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A molecular evolutionary framework for the phylum Nematoda

Abstract

Nematodes are important: parasitic nematodes threaten the health of plants, animals and humans on a global scale1,2; interstitial nematodes pervade sediment and soil ecosystems in overwhelming numbers3; and Caenorhabditis elegans is a favourite experimental model system4. A lack of clearly homologous characters and the absence of an informative fossil record have prevented us from deriving a consistent evolutionary framework for the phylum. Here we present a phylogenetic analysis, using 53 small subunit ribosomal DNA sequences from a wide range of nematodes. With this analysis, we can compare animal-parasitic, plant-parasitic and free-living taxa using a common measurement. Our results indicate that convergent morphological evolution may be extensive and that present higher-level classification of the Nematoda will need revision. We identify five major clades within the phylum, all of which include parasitic species. We suggest that animal parasitism arose independently at least four times, and plant parasitism three times. We clarify the relationship of C. elegans to major parasitic groups; this will allow more effective exploitation of our genetic and biological knowledge of this model species.

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Figure 1: MP analysis of SSU sequences from 53 nematode taxa.
Figure 2: A phylogenetic hypothesis for the phylum Nematoda based on the SSU-sequence dataset.

References

  1. Luc, M., Sikora, R. A. & Bridge, J. Plant Parasitic Nematodes in Tropical and Subtropical Agriculture (CAB International, Wallingford, UK, (1990)).

    Google Scholar 

  2. Anderson, R. C. Nematode Parasites of Vertebrates. Their Development and Transmission (CAB International, Wallingford, UK, (1992)).

    Google Scholar 

  3. Lambshead, J. Recent developments in marine benthic biodiversity research. Oceanis 19, 5–24 (1993).

    Google Scholar 

  4. Riddle, D., Blumenthal, T., Meyer, B. & Priess, J. (eds) C. elegans II (Cold Spring Harbor Laboratory Press, NY, (1997)).

    Google Scholar 

  5. Ellis, R. E., Sulston, J. E. & Coulson, A. R. The rDNA of C. elegans: sequence and structure. Nucleic Acids Res. 14, 2345–2364 (1986).

    Article  CAS  Google Scholar 

  6. Zarlenga, D. S., Stringfellow, F., Nobary, M. & Lichtenfels, J. R. Cloning and characterisation of ribosomal RNA genes from three species of Haemonchus (Nematoda: Trichostrongyloidea) and identification of PCR primers for rapid differentiation. Exp. Parasitol. 78, 28–36 (1994).

    Article  CAS  Google Scholar 

  7. Fitch, D. H. A., Bugaj-gaweda, B. & Emmons, S. W. 18S ribosomal gene phylogeny for some rhabditidae related to Caenorhabditis elegans. Mol. Biol. Evol. 12, 346–358 (1995).

    CAS  PubMed  Google Scholar 

  8. Baldwin, J. G., Frisse, L. M., Vida, J. T., Eddleman, C. D. & Thomas, W. K. An evolutionary framework for the study of developmental evolution in a set of nematodes related to Caenorhabditis elegans. Mol. Phylogenet. Evol. 8, 249–259 (1997).

    Article  CAS  Google Scholar 

  9. Baldwin, J. G. et al. The buccal capsule of Aduncospiculum halicti (Nemata: Diplogasterina): an ultrastructural and molecular phylogenetic study. Can. J. Zool. 75, 407–423 (1997).

    Article  CAS  Google Scholar 

  10. Swofford, D. L., Olsen, G. J., Waddell, P. J. & Hillis, D. M. in Molecular Systematics (eds Hillis, D. M., Moritz, C. & Mable, B. K.) 407–514 (Sinauer, Sunderland, MA, (1996))

    Google Scholar 

  11. Aguinaldo, A. M. A. et al. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489–493 (1997).

    Article  CAS  Google Scholar 

  12. Lorenzen, S. The Phylogenetic Systematics of Free-Living Nematodes (The Ray Society, London, (1994)).

    Google Scholar 

  13. Malakhov, V. V. Nematodes. Structure, Development, Classification and Phylogeny (Smithsonian Institution Press, Washington, (1994)).

