Advertisement

The major lines of metazoan evolution: Summary of traditional evidence and lessons from ribosomal RNA sequence analysis

Chapter
Part of the EXS book series (EXS, volume 63)

Abstract

Contrary to a widespread belief among biologists, and to diagrams still found in many elementary biology or zoology textbooks, the general pattern of the phylogeny of Metazoa (the multicellular animals) is far from being settled. While there is a strong body of essentially congruent morphological, paleontological and molecular data concerning the branching pattern within some phyla or classes, most notably the vertebrates, the problem of the overall relationships of the invertebrate phyla is much more open (see Fig. 1 for a summary of conflicting schemes). These 32–36 phyla, however, account by far for most of the biological diversity of animals. They include some huge groups such as Arthopoda or Mollusca, to which many of the favorite experimental organisms discussed at this meeting belong as well as many additional groups also containing experimentally important species (e.g. Nematoda: Caenorhabditis; Echinodermata: the various sea urchins, both extensively used models in developmental biology; Annelida and Platyhelminthes, classical organisms for the study of embryology and regeneration, etc.). As illustrated in detail in books recently devoted to the subject (Barnes, 1987; Brusca and Brusca, 1990; Willmer, 1990), summarizing and updating over 200 years of comparative anatomy and embryology, defining a phylum is usually straightforward, but it is the establishment of the evolutionary relationships linking the different phyla that is difficult to achieve.

