Review paper: The evolutionary relationships of rotifers and acanthocephalans

  • James R. Garey
  • Andreas Schmidt-Rhaesa
  • Thomas J. Near
  • Steven A. Nadler
Part of the Developments in Hydrobiology book series (DIHY, volume 134)


Advances in morphological and molecular studies of metazoan evolution have led to a better understanding of the relationships among Rotifera (Monogononta, Bdelloidea, Seisonidea) and Acanthocephala, and their relationships to other bilateral animals. The most accepted morphological analysis places Acanthocephala as a sister group to Rotifera, although other studies have placed Acanthocephala as a sister taxon to Bdellodea or Seisonidea. Molecular analyses using nuclear 18S rRNA and mitochondrial 16S rRNA genes support Acanthocephala as a sister taxon to Bdelloidea, although no molecular data is available for Seisonidea. Combining molecular and morphological analyses of Bilateria leads to a tree with Platyhelminthes, Rotifera, Acanthocephala and Gnathostomulida (and probably Gastrotricha) as a sister group to the annelid-mollusc lineage of the Spiralia (Lophotrochozoa).

Key words

phylogeny acanthocephala rotifera bilateria evolution 18S rRNA gene 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aguinaldo, A. M. A., J. M. Turbeville, L. S. Linford, M. C. Rivera, J. R. Garey, R. A. Raff & J. A. Lake, 1997. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387: 489–493.PubMedCrossRefGoogle Scholar
  2. Ahlrichs, W., 1995. Zur Ultrastruktur und Phylogenie von Seison nebaliae Grube, 1859 und Seison annulatus Claus, 1876-Hypothesen zu phylogenetischen Verwandtschaftsverhältnissen innerhalb der Bilateria. Cuvillier, Göttingen, 310 pp.Google Scholar
  3. Ahlrichs, W., 1997. Epidermal ultrastructure of Seison nebaliae and Seison annulatus, and a comparison of epidermal structures within the Gnathifera. Zoomorphology 117: 41–48.CrossRefGoogle Scholar
  4. Ax, P., 1996. Multicellular Animals, a new approach to the phylogenetic order in nature, Vol. I. Springer, Berlin, 225 pp.Google Scholar
  5. Brusca, R. C. & G. J. Brusca, 1990. Invertebrates. Sinauer, Sunderland, 922 pp.Google Scholar
  6. Clement, P. & E. Wurdak, 1991. Rotifera. In F. W. Harrison & E. E. Ruppert (eds), Microscopic Anatomy of Invertebrates, Vol. 4. Wiley-Liss, Inc., New York: 219–297.Google Scholar
  7. Clement, P., 1993. The phylogeny of rotifers: molecular, ultrastructural and behavioural data. Hydrobiologia 255/256: 527–544.CrossRefGoogle Scholar
  8. Davies, K. A. & J. M. Fisher, 1994. On hormonal control of moulting in Aphelenchus avenae (Nematoda: Aphelenchida). Int. J. Parasitai. 24: 649–655.CrossRefGoogle Scholar
  9. De Rijk, P. & R. De Wächter, 1993. DCSE, an interactive tool for sequence alignment and secondary struture research. Comput. Appl. Biosci. 9: 735–740.PubMedGoogle Scholar
  10. Donoghue, M. J., R. G. Olmstead, F. F. Smith & J. D. Palmer, 1992. Phylogenetic relationships of Dipsacaleson RbcL sequences. Ann. MO Bot. Gard. 79: 333–345.CrossRefGoogle Scholar
  11. Dunagan, T. T. & D. M. Miller, 1991. Acanthocephala. In F. W. Harrison & E. E. Ruppert (eds), Microscopic Anatomy of Invertebrates, Vol. 4. Wiley-Liss, Inc., New York: 299–332.Google Scholar
  12. Eernisse, D. J., J. S. Albert, & F. E. Anderson, 1992. Annelida and Arthropoda are not sister taxa: a phylogenetic analysis of spiralian metazoan morphology. Syst. Biol. 41: 305–330.Google Scholar
  13. Ehlers, U., W. Ahlrichs, C. Lemburg & A. Schmidt-Rhaesa, 1996. Phylogenetic systematization of the Nemathelminthes (Aschelminthes). Verh. Dtsch. Zool. Ges. 89.1: 8.Google Scholar
