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Part of the book series: Developments in Hydrobiology ((DIHY,volume 179))

Abstract

The biphasic life cycle in annelids is characterized by two completely different types of organisation, i.e. the acoelomate/pseudocoelomate larva and the coelomate adult. Based on this observation the recent literature on the different assumptions on the organisation of the bilaterian stem species with special emphasis on the evolution of the annelid body plan is reviewed. The structure of the coelomic lining ranges between a simple myoepithelium composed of epithelio-muscle cells and a non-muscular peritoneum that covers the body wall muscles. The direction of the evolution of these linings is discussed with respect to coelomogenesis. As the coelom originates from mesodermal cell bands, different assumption on the acoelomate condition in Bilateria can be substantiated. The origin of segmentation in annelids is explained by current hypothesis. Although no final decision can be made concerning the origin of the annelid body plan and the organisation of the bilaterian stem species, this paper elaborates those questions that need to be resolved to unravel the relation between the different body plans.

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References

  • Adoutte, A., G. Balavoine, N. Lartillot & R. de Rosa, 1999. Animal evolution the end of the intermediate taxa? Trends in Genetics 15: 105–108.

    Article  Google Scholar 

  • Adoutte, A., G. Balavoine, N. Lartillot, O. Lespinet, B. Prudʻhomme & R. de Rosa. 2000. The new animal phylogeny: reliability and implications. Proceedings of the National Academy of Sciences, USA 97: 4453–4456.

    Article  CAS  Google Scholar 

  • Anderson, D. T., 1973. Embryology and Phylogeny in Annelids and Arthropods. Pergamon, Oxford, 495 pp.

    Google Scholar 

  • Ax, P., 1996. Multicellular Aminals. A New Approach to the Phylogenetic Order in Nature. Springer, Berlin, Heidelberg, New York, 225 pp.

    Google Scholar 

  • Balavoine, G., 1998. Are Platyhelminthes coelomates without a coelom? An argument based on the evolution of Hox genes. American Zoologist 38: 843–858.

    CAS  Google Scholar 

  • Bartolomaeus, T., 1994. On the ultrastructure of the coelomic lining in Annelida, Echiura and Sipuncula. Microfauna Marina 9: 171–220.

    Google Scholar 

  • Budd, G. E., 2001. Why are arthropods segmented? Evolution and Development 3: 332–342.

    Article  PubMed  CAS  Google Scholar 

  • Budd, G. E., 2003. Arthropods as ecdysozoans: the fossil evidence. In Legakis, A., S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki (eds), The new Panorama of Animal Evolution. Proceedings XVIII International Congress of Zoology, Pensoft, Sofia: 479–487.

    Google Scholar 

  • Clark, R. B., 1964. Dynamics in Metazoan Evolution. The Origin of the Coelom and Segments. Clarendon, Oxford, 313 pp.

    Google Scholar 

  • Davidson, E. H., K. J. Peterson & R. A. Cameron, 1995. Origin of adult bilaterian body plans: evolution of developmental regulatory mechanisms. Science 270: 1319–1325.

    PubMed  CAS  Google Scholar 

  • Davis, G. K. & N. H. Patel, 1999. The origin and evolution of segmentation. Trends in Genetics 15: M68–M72.

    Article  CAS  Google Scholar 

  • Fawcett, D. W., 1994. A Textbook of Histology. Chapman & Hall, New York, 964 pp.

    Google Scholar 

  • Fransen, M. E., 1980. Ultrastructure of the coelomic organisation. I. Archiannelids and other small polychaetes. Zoomorphologie 95: 235–249

    Article  Google Scholar 

  • Fransen, M. E., 1982. The role of ECM in the development of invertebrates: a phylogeneticists view. In Hawkes S. & J. L. Wang (eds), Extracellular Matrix 478. Academic, New York: 177–181.

    Google Scholar 

  • Fransen, M., 1988. Coelomic and vascular system. In Westheide W. & C. O. Hermans (eds), The Ultrastructure of Polychaeta. Microfauna Marina 4: 199–213.

    Google Scholar 

  • Gardiner, S. L., 1992. Polychaeta. General organization, integument, musculature, coelom, and vascular system. In Harrison, F. W. & S. L. Gardiner (eds), Microscopic Anatomy of Invertebrates Vol. 7 Annelida. Wiley-Liss, New York: 19–52.

    Google Scholar 

  • Garey, J. R., 2003. Ecdysozoa: the evidence for a close relationship between arthropods and nematodes. In Legakis, A., S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki (eds), The new Panorama of Animal Evolution. Proceedings XVIII International Congress of Zoology, Pensoft, Sofia: 503–509.