Keywords

Multicellular Animal Spiral Cleavage Invertebrate Phyla Placopecten Magellanicus Tree Construction Method 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abele, L. G., Kim, W., and Felgenhauer, B. E. (1989) Molecular evidence for inclusion of the phylum Pentastomida in the Crustacea. Molec. Biol. Evol. 6, 685–691Google Scholar
  2. Ax, P. (1989) Basic phylogenetic systematization of the Metazoa, in: The Hierarchy of Life. Molecules and Morphology in Phylogenetic Analysis, pp. 229–245. Eds B. Fernholm, K. Bremer and H. Jörnvall. Excerpta Medica, Amsterdam.Google Scholar
  3. Barnes, R. D. (1987) in: Invertebrate Zoology, pp. 1–893. Saunders College Publishing, Philadelphia.Google Scholar
  4. Baroin, A., Perasso, R., Qu, L. H., Brugerolle, G., Bachellerie, J. P., and Adoutte, A. (1988) Partial phylogeny of the unicellular eukaryotes based on rapid sequencing of a portion of 28S ribosomal RNA. Proc. Natl Acad. Sci. USA 85, 3474–3478.CrossRefGoogle Scholar
  5. Bode, H. R., and Steele, R. E. (1989) Phylogeny and molecular data. Science 243, 549–550.CrossRefGoogle Scholar
  6. Brooks, R., Fantes, P., Hunt, T., and Wheatley, D. (1989) The cell cycle. J. Cell Sci., Supplement 12, pp. 1–300. The Company of Biologists Limited, Cambridge.Google Scholar
  7. Brusca, R. C., and Brusca, G. J. (1990) Invertebrates, pp. 1–922. Sinauer Ass., Ins., Publishers, Sunderland, MA, USA.Google Scholar
  8. Cedergren, R., Gray, M. W. Abel, Y., and Sankoff, D. (1988) The evolutionary relationships among known life forms. J. Molec. Evol. 28, 98–112.CrossRefGoogle Scholar
  9. Chapman, R. L., and Buchheim, M. A. (1991) Ribosomal RNA gene sequences: analysis and significance in the phylogeny and taxonomy of green algae. Crit. Rev. Plant Sci. 10, 343–368.CrossRefGoogle Scholar
  10. Christen, R., Ratto, A., Baroin, A., Perasso, R., Grell, K. G., and Adoutte, A. (1991) An analysis of the origin of metazoans, using comparisons of partial sequences of the 28S RNA, reveals an early emergence of triploblasts. Europ. Mol. Biol. Org. J. 10, 499–503.Google Scholar
  11. Cloud, P., and Glaessner, M. F. (1982) The ediacarian period and system: Metazoa inherit the earth. Science 217, 783–792.CrossRefGoogle Scholar
  12. Conway Morris, S. (1989) Burgess shale faunas and the Cambrian explosion. Science 246, 339–346.CrossRefGoogle Scholar
  13. Erwin, D. H. (1991) Metazoan phylogeny and the Cambrian radiation. Trends Ecol. Evol. 6, 131–134.CrossRefGoogle Scholar
  14. Felsenstein, J. 1978 Cases in which parsimony and compatibility methods may be positively misleading. Syst. Zool. 27, 401–410.CrossRefGoogle Scholar
  15. Felsenstein, J. (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Molec. Evol. 17, 368–376.CrossRefGoogle Scholar
  16. Felsenstein, J. (1988) Phylogenies from molecular sequences: inference and reliability. Annu. Rev. Genet. 22, 521–565.CrossRefGoogle Scholar
  17. Field, K. G., Olsen, G. J., Giovannoni, S. J., Raff, E. C., Pace, N. R., and Raff, R. A. (1989) Phylogeny and molecular data. Science 243, 550–551.CrossRefGoogle Scholar
  18. Field, K. G., Olsen, G. J., Lane, D. J., Giovannoni, S. J., Ghiselin, M. T., Raff, E. C., Pace, N. R., and Raff, R. A. (1988) Molecular phylogeny of the animal kingdom. Science 239, 748–753.CrossRefGoogle Scholar
  19. Frankel, J. (1989) Pattern Formation. Ciliate Studies and Models, pp. 1–314. Oxford University Press, New York.Google Scholar
  20. Ghiselin, M. T. (1989) Summary of our present knowledge of metazoan phylogeny, in: The Hierarchy of Life. Molecules and Morphology in Phylogenetic Analysis, pp. 261–272. Eds B. Fernholm, K. Bremer and H. Jörnvall. Excerpta Medica, Amsterdam.Google Scholar
  21. Gouy, M., and Li, W.-H. (1989) Molecular phylogeny of the kingdoms animalia, plantae, and fungi. Molec. Biol. Evol. 6, 109–122.Google Scholar
  22. Gray, M. W. (1988) Organelle origins and ribosomal RNA. Biochem. Cell Biol. 66, 325–348.CrossRefGoogle Scholar
  23. Hanson, E. D. (1977) The Origin and Early Evolution of Animals, pp. 1–670. Wesleyan University Press, Middletown, CT, USA.Google Scholar
  24. Harz, H., and Hegemann, P. (1991) Rhodopsin-regulated calcium currents in Chlamydomonas.Nature 351, 489–491.CrossRefGoogle Scholar