  14. Felsenstein, J., 1988. Phylogenies from molecular sequences: inference and reliability. Annu. Rev. Genet. 22: 521–565.PubMedCrossRefGoogle Scholar
  15. Felsenstein, J., 1993. PHYLIP: phylogeny inference package, version 3.5, University of Washington, Seattle.Google Scholar
  16. Felsenstein, J. & G. A. Churchill, 1996. A hidden Markov model approach to variation among sites in rate of evolution. Mol. Biol. Evol. 13: 930–104.CrossRefGoogle Scholar
  17. Garey J. R., T. J. Near, M. R. Nonnemacher & S. A. Nadler, 1996a. Molecular evidence for Acanthocephala as a sub-taxon of Rotifera. J. Mol. Evol. 43: 287–292.PubMedCrossRefGoogle Scholar
  18. Garey, J. R., M. Krotec, D. R. Nelson & J. Brooks, 1996b. Molecular analysis supports a Tardigrade-Arthropod association. Invert. Biol. 115:79–88.CrossRefGoogle Scholar
  19. Gupta, A. P., 1990. Morphogenetic hormones and their glands in arthropods: evolutionary aspects. In: Gupta (ed.), Morphogenetic Hormones of Arthropods. New Brunswick: Rutgers University Press: 1–34.Google Scholar
  20. Haffner, K. von, 1950. Organisation und systematische Stel ung der Acanthocephalen. Zool. Anz. 145: (suppl.) 243–274.Google Scholar
  21. Halanych, K. M., J. D. Bachelier, A. A. Aguinaldo, S. M. Liva, D. M. Hillis & J. A. Lake, 1995. Evidence of 18S ribosomal DNA that the Lophophorates are Protostome Animals. Science, 267: 1641–1643.PubMedCrossRefGoogle Scholar
  22. Hillis, D. M., J. P. Huelsenbeck & C. W. Cunningham, 1994. Application and accuracy of molecular phylogenies. Science 264: 671–677.PubMedCrossRefGoogle Scholar
  23. Hillis, D. M. & M. T. Dixon, 1991. Ribosomal DNA: molecular evolution and phylogenetic inference. Quart. Rev. Biol. 66: 411–446.PubMedCrossRefGoogle Scholar
  24. Hillis, D. M. & J. J. Bull, 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42: 182–192.Google Scholar
  25. Hyman, L., 1951. The invertebrates: Acanthocephala, Aschelminthes, and Entoprocta. McGraw Hill, New York, 572 pp.Google Scholar
  26. Kumar S, K. Tamura & M. Nei, 1994. MEGA: molecular evolutionary genetics analysis software for microcomputers. Comput. Appl. Biosci. 10: 189–191.PubMedGoogle Scholar
  27. Li, W.-H., 1997. Molecular Evolution. Sinauer Associates, Inc., Sunderland, MA, 487 pp.Google Scholar
  28. Lorenzen, S., 1985. Phylogenetic aspects of pseudocoelomate evolution. In S. Conway-Morris, J. D. George, R. Gibson & H. M. Platt (eds), The Origin and Relationships of Lower Invertebrates. Claredon Press, Oxford: 210–223.Google Scholar
  29. Mackey, L. Y, B. Winnepennickx, T. Backeljau, R. De Wachter, P. Emschermann & J. R. Garey, 1996. 18S rRNA suggests that Entoprocta are Protostomes, unrelated to Ectoprocta. J. Mol. Evol. 42: 552–559.PubMedCrossRefGoogle Scholar
  30. Malakhov, V. V, 1994. Nematodes. Smithsonian Institution Press, Washington, 286 pp.Google Scholar
  31. Markevich, F. I., 1993. Phylogenetic relationships of Rotifera to other vermiform taxa. Hydrobiologia 255/256: 521–526.CrossRefGoogle Scholar
  32. Miller, D. M. & T. T. Dunagan, 1985. Functional morphology. In D. W. T. Crompton & B. B. Nickol (eds), Biology of the Acanthocephala. Cambridge University Press, Cambridge: 73–123.Google Scholar
  33. Near, T. J., J. R. Garey & S. A. Nadler, 1997. Phylogenetic relationships of the acanthocephala inferred from 18S ribosomal DNA sequences. Mol. Phyl. Evol., in press.Google Scholar