    Google Scholar 

  • Goodrich, E. S., 1946. The study of nephridia and genital ducts since 1895. Quarterly Reviews of microscopical Science, New Series 86: 113–392.

    Google Scholar 

  • Green, C. R., 1981. A clarification of the two types of invertebrate pleated septate junction. Tissue & Cell 13: 173–188.

    CAS  Google Scholar 

  • Green, C. R. & P. R. Bergquist, 1982. Phylogenetic relationships within the invertebrata in relation to the structure of septate junctions and the development of ‘occluding’ junctional types. Journal of Cell Sciences 53: 279–305.

    Google Scholar 

  • Hartmann, W., 1963. A critique of the enterocoele theory. In Dougherty, C. E. (ed.), The Lower Metazoa Vol. 5. University California, Berkeley: 55–77.

    Google Scholar 

  • Haszprunar, G., 1996. The Mollusca: coelomate turbellarians or mesenchymate annelids? In Taylor, J. (ed.), Origin and Evolutionary Radiation of the Mollusca. Oxford University, Oxford: 1–28.

    Google Scholar 

  • Heimler, W., 1981a. Untersuchungen zur Larvalentwicklung von Lanice conchilega (Pallas) 1766 (Polycheata, Terebellomorpha). Teil I: Entwicklungsablauf. Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere 106: 12–45.

    Google Scholar 

  • Heimler, W., 1981b. Untersuchungen zur Larvalentwicklung von Lanice conchilega (Pallas) 1766 (Polycheata, Terebellomorpha). Teil II: Bau und Ultrastruktur der Trochophora-Larve. Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere 106: 236–277.

    Google Scholar 

  • Heimler, W., 1983. Untersuchungen zur Larvenentwicklung von Lanice conchilega (Pallas) 1766 (Polychaeta, Terebellomorpha) Teil III: Bau und Struktur der Aulophora-Larve. Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere 110: 411–478.

    Google Scholar 

  • Heimler, W., 1988. Larvae. In Westheide, W. & C. O. Hermans (eds), The Ultrastructure of Polychaeta. Microfauna Marina 4: 353–371.

    Google Scholar 

  • Hyman, L. H., 1951. The Invertebrates: Platyhelminthes and Rhynchocoela. The Acoelomate Bilateria. McGraw-Hill. New York, 550 pp.

    Google Scholar 

  • Jouve, C., T. Iimura & O. Pourquier, 2002. Onset of the segmentation clock in the chick embryo: evidence for oscillations in the somite precursors in the primitive streak. Development 129: 1107–1117.

    PubMed  CAS  Google Scholar 

  • Kleinig, H. & U. Maier, 1999. Zellbiologie. Gustav Fischer, Stuttgart, Jena, 534 pp.

    Google Scholar 

  • Ladurner, P. & R. M. Rieger, 2000. Embryonic muscle development of Convoluta pulchra (Turbellaria-Acoelomorpha, Platyhelminthes). Developmental Biology 222: 359–375.

    Article  PubMed  CAS  Google Scholar 

  • Minelli, A., 1995. Body cavities and body segmentation: problems of homology and phylogenetic reconstruction. In Lanzavecchia, G. R. Valvassori & M. D. Candia Carnevalli (eds), Body Cavities: Function and Phylogeny. Selected Symposia and Monographs, U.Z.I., 8, Mucchi, Modena: 69–73.

    Google Scholar 

  • Nielsen, C., 2001. Animal Evolution. Interrelationships of the Living Phyla. Oxford University, New York, 563 pp.

    Google Scholar 

  • Pedersen, K. J., 1991. Structure and composition of basement membranes and other basal matrix systems in selected invertebrates. Acta Zoologica (Stockholm) 72: 181–201.

    Article  Google Scholar 

  • Peterson, K. J. & E. H. Davidson, 2000. Regulatory evolution and the origin of the bilaterians. Proceedings of the National Academy of Sciences of the USA 97: 4430–4433.

    PubMed  CAS  Google Scholar 

  • Peterson, K. J., R. A. Cameron & E. H. Davidson, 1997. Setaside cells in maximal indirect development: evolutionary and developmental significance. Bioessays 19: 623–631.

    Article  PubMed  CAS  Google Scholar 

  • Peterson, K. J., R. A. Cameron & E. H. Davidson, 2000. Bilaterian origins: significance of new experimental observations. Developmental Biology 219: 1–17.

