Skip to main content
Log in

Reconstructing the phylogeny of the Sipuncula

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Sipunculans are marine spiralian worms with possible close affinities to the Mollusca or Annelida. Currently 147 species, 17 genera, 6 families, 4 orders and 2 classes are recognized. In this paper we review sipunculan morphology, anatomy, paleontological data and historical affiliations. We have conducted cladistic analyses for two data sets to elucidate the phylogenetic relationships among sipunculan species. We first analyzed the relationships among the 45 species of Phascolosomatidea with representatives of the Sipunculidea as outgroups, using 35 morphological characters. The resulting consensus tree has low resolution and branch support is low for most branches. The second analysis was based on DNA sequence data from two nuclear ribosomal genes (18S rRNA and 28S rRNA) and one nuclear protein-coding gene, histone H3. Outgroups were chosen among representative spiralians. In a third analysis, the molecular data were combined with the morphological data. Data were analyzed using parsimony as the optimality criterion and branch support evaluated with jackknifing and Bremer support values. Branch support for outgroup relationships is low but the monophyly of the Sipuncula is well supported. Within Sipuncula, the monophyly of the two major groups, Phascolosomatidea and Sipunculidea is not confirmed. Of the currently recognized families, only Themistidae appears monophyletic. The Aspidosiphonidae, Phascolosomatidae and Golfingiidae would be monophyletic with some adjustments in their definition. The Sipunculidae is clearly polyphyletic, with Sipunculus nudus as the sister group to the remaining Sipuncula, Siphonosoma cumanense the sister group to a clade containing Siphonosoma vastumand the Phascolosomatidea, and Phascolopsis gouldi grouping within the Golfingiiformes, as suggested previously by some authors. Of the genera with multiple representatives, only Phascolosoma and Themiste are monophyletic as currently defined. We are aiming to expand our current dataset with more species in our molecular database and more detailed morphological studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • B. Åkesson (1958) ArticleTitleA study of the nervous system of the Sipunculoideae, with some remarks on the development of the two species Phascolion strombi Montagu and Golfingia minuta Keferstein Undersokningar over Oresund 38 1–249

    Google Scholar 

  • T. Backeljau B. Winnepenninckx L. De Bruyn (1993) ArticleTitleCladistic analysis of metazoan relationships: a reappraisal Cladistics 9 167–181 Occurrence Handle10.1111/j.1096-0031.1993.tb00216.x

    Article  Google Scholar 

  • W.C. Banta M.E. Rice (1976) A restudy of the Middle Cambrian Burgess Shale fossil worm, Ottoia prolifica M.E. Rice M. Todorovic (Eds) Proceedings of the International Symposioum on the Biology of the Sipuncula and Echiura Nauçno Delo Press Belgrade 79–90

    Google Scholar 

  • J.L. Boore J.L. Staton (2002) ArticleTitleThe mitochondrial genome of the sipunculid Phascolopsis gouldii supports its association with Annelida rather than Mollusca Molecular Biology and Evolution 19 127–137 Occurrence Handle11801741 Occurrence Handle1:CAS:528:DC%2BD38XovVCjtg%3D%3D

    PubMed  CAS  Google Scholar 

  • C.E. Brett J.F. Cottrell (1982) ArticleTitleSubstrate specificity in the Devonian tabulate coral Pleurodictyum Lethaia 15 247–262

    Google Scholar 

  • C.E. Brett W.D. Liddell K.L. Derstler (1983) ArticleTitleLate Cambrian hard substrate communities from Montana/Wyoming: the oldest known hardground encrusters Lethaia 16 281–289

    Google Scholar 

  • R.C. Brusca G.J. Brusca (1990) Invertebrates Sinauer Associates Sunderland

    Google Scholar 

  • R.C. Brusca G.J. Brusca (2003) Invertebrates. Second edition Sinauer Associates Sunderland

    Google Scholar 

  • S. Conway Morris (1989) ArticleTitleBurgess Shale faunas and the Cambrian explosion Science 246 339–346 Occurrence Handle17747916