  34. Nebelsick, M., 1993. Introvert, mouth cone, and nervous system of Echinoderes capitatus (Kinorhyncha, Cyclorhagida) and implications for the phylogenetic relationships of Kinorhyncha. Zoomorphology 113: 211–232.CrossRefGoogle Scholar
  35. Neuhaus, B., 1994. Ultrastructure of alimentary canal and body cavity, ground pattern, and phylogenetic relationships of the Kinorhyncha. Microfauna Marina 9: 61–156.Google Scholar
  36. Nielsen, C., 1995. Animal evolution. Interrelationships of the living phyla. Oxford University Press, Oxford, 467 pp.Google Scholar
  37. Nielsen, C., N. Scharff & D. Eibye-Jacobsen, 1996. Cladistic analysis of the animal kingdom. Biol. J. linn. Soc. 57: 385–410.CrossRefGoogle Scholar
  38. Pennak, R. W., 1989. Fresh-water invertebrates of the United States, Protozoa to Mollusca, 3rd Ed. John Wiley and Sons, New York, 628 pp.Google Scholar
  39. Raff, R. A., C. R. Marshall & J. M. Turbeville, 1994. Using DNA sequences to unravel the Cambrian radiation of the animal phyla, Annu. Rev. Ecol. Syst. 25: 351–374.CrossRefGoogle Scholar
  40. Remane, A., 1963. The systematic position and phylogeny of the pseudocoelomates. In E. C. Dougherty (ed.), The Lower Metazoa. Univ. of Calif. Press, Berkeley: 247–255.Google Scholar
  41. Ricci, C., G. Melone & C. Sotgia, 1993. Old and new data on Seisonidea (Rotifera). Hydrobiologia 255/256: 495–511.CrossRefGoogle Scholar
  42. Rieger, R. M. & S. Tyler, 1995. Sister-group relationship of Gnathostomulida and Rotifera-Acanthocephala. Invertebrate Biology 114: 186–188.CrossRefGoogle Scholar
  43. Ruppert, E. E. (1991) Introduction to the aschelminth phyla: a consideration of mesoderm, body cavities, and cuticle. In F. W. Harrison & E. E. Ruppert (eds), Microscopic Anatomy of Invertebrates, Vol. 4 Aschelminthes. Wiley-Liss, New York: 1–17.Google Scholar
  44. Ruppert, E. E. & R. D. Barnes, 1994. Invertebrate Zoology, 6th Ed., Saunders College Publ., Fort Worth, 1056 pp.Google Scholar
  45. Schram, F. R., 1991. Cladistic analysis of metazoan phyla and the placement of fossil problematica. In A. Simonetta & S. Conway Morris (eds), The Early Evolution of Metazoa and the Significance of Problematic Taxa. Cambridge University Press, Cambridge: 35–46.Google Scholar
  46. Storch, V. & U. Welsch, 1969. Über den Aufbau des Rotatorienintegumentes. Z. Zellforsch. 95: 405–414.PubMedCrossRefGoogle Scholar
  47. Telford, M. J. & P. W. H. Holland, 1993. The phylogenetic affinities of the chaetognaths: A molecular analysis. Mol. Biol. Evol. 10: 660–676.PubMedGoogle Scholar
  48. Wallace, R. L., C. Ricci & G. Melone, 1996. A cladistic analysis of pseudocoelomate (aschelminth) morphology. Invertebrate Biol. 115: 104–112.CrossRefGoogle Scholar
  49. Wallace, R. L. & R. A. Colburn, 1989. Phylogenetic relationships within phylum Rotifera: orders and genus Notholca. Hydrobiologia 186/187: 311–318.CrossRefGoogle Scholar
  50. Winnepenninckx, B., T. Backeljau, L. Y Mackey, J. M. Brooks, R. De Wachter, S. Kumar & J. R. Garey, 1995. 18S rRNA data indicate that the aschelminthes are polyphyletic and consist of at least three distinct clades. Molec. Biol. Evol. 12: 1132–1137.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1998

Authors and Affiliations

  • James R. Garey
    • 1
  • Andreas Schmidt-Rhaesa
    • 1
  • Thomas J. Near
    • 2
  • Steven A. Nadler
    • 3
  1. 1.Department of BiologyUniversity of South FloridaTampaUSA
  2. 2.Center for BiodiversityIllinois Natural History SurveyChampaignUSA
  3. 3.Department of NematologyUniversity of CaliforniaDavisUSA

Personalised recommendations