    Article  PubMed  CAS  Google Scholar 

  • Potswald, H., 1981. Abdominal segment formation in Spirorbis moerchi (Polychaeta). Zoomorphology 97: 225–245.

    Article  Google Scholar 

  • Reiter, D., B. Boyer, P. Ladurner, G. Mair, W. Salvenmoser & R. Rieger, 1996. Differentiation of the body wall musculature in Macrostomum hystricinum marinum and Hoploplana inquilina (Plathelminthes), as models for muscle development in lower Spiralia. Rouxs Archives of Developmental Biology 205: 410–423.

    Google Scholar 

  • Remane, A., 1950. Die Entstehung der Metamerie der Wirbellosen. Zoologischer Anzeiger, Supplementband 14: 16–23.

    Google Scholar 

  • Remane, A., 1954. Die Geschichte der Tiere. In Herberer, G. (ed.), Die Evolution der Organismen. Vol. 2, 2nd edn. Fischer, Stuttgart: 340–422.

    Google Scholar 

  • Remane, A. 1963a. The enterocelic origin of the coelom. In. Dougherty, C. E. et al. (eds), The Lower Metazoa. University of California, Berkeley, CA: 78–90.

    Google Scholar 

  • Remane, A. 1963b. The evolution of the Metazoa from colonial flagellates vs. plasmodial ciliates. In Dougherty, C. E. et al. (eds), The Lower Metazoa. Comparative Biology and Phylogeny. University of California, Berkeley, CA: 23–32.

    Google Scholar 

  • Rieger, R. M., 1985. The phylogenetic status of the acoelomate organization within the bilateria. a histological perspective. In Conway-Morris, S., J. D. George, R. Gibson & H. M. Platt (eds), The Origins and Relationships of Lower Invertebrates. Clarendon, Oxford: 101–122.

    Google Scholar 

  • Rieger, R. M., 1986. Über den Ursprung der Bilateria: die Bedeutung der Ultrastrukturforschung für ein neues Verstehen der Metazoenevolution. Verhandlungen der Deutschen Zoologischen Gesellschaft 79: 31–50. (English translation at http://www.umsci.maine.edu./biology/labs/original/)

    Google Scholar 

  • Rieger, R. M., 1994. Evolution of the ‘lower’ Metazoa. In Bengtson, S. (ed.), Early Life on Earth. Nobel Symposium no. 84. Columbia University, New York: 475–488 (references on 517–598).

    Google Scholar 

  • Rieger, R. M., 1991a. Neue Organisationstypen aus der Sandlückenfauna: die Lobatocerebriden und Jenneria pulchra. Verhandlungen der Deutschen Zoologischen Gesellschaft 84: 247–259.

    Google Scholar 

  • Rieger, R. M., 1991b. Jennaria pulchra, nov. gen. nov. spec., eine den psammobionten Anneliden nahestehende Gattung aus dem Küstengrundwasser von North Carolina. Berichte des Naturwissenschaftlich Medizinischen Vereins in Innsbruck 78: 203–215.

    Google Scholar 

  • Rieger, R. M. & P. Ladurner, 2001. Searching for the stem species of the Bilateria. Belgian Journal of Zoology, 131(Supplement 1): 27–34.

    Google Scholar 

  • Rieger, R. M. & P. Ladurner, 2003. The significance of muscle cells for the origin of mesoderm in Bilateria. Integrative & Comparative Biology 43: 47–54.

    Google Scholar 

  • Rieger, R. M. & J. Lombardi, 1987. Comparative ultrastructure of coelomic linings in echinoderm tube feet and the evolution of peritoneal linings in the Bilateria. Zoomorphology 107: 191–208.

    Article  Google Scholar 

  • Rieger, R. M. & S. Tyler, 1979. The homology theorem in ultrastructure research. American Zoologist 19: 654–666.

    Google Scholar 

  • Ruppert, E. E. & K. J. Carle, 1983. Morphology of metazoan circulatory systems. Zoomorphology 103: 193–208.

    Article  Google Scholar 

  • Salvini-Plawen, L. v. & T. Bartolomaeus, 1995. Mollusca: mesenchymata with a coelom. In Lanzavecchia, G. R. Valvassori & M. D. Candia Carnevalli (eds), Selected Symposia and Monographs U.Z.I., 8, E. Muncchi, Modena: 75–92.

    Google Scholar 

  • Schiebler, T. H. & W. Schmidt, 2002. Anatomie. Springer, Berlin Heidelberg, 892 pp.

    Google Scholar 

  • Schmidt-Rhaesa, A., 2003. Integrative approaches to phylogenetic relationships of arthropods: introduction to the symposium. In Legakis, A., S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki (eds), The new Panorama of Animal Evolution. Proceedings XVIII International Congress of Zoology, Pensoft, Sofia: 461–466.