    PubMed  Google Scholar 

  • S. Conway Morris (1998) The Crucible of Creation The Burgess Shale and the Rise of Animals. Oxford University Press Oxford 242

    Google Scholar 

  • E.B. Cutler (1994) The Sipuncula. Their Systematics, Biology and Evolution Cornell University Press Ithaca, NY 453

    Google Scholar 

  • E.B. Cutler P.E. Gibbs (1985) ArticleTitleA phylogenetic analysis of higher taxa in the phylum Sipuncula Systematic Zoology 34 162–173

    Google Scholar 

  • B. Cuvier (1830) Le règne animal distribué d’après son oranisation, pour servir de base a l’histoire naturelle des animaux et d’introduction à l’anatomie comparèe, Ser. 2, Vol. 3 Deterville Paris 1–244

    Google Scholar 

  • L. Dybas (1981) Sipunculans and echiuroids N.A. Ratcliff A.F. Rowley (Eds) Invertebrate Blood Cells Academic Press New York 161–188

    Google Scholar 

  • S.J. Edmonds (2000) Phylum Sipuncula P.L. Beesley G.J.B. Ross C.J. Glasby (Eds) Fauna of Australia 4, Polychaetes & Allies: The Southern Synthesis CSIRO Publishing Melbourne 375–400

    Google Scholar 

  • D.J. Eernisse J.S. Albert F.E. Anderson (1992) ArticleTitleAnnelida and Arthropoda are not sister taxa: a phylogenetic analysis of spiralian metazoan morphology Systematic Biology 41 305–330

    Google Scholar 

  • A. Erber D. Riemer M. Bovenschulte K. Weber (1998) ArticleTitleMolecular phylogeny of metazoan intermediate filament proteins Journal of Molecular Evolution 47 751–762 Occurrence Handle9847417 Occurrence Handle1:CAS:528:DyaK1cXotVGhsr4%3D

    PubMed  CAS  Google Scholar 

  • Eriksson, T., 1998. AutoDecay. Stockholm, Distributed by the Author. Department of Botany, Stockholm University

  • D.E. Ferrier P.W. Holland (2001) ArticleTitleSipunculan ParaHox genes Evolution & Development 3 263–270 Occurrence Handle1:CAS:528:DC%2BD38XitlWlsbw%3D

    CAS  Google Scholar 

  • M. Florkin (1975) Biochemical evidence for the phylogenetic relationships of the Sipuncula M.E. Rice M. Todorovic (Eds) Proceedings of the International Symposium on the biology of the Sipuncula and Echiura Naucno Delo Press Belgrade 95–110

    Google Scholar 

  • R.W. Frey G. Pemberton J.A. Fagerstrom (1984) ArticleTitleMorphological, ethological and environmental significance of the ichnogenera Scoyenia and Ancorichnus Journal of Paleontology 58 511–528

    Google Scholar 

  • P.E. Gibbs E.B. Cutler (1987) ArticleTitleA classification of the phylum Sipuncula Bulletin of the British Museum of Natural History (Zoology) 52 43–58

    Google Scholar 

  • G.A. Gill A.G. Coates (1977) ArticleTitleMobility, growth patterns and substrate in some fossil and Recent corals Lethaia 10 119–134

    Google Scholar 

  • G. Giribet (2002) ArticleTitleCurrent advances in the phylogenetic reconstruction of metazoan evolution. A new paradigm for the Cambrian explosion? Molecular Phylogenetics and Evolution 24 345–357 Occurrence Handle10.1016/S1055-7903(02)00206-3 Occurrence Handle12220976 Occurrence Handle1:CAS:528:DC%2BD38Xms1Ggt7w%3D

