Journal of Molecular Evolution

, Volume 42, Issue 5, pp 552–559 | Cite as

18S rRNA suggests that Entoprocta are protostomes, unrelated to Ectoprocta

  • L. Y. Mackey
  • B. Winnepenninckx
  • R. De Wachter
  • T. Backeljau
  • P. Emschermann
  • J. R. Garey


The Ento- and Ectoprocta are sometimes placed together in the Bryozoa, which have variously been regarded as proto- or deuterostomes. However, Entoprocta have also been allied to the pseudocoelomates, while Ectoprocta are often united with the Brachiopoda and Phoronida in the (super)phylum Lophophorata. Hence, the phylogenetic relationships of these taxa are still much debated. We determined complete 18S rRNA sequences of two entoprocts, an ectoproct, an inarticulate brachiopod, a phoronid, two annelids, and a platyhelminth. Phylogenetic analyses of these data show that (1) entoprocts and lophophorates have spiralian, protostomous affinities, (2) Ento- and Ectoprocta are not sister taxa, (3) phoronids and brachiopods form a monophyletic clade, and (4) neither Ectoprocta or Annelida appear to be monophyletic. Both deuterostomous and pseudocoelomate features may have arisen at least two times in evolutionary history. These results advocate a Spiralia-Radialia-based classification rather than one based on the Protostomia-Deuterostomia concept.

Key words

Ectoprocta Entoprocta Phoronida Brachiopoda Lophophorata 18S rRNA Molecular phylogeny Oligochaeta Hirudinida Polychaeta 