  25. Hendriks, L., De Baere, R., Van Broeckhoven, C., and De Wachter, R. (1988a) Primary and secondary structure of the 18S ribosomal RNA of the insect species Tenebrio molitor. Fedn Europ. Biochem. Soc. Lett. 232, 115–120.CrossRefGoogle Scholar
  26. Hendriks, L., Van Broekhoven, C., Vanderberghe, A., Van De Peer, Y., and De Wachter, R. (1988b) Primary and secondary structure of the 18S ribosomal RNA of the bird spider Eurypelma californica and evolutionary relationships among eukaryotic phyla. Europ. J. Biochem. 177, 15–20.CrossRefGoogle Scholar
  27. Hendriks, L., Van de Peer, Y., Van Herks, M., Neefs, J. M., and De Wachter, R. (1990) The 18S ribosomal RNA sequence of the sea anemone Anemonia sulcata and its evolutionary position among other eukaryotes. Fedn. Europ. Biochem. Soc. Lett. 269, 445–449.Google Scholar
  28. Hennig, W. (1966) Phylogenetic Systematics. University of Illinois Press, Urbana.Google Scholar
  29. Holland, P. W. H., Hacker, A. M., and Williams, N. A. (1991) A molecular analysis of the phylogenetic affinities of Saccoglossus cambresis Brambell & Cole (Hemichordata). Phil. Trans. Roy. Soc. London, B 332, 185–189.CrossRefGoogle Scholar
  30. Hyman, L. H. (1940) The Invertebrates; Protozoa through Ctenophora. McGraw Hill, New York.Google Scholar
  31. Hyman, L. H. (1951a) The Invertebrates; Platyhelminthes and Rhynchocoela. McGraw Hill, New York.Google Scholar
  32. Hyman, L. H. (1951b) The Invertebrates; Acanthocephala, Aschelminthes, and Entoprocta. McGraw Hill, New York.Google Scholar
  33. Iftode, F., Cohen, J., Ruiz, F., Torres Rueda, A., Chen-Shan, L., Adoutte, A., and Beisson, J. (1989) Development of surface pattern during division in Paramecium. I. Mapping of duplication and reorganization of cortical cytoskeletal structures in the wild type. Development 105, 191–211.Google Scholar
  34. Jeffries, R. P. S. (1986) The Ancestry of the Vertebrates. British Museum (N.H.) London.Google Scholar
  35. Johannes, E., Brasman, J. M., and Sanders, D. (1991) Calcium channels and signal transduction in plant cells. BioEssays 13, 331–336.Google Scholar
  36. Kelly-Borges, M., Bergquist, P. R., and Bergquist P. L. (1991) Phylogenetic relationships within the Order Hadromerida (Porifera, Demospongiae, Tetractinomorpha) as indicated by ribosomal RNA sequence comparisons. Biochem. Syst. Ecol. 19, 117–125.CrossRefGoogle Scholar
  37. Krumlauf, R. (1992) Evolution of the vertebrate Hox homeobox genes. BioEssays 14, 245–252.Google Scholar
  38. Kung, C., and Saimi Y. (1982) The physiological basis of taxes in Paramecium. Annu. Rev. Physiol. 44, 519–534.CrossRefGoogle Scholar
  39. Lake, J. A. (1990) Origin of the Metazoa. Proc. Natl Acad. Sci. USA 87, 763–766.CrossRefGoogle Scholar
  40. Lake, J. A. (1991) Tracing origins with molecular sequences: metazoan and eukaryotic beginnings. Trends Biochem. Sci. 16, 46–50.CrossRefGoogle Scholar
  41. Li, W. H., and Graur, D. (1991) Fundamentals of Molecular Evolution, pp. 1–284. Sinauer Associates, Inc., Publishers, Sunderland, MA, USA.Google Scholar
  42. Mayr, E., and Ashlock, P. D. (1991) Principles of Systematic Zoology, pp. 1–475. McGraw-Hill Inc., New York.Google Scholar
  43. Miceli, C., La Terza, A., Bradshaw, R. A., and Luporini, P. (1992) Identification and structural characterization of a cDNA clone encoding a membrane-bound form of the polypeptide pheromone Er-1 in the ciliate protozoan Euplotes raikovi. Proc. Natl Acad. Act USA 89, 1988–1992.CrossRefGoogle Scholar
  44. Nei (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.Google Scholar
  45. Nielsen, C. (1989) Phylogeny and molecular data. Science 243, 548.Google Scholar
  46. Patterson, C. (1989) Phylogenetic relations of major groups: conclusions and prospects, in: The Hierarchy of Life. Molecules and Morphology in Phylogenetic Analysis, pp. 471–488. Eds B. Fernholm, K. Bremer and H. Jörnvall. Excerpta Medica, Amsterdam.Google Scholar
  47. Penny, D., Hendy, M. D., and Steel, M. A. (1992) Progress with methods for constructing evolutionary trees. TREE 7, 73–79.Google Scholar
  48. Perasso, R., Baroin, A., Qu, L. H., Bachellerie, J. P., and Adoutte, A. (1989) Origin of the algae. Nature 339, 142–144CrossRefGoogle Scholar
  49. Qu, L. H., Michot, B., and Bachellerie, J. P. (1983) Improved methods for structure probing in large RNAs: a rapid “heterologous” sequencing approach is coupled to the direct mapping of nuclease accessible sites. Application to the 5′ terminal domain if eukaryotic 28S rRNA. Nucl. Acids Res. 11, 5903–5920.CrossRefGoogle Scholar