    Article  PubMed  CAS  Google Scholar 

  • G. Giribet D.L. Distel M. Polz W. Sterrer W.C. Wheeler (2000) ArticleTitleTriploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Platyhelminthes, and Chaetognatha: a combined approach of 18S rDNA sequences and morphology Systematic Biology 49 539–562 Occurrence Handle12116426 Occurrence Handle1:STN:280:DC%2BD38zntVKquw%3D%3D

    PubMed  CAS  Google Scholar 

  • C.R. Green P.R. Berquist (1982) ArticleTitlePhylogenetic relationships within the Invertebrata in relation to the structure of septate junctions and the development of occluding junctional types Journal of Cell Science 53 279–306

    Google Scholar 

  • R. Guralnick (2002) ArticleTitleA recapitulation of the rise and fall of the cell lineage research program: the evolutionary developmental relationship of cleavage to homology, body plans and life history Journal of History of Biology 35 527–567

    Google Scholar 

  • R.P. Guralnick D.R. Lindberg (2001) ArticleTitleReconnecting cell and animal lineages: what do cell lineages tell us about the evolution and development of Spiralia? Evolution 55 1501–1519 Occurrence Handle11580011 Occurrence Handle1:STN:280:DC%2BD3MrjtlaksQ%3D%3D

    PubMed  CAS  Google Scholar 

  • R.P. Henry (1987) ArticleTitleInvertebrate red blood cell carbonic anhydrase Journal of Experimental Zoology 242 113–116 Occurrence Handle10.1002/jez.1402420117 Occurrence Handle3110365 Occurrence Handle1:CAS:528:DyaL2sXksFKjtr4%3D

    Article  PubMed  CAS  Google Scholar 

  • P.W.H. Holland (1998) ArticleTitleMajor transitions in animal evolution: A developmental genetic perspective American Zoology 38 878–887

    Google Scholar 

  • D. Huang J. Chen J. Vannier J.I. Saiz Salinas (2004) ArticleTitleEarly Cambrian sipunculan worms from southwest China Proceedings of the Royal Society of London, Series B 271 1671–1676 Occurrence Handle10.1098/rspb.2004.2774

    Article  Google Scholar 

  • L.H. Hyman (1959) The Invertebrates 5, Smaller Coelomate Groups McGraw-Hill New York 783

    Google Scholar 

  • M. Ionescu-Varo M. Tufescu (1982) ArticleTitleQuantitative remarks on immune evolution in the animal series Rev. Roumaine Biol. série Biol. Animale 27 29–39

    Google Scholar 

  • W. Keferstein (1863) ArticleTitleBeiträge sur Kenntnis der Gattung Phascolosoma F.S. Leuck. Untersuchungen über niedere Seethiere Zeitschrift für Wissenschaftliche Zoologie 12 35–51

    Google Scholar 

  • W. Keferstein (1865a) ArticleTitleBeiträge zur anatomischen und systematischen Kenntnis der Sipunculiden Nachrichten der Gesellschaft der Wissenschaften, Göttingen 1865 189–209

    Google Scholar 

  • W. Keferstein (1865b) ArticleTitleBeiträge zur anatomischen und systematischen Kenntniss der Sipunculiden Zeitschrift für Wissenschaftliche Zoologie 15 404–445

    Google Scholar 

  • W. Keferstein (1866) ArticleTitleUntersuchungen uber einige amerikanische Sipunculiden Nachrichten von der Königlichen Gesellschaft der Wissenschaften und der Georg-August-Universität zu Göttingen 14 215–228

    Google Scholar 

  • W. Keferstein (1867) ArticleTitleUntersuchungen über einige amerikanische Sipunculiden Zeitschrift Fur Wissenschaftliche Zoologie 17 44–55

    Google Scholar 

  • W. Klepal (1987) ArticleTitleThe anchoring fiber apparatus in the sperm of Aspidosiphon sp. (Sipunculida) European Journal of Cell Biology Suppl 0 18

    Google Scholar 

  • E.Y. Kotetskii (1984) ArticleTitleThe phospholipid composition of Spongia, Coelenterata and free living Platyhelminthes, Nemertini, Annelida, Sipunculida and Echiurida Biologiya Morya 0 46–53