    Google Scholar 

  14. Maggenti, A. R. in Concepts in Nematode Systematics (eds Stone, A. R., Platt, H. M. & Khalil, L. F.) 25–40 (Academic, London, (1983)).

    Google Scholar 

  15. Baldwin, J. G. & Eddleman, C. D. Buccal capsule of Zeldia punctata (Nemata: Cephalobidae): an ultrastructural study. Can. J. Zool. 73, 648–656 (1995).

    Article  Google Scholar 

  16. Etzinger, A. & Sommer, R. The homeotic gene lin-39 and the evolution of nematode epidermal cell fates. Science 278, 452–455 (1997).

    Article  ADS  Google Scholar 

  17. Poinar, G. Origins and phylogenetic relationships of the entomophilic rhabditids, Heterorhabditis and Steinernema. Fund. Appl. Nematol. 16, 332–338 (1993).

    Google Scholar 

  18. Siddiqi, M. R. Phylogenetic relationships of the soil orders Dorylaimida, Mononchida, Triplonchida and Alaimida, with a revised classification of the subclass Enoplia. Pak. J. Nematol. 1, 79–110 (1983).

    Google Scholar 

  19. Poinar, G. O. The Natural History of Nematodes (Prentice-Hall, Englewood Cliffs, NJ, (1983)).

    Google Scholar 

  20. De Ley, P., van de Velde, M. C., Mounport, D., Baujard, P. & Coomans, A. Ultrastructure of the stoma in Cephalobidae, Panagrolaimidae and Rhabditidae, with a proposal for a revised stoma terminology in Rhabditida. Nematologica 41, 153–182 (1995).

    Article  Google Scholar 

  21. Winnepenninckx, B. et al. 18S rRNA data indicate that Aschelminthes are polyphyletic in origin and consist of at least three distinct clades. Mol. Biol. Evol. 12, 1132–1137 (1995).

    CAS  PubMed  Google Scholar 

  22. Blaxter, M. L. et al. Genes expressed in Brugia malayi infective third stage larvae. Mol. Biochem. Parasitol. 77, 77–96 (1996).

    Article  CAS  Google Scholar 

  23. Swofford, D. L. PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1 (Illinois Natural History Society, Champaign, (1993)).

    Google Scholar 

  24. Maddison, W. & Maddison, D. MacClade v3.0 (Sinauer, Sunderland, MA, (1993)).

    Google Scholar 

  25. Kumar, S., Tamura, K. & Nei, M. MEGA: Molecular Evolutionary Genetics Analysis. Version 1.0 (Pennsylvania State Univ., (1993)).

    Google Scholar 

  26. Van de Peer, Y., Rensing, S., Maire, U.-G. & De Wachter, R. Substitution rate calibration of small subunit subunit RNA identifies chlorarachniophyte nucleomorphs as remnants of green algae. Proc. Natl Acad. Sci. USA 93, 7732–7736 (1996).

    Article  ADS  CAS  Google Scholar 

  27. Van de Peer, Y. & De Wachter, R. TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput. Appl. Biosci. 10, 569–570 (1994).

    CAS  PubMed  Google Scholar 

  28. Yang, Z. Phylogenetic Analysis by Maximum Likelihood (PAML) Version 1.2 (Univ. California, Berkeley, (1996)).

    Google Scholar 

  29. Felsenstein, J. Cases in which parsimony and compatibility methods will be positively misleading. Syst. Zool. 27, 401–410 (1978).

    Article  Google Scholar 

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Acknowledgements

We thank our colleages for donations of nematode material, and D. Swofford for use of prerelease versions of PAUP*4.0. This work was supported by grants from the Wellcome Trust, the Linnean Society of London, the Belgian National Fund for Scientific Research, the NSF, the NIH and the United States Department of Agriculture.

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Correspondence to Mark L. Blaxter.

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Blaxter, M., De Ley, P., Garey, J. et al. A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71–75 (1998). https://doi.org/10.1038/32160

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