Skip to main content
×
Home

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

  • S. W. ATTWOOD (a1) (a2), F. A. FATIH (a2), M. M. H. MONDAL (a3), M. A. ALIM (a3), S. FADJAR (a4), R. P. V. J. RAJAPAKSE (a5) and D. ROLLINSON (a2)...
Summary
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.

Copyright
Corresponding author
*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
References
Hide All
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, 719.
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, 113.
Barker S. C. and Blair D. (1996). Molecular phylogeny of Schistosoma species supports traditional groupings within the genus. Journal of Parasitology 82, 292298.
Batchelor B. C. (1979). Discontinuously rising late Cainozoic eustatic sea-levels, with special reference to Sundaland, Southeast Asia. Geologie en Mijnbouw 58, 120.
Bednarik R. G. (1995). Seafaring Homo erectus. The Artefact 18, 9192.
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, 179183.
Chitsulo L., Engels D., Montresor A. and Savioli L. (2000). The global status of schistosomiasis and its control. Acta Tropica 77, 4151.
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. 187214. Oxford University Press, Oxford, UK.
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, 1235.
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, 30413056.
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, 157164.
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, 295304.
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, 483486.
Edwards S. V. and Beerli P. (2000). Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54, 18391854.
Farris J. S., Kallersjo M., Kluge A. G. and Bult C. (1995). Constructing a significance test for incongruence. Systematic Biology 44, 570572.
Felsenstein J. (1988). Phylogenies from molecular sequences: inference and reliability. Annual Reviews of Genetics 22, 521565.
Fenwick A., Rollinson D. and Southgate V. R. (2006). Implementation of human schistosomiasis control: challenges and prospects. Advances in Parasitology 61, 568623.
Foster P. G. (2004). Modelling compositional heterogeneity. Systematic Biology 53, 485495.
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, S96S99.
Holder M. and Lewis P. O. (2003). Phylogeny estimation: traditional and Bayesian approaches. Nature Reviews: Genetics 4, 275284.
Huelsenbeck J. P., Ronquist F. and Hall B. (2000). MrBayes: Bayesian Inference of Phylogeny; the Manual. Department of Biology, University of Rochester, Rochester, USA.
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, 131137.
Kolaczkowski B. and Thornton J. W. (2006). Is there a star tree paradox? Molecular Biology and Evolution 23, 18191823.
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, 11231125.
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, 243256.
Lee M. S. Y. (2001). Uninformative characters and apparent conflict between molecules and morphology. Molecular Biology and Evolution 18, 676680.
Lewis P. O., Holder M. E. and Holsinger K. E. (2005). Polytomies and Bayesian phylogenetic inference. Systematic Biology 54, 241253.
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, 452467.
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, 203224.
Matthee C., Burzlaft J. D., Taylor J. F. and Davis S. K. (2001). Mining the mammalian genome for artiodactyl systematics. Systematic Biology 50, 367390.
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, 550559.
McCarthy C. (1996). Chromas, version 1.3, Griffith University, Brisbane, Australia.
Montgomery R. E. (1906). Observations on bilharziasis among animals in India. II. Journal of Tropical Veterinary Science 1, 138174.
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, 977985.
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. 90128. Oxford University Press, Oxford, UK.
Nei M. and Kumar S. (2000). Molecular Evolution and Phylogenetics. Oxford University Press, New York.
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, 664671.
Posada D. and Crandall K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.
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, 586602.
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, 321324.
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. 149. Academic Press, London.
Ronquist F. and Huelsenbeck J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.
Rozas J. and Rozas R. (1999). DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174175.
Shimodaira H. and Hasegawa M. (1999). Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 11141116.
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, 91100.
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, 283288.
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, 651656.
Swofford D. L. (2002). PAUP* Phylogenetic Analysis Using Parsimony (and Other Methods), 4th Edn. Sinauer Associates, Sunderland, Massachusetts.
Tajima F. (1989). Statistical methods for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585595.
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, 46734680.
Tija H. D. (1980). The Sunda shelf, Southeast Asia. Zeitschrift für Geomorphologie N.F. 24, 405427.
Van Dongen S. (2006). Prior specification in Bayesian statistics: three cautionary tales. Journal of Theoretical Biology 242, 90100.
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, 947955.
Winnepenninck B., Backeljau T. and De Wachter R. (1993). Extraction of high molecular weight DNA from molluscs. Trends in Genetics 9, 407.
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.
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, 17.
Zwickl D. J. and Hillis D. M. (2002). Increased taxon sampling greatly reduces phylogenetic error. Systematic Biology 51, 588598.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 16
Total number of PDF views: 32 *
Loading metrics...

Abstract views

Total abstract views: 259 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 14th December 2017. This data will be updated every 24 hours.