    Google Scholar 

  • J.A. Lake (1990) ArticleTitleOrigin of the Metazoa Proceedings of the National Academy of Sciences of the United State of America 87 763–766 Occurrence Handle1:STN:280:DyaK3c7jvV2jtQ%3D%3D Occurrence Handle10.1073/pnas.87.2.763

    Article  CAS  Google Scholar 

  • Lamarck, J. P. B. A., de M., 1816. Histoire naturelle des animaux sans vertébrés. Vol. 3. Verdière: Paris, 683 pp

  • W. Lehman A.G. Szent-Györgyi (1975) ArticleTitleRegulation of muscular contraction: distribution of actin control and myosin control in the animal kingdom Journal of General Physiology 66 1–30 Occurrence Handle10.1085/jgp.66.1.1 Occurrence Handle125778 Occurrence Handle1:CAS:528:DyaE2MXkslGqsrc%3D

    Article  PubMed  CAS  Google Scholar 

  • D.R. Livingstone A. Dezwaan M. Leopold E. Marteijn (1983) ArticleTitleStudies on the phylogenetic distribution of pyruvate oxidoreductases Biochem. Syst. Ecol 1 415–425

    Google Scholar 

  • D.R. Maddison W.P. Maddison (2001) MacClade Sinauer Associates Sunderland, MA

    Google Scholar 

  • C.P. Mangum (1990) ArticleTitleThe role of physiology and biochemistry in understanding animal phylogeny Proceedings of the Biological Society of Washington 103 235–247

    Google Scholar 

  • M. Marti Mus J. Bergstrom (2001) ArticleTitleThe skeleton-muscular system of hyolithids American Zoologist 41 1514

    Google Scholar 

  • A.B. Maxmen B.F. King E.B. Cutler G. Giribet (2003) ArticleTitleEvolutionary relationships within the protostome phylum Sipuncula: a molecular analysis of ribosomal genes and histone H3 sequence data Molecular Phylogenetics and Evolution 27 489–503 Occurrence Handle10.1016/S1055-7903(02)00443-8 Occurrence Handle12742753 Occurrence Handle1:CAS:528:DC%2BD3sXjs1Wmsrs%3D

    Article  PubMed  CAS  Google Scholar 

  • E.F. McBride M.D. Picard (1991) ArticleTitleFacies implications of Trichichnus and Chondrites in turbidites and hemipelagites, Marnoso-arenacea formation (Miocene), northern Apennine, Italy Palaios 6 281–290

    Google Scholar 

  • P.A. Meglitsch F.R. Schram (1991) Invertebrate Zoology Oxford University Press Oxford

    Google Scholar 

  • D. Nichols (1967) ArticleTitleThe origin of echinoderms Symposia of the Zoological Society of London 20 209–229

    Google Scholar 

  • Nielsen, C., 1987. Structure and function of metazoan ciliary bands and their phylogenetic significance. Acta Zoologica 68

  • C. Nielsen N. Scharff D. Eibye-Jacobsen (1996) ArticleTitleCladistic analyses of the animal kingdom Biological Journal of the Linnean Society 57 385–410 Occurrence Handle10.1006/bijl.1996.0023

    Article  Google Scholar 

  • F.J. Ocharan (1974) ArticleTitleSobre los nefridios de Phascolosoma granulatum (Sipuncula) Separata de la revista de la “Facultad de Ciencias” 15 21–40

    Google Scholar 

  • S.G. Pemberton D.R. Kobluk R.K. Yeo M.J. Risk (1980) ArticleTitleBoring Trypanites at the Silurian-Devonian disconformity in southern Ontario, Canada Journal of Paleontology 54 1258–1266

    Google Scholar 

  • K. Peterson D.J. Eernisse (2001) ArticleTitleAnimal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences Evolution & Development 3 170–205 Occurrence Handle1:CAS:528:DC%2BD38XisVWms7Y%3D Occurrence Handle10.1046/j.1525-142x.2001.003003170.x