maximum parsimony


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1995) Current protocols in molecular biology. Greene, New YorkGoogle Scholar
  2. Bej AK, Mahbubani MH, Atlas RM (1991) Amplifications of nucleic acids by polymerase chain reaction (PCR) and other methods and their applications. Crit Rev Biochem Mol Biol 26:301–334PubMedGoogle Scholar
  3. Bergström J (1986) Metazoan evolution—a new model. Zool Scr 15:189–200Google Scholar
  4. Bevan IS, Rapley R,Walker MR (1992) Sequencing of PCR-amplified DNA. PCR Methods Appl 1:222–228PubMedGoogle Scholar
  5. Bremer K (1988) The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 2:795–803Google Scholar
  6. Brusca RC, Brusca GJ (1990) Invertebrates. Sinauer, Sunderland, MAGoogle Scholar
  7. Clark AH (1921) A new classification of animals. Bull Inst Oceanogr Monaco 400:1–24Google Scholar
  8. Clark RB (1969) Systematics and phylogeny: Annelida, Echiura, Sipuncula. In: Florkin M, and Scheer BT (eds) Chemical zoology, vol IV: Annelida, Echiura and Sipuncula. Academic Press, New York, pp 1–68Google Scholar
  9. Cori C (1936) Kamptozoa. In: Bronn HG (ed) Klassen and Ordnungen des Tierreichs 4, II. Abt, 4. Buch Akad Verlagsgesellschaft, Leipzig, pp 1–119Google Scholar
  10. De Rijk P, De Wachter R (1993) DCSE, an interactive tool for sequence alignment and secondary structure research. Comput Appl Biosci 9:735–740PubMedGoogle Scholar
  11. Donoghue MJ, Olmstead RG, Smith JF, Palmer JD (1992) Phylogenetic relationships of Dipsacales based on RbcL sequences. Ann MO Bot Gard 79:333–345Google Scholar
  12. Eckert KA, Kunkel TA (1991) DNA polymerase fidelity and the polymerase chain reaction. PCR Methods Appl 1:17–24PubMedGoogle Scholar
  13. Eernisse DJ, Albert IS, Anderson FE (1992) Annelida and Arthropoda are not sister taxa: a phylogenetic analysis of spiralian metazoan morphology. Syst Biol 41:305–330Google Scholar
  14. Emig C (1984) On the origin of the Lophophorata. Z Zool Syst Evolutforsch 22:91–94Google Scholar
  15. Emschermann P (1982) Les Kamptozoaires. Etat actuel de nos connaissances sur leur anatomic, leur développement, leur biologie et leur position phylogénétique. Bull Soc Zool Fr 107:317–344Google Scholar
  16. Emschermann P (1985) Cladus Kamptozoa. In: Siewing R (ed) Lehrbuch der Zoologie. Band 11: Systematik. Gustav Fisher Verlag, Stuttgart, pp 576–586Google Scholar
  17. Emschermann P (1987) A circulating water tank for culturing sessile or hemisessile aquatic organisms in a continuous water current. Arch Hydrobiol 108:425–438Google Scholar
  18. Felsenstein J (1988) Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22:521–565CrossRefPubMedGoogle Scholar
  19. Field KG, Olsen GJ, Lane DJ, Giovannoni SJ, Ghiselen MT, Raff EC, Pace NR, Raff RA (1988) Molecular phylogeny of the animal kingdom. Science 239:748–753PubMedGoogle Scholar
  20. Ghiselen MT (1988) The origin of molluscs in the light of molecular evidence. In: Harvey PH, Partridge L (eds) Oxford surveys in evolutionary biology, vol 5. Oxford University Press, Oxford, pp 66–95Google Scholar
  21. Gustus RM, Cloney RA (1972) Ultrastructural similarities between setae of brachiopods and polychaetes. Acta Zool 53:229–233Google Scholar
  22. Gutmann WF (1978) Brachiopods: biomechanical interdependencies governing their origin and phylogeny. Science 100:890–893Google Scholar
  23. Halanych KM, Bacheller JD, Aguinaldo AMA, Liva SM, Hillis DM, Lake JA (1995) Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 267:1641–1643PubMedGoogle Scholar
  24. Hempstead PG, Regular SC, Ball IR (1990) A method for the preparation of high-molecular-weight DNA from marine and freshwater triclads. DNA Cell Biol 9:57PubMedGoogle Scholar
  25. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192Google Scholar
  26. Hyman LH (1951) The invertebrates: Acanthocephala, Aschelminthes and Entoprocta-the pseudocoelomate Bilateria. McGraw-Hill, New YorkGoogle Scholar
  27. Hyman LH (1959) The invertebrates: smaller coelomate groups: Chaetognatha, Hemichordata, Pogonophora, Phoronida, Ectoprocta, brachiopoda, Sipunculida. McGraw-Hill, New YorkGoogle Scholar
  28. Jägersten G (1972) Evolution of the metazoan life cycle. Academic Press, New YorkGoogle Scholar
  29. Jeuniaux C (1982) La chitine dans le règne animal. Bull Soc Zool FR 107:363–386Google Scholar