    Google Scholar 

  • Schmidt-Rhaesa, A., T. Bartolomaeus, C. Lemburg, U. Ehlers & J. R. Garey, 1998. The position of the Arthopoda in the phylogenetic system. Journal of Morphology 238: 413–418.

    Article  Google Scholar 

  • Scholtz, G., 2003. Is the taxon Articulata obsolete? Arguments in favour of a cose relationship between annelids and arthropods. In Legakis, A., S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki (eds), The new Panorama of Animal Evolution. Proceedings XVIII International Congress of Zoology, Pensoft, Sofia: 489–501.

    Google Scholar 

  • Shankland, M. & E. C. Seaver, 2000. Evolution of the bilaterian body plan: what have we learned from annelids? Proceedings of the National Academy of Sciences of the USA 97: 4434–4437.

    Article  PubMed  CAS  Google Scholar 

  • Siewing, R., 1985. Lehrbuch der Zoologie Vol. 2, Systematik. Fischer, Stuttgart, New York, 1107 pp.

    Google Scholar 

  • Smith, J. P. S., J. Lombardi & R. M. Rieger, 1986. Ultrastructure of the body cavity lining in a secondary acoelomate, Microphthalmus cf. listensis Westheide (Polychaeta, Hesionidae). Journal of Morphology 188: 257–271.

    Article  Google Scholar 

  • Stauber, M., 1993. The latern of Aristotle: organization of its coelom and origin of its muscles (Echinodermata, Echinoida). Zoomorphology 113: 137–151.

    Article  Google Scholar 

  • Takeichi, M., 1991. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251: 1451–1455.

    PubMed  CAS  Google Scholar 

  • Tepass, U., K. Truong, D. Goudt, M. Ikura & M. Pfeifer, 2000. Cadherins in embryonic and neural morphogenesis. Nature Reviews of Molecular Cell Biology 1: 91–100.

    CAS  Google Scholar 

  • Turbeville J. M., 1986. An ultrastructural analyis of coelomogenesis in the hoplonemertine Prosorhochmus americanus and the polychaete Magelona sp. Journal of Morphology 187: 51–60.

    Article  Google Scholar 

  • Tyler, S., 1988. The role of function in determination of homology and convergence — examples from invertebrate adhesive organs. In Ax, P., U. Ehlers & B. Sopott-Ehlers (eds), Free-living and Symbiotic Plathelminthes. Progress in Zoology 36: 331–374.

    Google Scholar 

  • Tyler, S., 2001. Origin and relationship of lower flatworms. In Littlewood, D. T. J. & R. A. Bray (eds), Interrelationsships of the Platyhelminthes. Taylor and Francis, New York: 3–12.

    Google Scholar 

  • Tyler, S., 2003. Epithelum — the primary building block for metazoan complexity. Integrative and Comparative Biology 43: 55–63.

    Google Scholar 

  • Wanninger, A. & G. Haszprunar, 2002. Chiton Myogenesis: Perspectives for the development and evolution of larval and adult muscle systems in molluscs. Journal of Morphology 251: 103–113.

    Article  PubMed  Google Scholar 

  • Westheide, W., 1987. Progenesis as a principle in meiofauna evolution. Journal of Natural History 21: 843–854.

    Google Scholar 

  • Westheide, W., 1997. The direction of evolution within the Polychaeta. Journal of Natural History 31: 1–15.

    Google Scholar 

  • Westheide, W. & R. Rieger, 1996. Spezielle Zoologie. Teil 1: Einzeller und Wirbellose Tiere. Gustav Fischer, Stuttgart, 909 pp.

    Google Scholar 

  • Willmer, P., 1991. Invertebrate Relationships. Patterns in Animal Evolution. Cambridge University, Melbourne: 400 pp.

    Google Scholar 

  • Willmer, P., 1995. Modern approaches to the phylogeny of body cavities. In Lanzavecchia, G., R. Valvassori & M. D. Candia Carnevalli (eds), Body Cavities: Function and Phylogeny. Selected Symposia and Monographs, U.Z.I., 8, Mucchi, Modena: 23–39.

    Google Scholar 

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Rieger, R.M., Purschke, G. (2005). The coelom and the origin of the annelid body plan. In: Bartolomaeus, T., Purschke, G. (eds) Morphology, Molecules, Evolution and Phylogeny in Polychaeta and Related Taxa. Developments in Hydrobiology, vol 179. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3240-4_8

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