  50. Qu, L. H., Nicoloso, M., and Bachellerie, J. P. (1988) Phylogenetic calibration of the 5′ terminal domain of large rRNA achieved by determining twenty eukaryotic sequences. J. Molec. Evol. 28, 113–124.CrossRefGoogle Scholar
  51. Raff, R. A., Field, K. G., Olsen, G. J., Giovannoni, S. J., Lane, D. J., Ghiselin, M. T., Pace, N. R., and Raff, E. C. (1989) Metazoan phylogeny based on analysis of 18S ribosomal RNA, in: The Hierarchy of Life. Molecules and Morphology in Phylogenetic Analysis, pp. 247–260. Eds B. Fernholm, K. Bremer and H. Jörnvall. Excerpta Medica, Amsterdam.Google Scholar
  52. Rosati, G., and F. Verni, (1991) Sexual recognition in Protozoa: chemical signals and transduction mechanisms. Zool. Sci. 8, 415–429.Google Scholar
  53. Saitou, N., and Nei, M. (1987) The Neighbor-Joining method: a new method for reconstructing phylogenetic trees. Molec. Biol. Evol. 4, 406–425.Google Scholar
  54. Salvini-Plawen, L. von (1985) Early evolution and the primitive groups, in: The Mollusca, pp. 59–150. Vol. 10, Evolution. Eds E. R. Trueman and M. R. Clarke. Academic Press, London, New York.Google Scholar
  55. Schlegel, M. (1991) Protist evolution and phylogeny as discerned from small subunit ribosomal RNA sequence comparisons. Europ. J. Protist. 27, 207–219.CrossRefGoogle Scholar
  56. Schram, F. R. (1991) Cladistic analysis of metazoan phyla and the placement of fossil problematica, in: The Early Evolution of Metazoa and the Significance of Problematic Taxa, pp. 35–46. Eds A. M. Simonetta and S. Conway Morris. Cambridge University Press, Cambridge.Google Scholar
  57. Sidow, A., and Bowman, B. H. (1991) Molecular phylogeny. Curr. Opin. Gen. Devl. 1, 451–456.CrossRefGoogle Scholar
  58. Siewing, R. (1980) Das Archicoelomatenkonzept. Zool Jb. Syst. 103, 439–482.Google Scholar
  59. Sogin, M. L. (1991) Early evolution and the origin of eukaryotes. Curr. Opin. Genet. Devl. 1, 457–463CrossRefGoogle Scholar
  60. Sonneborn, T. M. (1977) Genetics of cellular differentiation: stable nuclear differentiation in eukaryotic unicells. Annu. Rev. Genet. 11, 349–367.CrossRefGoogle Scholar
  61. Swofford, D. L., and Olsen, G. J. (1990) Phylogeny reconstruction, in: Molecular Systematics, pp. 411–501. eds D. M. Hillis and C. Moritz.Google Scholar
  62. Turbeville, J. M., Field, K. G., and Raff, R. A. (1992) Phylogenetic position of the phylum Nemertini, inferred from 18S rRNA sequences: molecular data as a test of morphological character homology. Molec. Biol. Evol. 9, 235–249.Google Scholar
  63. Turbeville, J. M., Pfeifer, D. M., Field, K. G., and Raff, R. A. (1991) The phylogenetic status of Arthropods, as inferred from 18S rRNA sequences. Molec. Biol. Evol. 8, 669–686.Google Scholar
  64. Van Houten, J. (1990) Chemosensory transduction in Paramecium, in: Biology of the Chemotactic Response, pp. 297–321. Eds J. P. Armitage and J. M. Lackie. Cambridge University Press.Google Scholar
  65. Walker, W. F. (1989) Phylogeny and molecular data. Science 243, 548–549.CrossRefGoogle Scholar
  66. Whittington H. B. (1985) The Burgess Shale. Yale University Press, New Haven & London.Google Scholar
  67. Wiley (1981) Phylogenetics: The Theory and Practice of Phylogenetic Systematics. John Wiley & Sons, New York.Google Scholar
  68. Willmer P. (1990) Invertebrate Relationships. Patterns in Animal Evolution, pp. 1–400. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  69. Woese, C. R. (1987) Bacterial evolution. Microbiol. Rev. 51, 221–271.Google Scholar
  70. Woese, C. R., Kandler, O., and Wheelis, M. L. (1990) Towards a natural system of organisms: Proposal for the domains Archae, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579.CrossRefGoogle Scholar
  71. Wolpert, L. (1990) The evolution of development. Biol. J. Linn. Soc. 39, 109–124.CrossRefGoogle Scholar
  72. Wolters, J. (1991) The troublesome parasites — molecular and morphological evidence that Apicomplexa belongs to the dinoflagellate-ciliate clade. BioSystems 25, 75–83.CrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag Basel/Switzerland 1993

Authors and Affiliations

  1. 1.Laboratoire de Biologie Cellulaire 4 (URA D-1134 CNRS)Université Paris XIOrsay CedexFrance

Personalised recommendations