  30. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  31. Kumar S (1995) PHYLTEST: phylogeny hypothesis testing using the minimum evolution method. Pennsylvania State University, State CollegeGoogle Scholar
  32. Lorenzen S (1985) Phylogenetic aspects of pseudocoelomate evolution. In: Conway-Morris S, George JD, Gibson R, Platt HM (eds) The origins and relationships of lower invertebrates. Clarendon Press, Oxford, pp 210–223Google Scholar
  33. Nielsen C (1977) The relationships of Entoprocta, Ectoprocta and Phoronida. Am Zool 17:149–150Google Scholar
  34. Nielsen C (1994) Larval and adult characters in animal phylogeny. Am Zool 34:492–501Google Scholar
  35. Nielsen C (1995) Animal evolution, interrelationships of the living phyla. Oxford University Press, OxfordGoogle Scholar
  36. Olsen GJ, Woese CR (1993) Ribosomal RNA: a key to phylogeny. FASEB J 7:113–123PubMedGoogle Scholar
  37. Rzhetsky A, Kumar S, Nei M (1995) Four-cluster analysis: a simple method to test phylogenetic hypotheses. Mol Biol Evol 12:163–167PubMedGoogle Scholar
  38. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  39. Siewing R (1976) Probleme und neuere Erkenntnisse in der Gross-Systematik der Wirbellosen. Verh Dtsch Zool Ges Stuttgart 1976:59–83Google Scholar
  40. Siewing R (1980) Das Archicoelomatenkonzept. Zool Jb Syst 103:439–82Google Scholar
  41. Specht A (1988) Chaetae. In: Westheide W, Hermans CO. The ultrastructure of the Polychaeta: Microfauna Marina, vol. 4 pp 45-59Google Scholar
  42. Swofford DL (1993) Phylogenetic analysis using parsimony, version 3.1. Illinois Natural History Survey, ChampaignGoogle Scholar
  43. Valentine JW (1973) Coelomate superphyla. Syst Zool 22:97–102Google Scholar
  44. Van de Peer Y, Neefs JM, De Wachter R (1990) Small ribosomal subunit RNA sequences, evolutionary relationships among different life forms, and mitochondrial origins. J Mot Evol 30:463–476Google Scholar
  45. Van de Peer Y, De Wachter R (1993) TRECON: a software package for the construction and drawing of evolutionary trees. Comput Appl Biosci 9:177–182PubMedGoogle Scholar
  46. Van de Peer Y, Van den Broeck I, De Rijk R, De Wachter R (1994) Database on the structure of small ribosomal subunit RNA. Nucleic Acids Res 22:3488–3494PubMedGoogle Scholar
  47. van der Auwera G, Chapelle S, De Wachter R (1994) Structure of the large ribosomal subunit RNA of Phytophtora megasperrna, and phylogeny of Oomycetes. FEBS Lett 338:133–136PubMedGoogle Scholar
  48. von Salvini-Plawen, L (1982) A paedomorphic origin of the oligomerous animals? Zool Scr 11:77–81Google Scholar
  49. Willmer P (1990) Invertebrate relationships. Cambridge University Press, CambridgeGoogle Scholar
  50. Wilmotte A, Van de Peer Y, Goris A, Chapelle S, De Baere R, Nelissen B, Neefs JM, Hennebert G, De Wachter R (1993) Evolutionary relationships among higher Fungi inferred from small ribosomal subunit RNA sequence analysis. Syst Appl Microbiol 16:436–444Google Scholar
  51. Winnepenninckx B, Backeljau T, De Wachter R (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9:407PubMedGoogle Scholar
  52. Winnepenninckx B, Backeljau T, De Wachter R (1994) Small ribosomal subunit RNA and the phylogeny of Mollusca. Nautilus Suppl 2:98–110Google Scholar
  53. Winnepenninckx B, Backeljau T, Mackey LY, Brooks JM, De Wachter R, Kumar S, Garey JR (1995) 18S rRNA data indicate that the aschelminthes are polyphyletic in origin and consist of at least three distinct clades. Mol Biol Evol 12:1132–1137PubMedGoogle Scholar
  54. Zimmer RL (1973) Morphological and developmental affinities of the lophophorates. In: Larwood GP (ed) Living and fossil Bryozoa. Academic Press, London, pp 593–599Google Scholar

Copyright information

© Springer-Verlag New York Inc 1996

Authors and Affiliations

  • L. Y. Mackey
    • 1
  • B. Winnepenninckx
    • 2
  • R. De Wachter
    • 3
  • T. Backeljau
    • 3
  • P. Emschermann
    • 4
  • J. R. Garey
    • 1
  1. 1.Department of Biological SciencesDuquesne UniversityPittsburghUSA
  2. 2.Departement BiochemieUniversiteit Antwerpen (UIA)AntwerpenBelgium
  3. 3.Koninklijk Belgisch Instituut voor NatuurwetenschappenBrusselBelgium
  4. 4.Institut für Biologie IIIAlbert-Ludwig-Universität-FreiburgFreiburgGermany

Personalised recommendations