    Article  CAS  Google Scholar 

  • G.E. Pickford (1947) Sipunculida. In Encyclopedia Britannica, Vol. 20 niversity of Chicago Chicago 717–718b

    Google Scholar 

  • J.F. Pilger M.E. Rice (1987) ArticleTitleUltrastructural evidence for the contractile vessel of sipunculans as a possible ultrafiltration site American Zoology 27 810a

    Google Scholar 

  • A. Pisera (1987) ArticleTitleBoring and nestling organisms from Upper Jurassic coral colonies from Northern Poland Acta Palaeontologia Polonica 32 83–104

    Google Scholar 

  • G. Purschke F. Wolfrath W. Westheide (1997) ArticleTitleUltrastructure of the nuchal organ and cerebral organ in Onchnesoma squamatum (Sipuncula, Phascolionidae) Zoomorphology 117 23–31 Occurrence Handle10.1007/s004350050026

    Article  Google Scholar 

  • A. Qautrefages Particlede (1847) ArticleTitleMémoires sur l’échine de Gaertner Annales des Sciences Naturelles, Zoologie, Série 3 307

    Google Scholar 

  • M.E. Rice (1985) Sipuncula: developmental evidence for phylogenetic inference S.C. Morris J.D. George R. Gibson H.M. Platt (Eds) The Origins and Relationships of Lower Invertebrates Oxford University Press Oxford 274–296

    Google Scholar 

  • M.E. Rice (1993) Sipuncula F.W. Harrison M.E. Rice (Eds) Microscopic Anatomy of Invertebrates: Onychophora, Chilopoda, and lesser Protostomata Wiley-Liss New York 237–325

    Google Scholar 

  • M.B. Romero-Wetzel (1987) ArticleTitleSipunculans as inhabitants of very deep narrow burrows in deep-sea sediments Marine Biology 96 87–92 Occurrence Handle10.1007/BF00394841

    Article  Google Scholar 

  • B. Runnegar B. Pojeta N.J. Morris J.D. Taylor M.E. Taylor G. McClung (1975) ArticleTitleBiology of the Hyolitha Lethaia 8 181–192

    Google Scholar 

  • E.E. Ruppert M.E. Rice (1995) ArticleTitleA functional organization of dermal coelomic canals in Sipunculus nudus (Sipuncula) with a discussion of respiratory designs in sipunculans Invertebrate Zoology 114 51–63

    Google Scholar 

  • A.H. Scheltema (1993) ArticleTitleAplacophora as progenetic aculiferans and the coelomate origin of mollusks as the sister taxon of Sipuncula Biological Bulletin 184 57–78

    Google Scholar 

  • A. Sedgwick (1898) A student’s textbook of zoology S. Sonnenschein, London; Macmillan New York 783

    Google Scholar 

  • E. Selenka (1875) ArticleTitleEifurchung und Larvenbildung von Phascolosoma elongatum Zeitschrift für Wissenschaftliche Zoologie 25 442–450

    Google Scholar 

  • E. Selenka (1885) ArticleTitleReport on the Gephyrea collected by H. M. S. Challenger during 1873–76 Report of scientific results of the Voyage of Challenger Zoology 13 1–25

    Google Scholar 

  • E. Selenka (1888) ArticleTitleOn the Gephyrea of the Mergui Archipelago collected for the Trustees of the Indian Museum J. Linn. Soc. London, Zool 21 220–222

    Google Scholar 

  • E. Selenka (1897) ArticleTitleDie Sipunculiden-Gattung Phymosoma Zoologischer Anzeiger 20 460

    Google Scholar 

  • E. Selenka J.G. Man Particlede C. Bülow (1883) ArticleTitleDie Sipunculiden, eine systematische Monographie Semper Reisen im Archipel der Phillippinen II 4 1–131

    Google Scholar 

  • S.W. Smith R. