lockyer, A. E., Webster, B. L., Johnston, D. A. and Le, T. H. (2006). The complete mitochondrial genomes of Schistosoma haematobium and Schistosoma spindale and the evolutionary history of mitochondrial genome changes among parasitic flatworms. Molecular Phylogenetics and Evolution 39, 452–467.Google 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. 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, 203–224.CrossRefGoogle ScholarPubMed
Matthee, C., Burzlaft, J. D., Taylor, J. F. and Davis, S. K. (2001). Mining the mammalian genome for artiodactyl systematics. Systematic Biology 50, 367–390.CrossRefGoogle ScholarPubMed
Matthee, C., Catzeflis, F. M. and Douzery, E. J. P. (1997). Phylogenetic relationships of artiodactyls and cetaceans as deduced from the comparison of cytochrome b and 12S rRNA mitochondrial sequences. Molecular Biology and Evolution 14, 550–559.Google Scholar
McCarthy, C. (1996). Chromas, version 1.3, Griffith University, Brisbane, Australia.Google Scholar
Montgomery, R. E. (1906). Observations on bilharziasis among animals in India. II. Journal of Tropical Veterinary Science 1, 138–174.Google Scholar
Morgan, J. A. T., Dejong, R. J., Kazibwe, F., Mkoji, G. M. and Loker, E. S. (2003). A newly-identified lineage of Schistosoma. International Journal for Parasitology 33, 977–985.Google Scholar
Nei, M. (1991). Relative efficiencies of different tree-making methods for molecular data. In Phylogenetic Analysis of DNA Sequences (ed. Miyamoto, M. M. and Cracraft, J.), pp. 90–128. Oxford University Press, Oxford, UK.Google Scholar
Nei, M. and Kumar, S. (2000). Molecular Evolution and Phylogenetics. Oxford University Press, New York.CrossRefGoogle Scholar
Pollock, D. D., Zwickl, D. J., Mcguire, J. A. and Hillis, D. M. (2002). Increased taxon sampling is advantageous for phylogenetic inference. Systematic Biology 51, 664–671.Google Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.Google Scholar
Qiu, Z.-D. and Li, C. (2003). Chapter 22: Rodents from the Chinese Neogene: Biogeographic relationships with Europe and North Africa. Bulletin of the American Museum of Natural History 279, 586–602.Google Scholar
Rao, M. A. N. and Ayyar, L. S. P. (1933). Schistosoma suis, N. SP. A schistosome found in pigs in Madras. Indian Journal of Veterinary Science and Animal Husbandry 3, 321–324.Google Scholar
Rollinson, D. and Southgate, V. R. (1987). The genus Schistosoma: a taxonomic appraisal. In The Biology of Schistosomes: From Genes to Latrines (ed. Rollinson, D. and Simpson, A. J. G.), pp. 1–49. Academic Press, London.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Rozas, J. and Rozas, R. (1999). DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174–175.Google Scholar
Shimodaira, H. and Hasegawa, M. (1999). Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 1114–1116.Google Scholar
Sinha, P. K. and Srivastava, H. D. (1956). Studies on Schistosoma incognitumChandler, 1926 I. On the synonymy and morphology of the blood fluke. Parasitology 46, 91–100.Google Scholar
Snyder, S. D. and Loker, E. S. (2000). Evolutionary relationships among the Schistosomatidae (Platyhelminthes: Digenea) and an Asian origin for Schistosoma. Journal of Parasitology 86, 283–288.Google Scholar
Southgate, V. R., Tchuem Tchuenté, L.-A., Vercruysse, J. and Jourdane, J. (1995). Mating behaviour in mixed infections of Schistosoma haematobium and S. mattheei. Parasitological Research 81, 651–656.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2002). PAUP* Phylogenetic Analysis Using Parsimony (and Other Methods), 4th Edn. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
Tajima, F. (1989). Statistical methods for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.Google Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive mulitple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.Google Scholar
Tija, H. D. (1980). The Sunda shelf, Southeast Asia. Zeitschrift für Geomorphologie N.F. 24, 405–427.Google Scholar
Van Dongen, S. (2006). Prior specification in Bayesian statistics: three cautionary tales. Journal of Theoretical Biology 242, 90–100.CrossRefGoogle ScholarPubMed
Webster, B. L., Southgate, V. R. and Littlewood, D. T. J. (2006). A revision of the interrelationships of Schistosoma including the recently described Schistosoma guineensis. International Journal for Parasitology 36, 947–955.Google Scholar
Winnepenninck, B., Backeljau, T. and De Wachter, R. (1993). Extraction of high molecular weight DNA from molluscs. Trends in Genetics 9, 407.Google Scholar
Xia, X. (1999). DAMBE (Data Analysis in Molecular Biology and Evolution) Software, Version 3.7.48. University of Hong Kong (Department of Ecology and Biodiversity), Hong kong.Google Scholar
Xia, X., Xie, Z., Salemi, M., Chen, L. and Wang, Y. (2003). An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 1–7.Google Scholar
Zwickl, D. J. and Hillis, D. M. (2002). Increased taxon sampling greatly reduces phylogenetic error. Systematic Biology 51, 588–598.Google Scholar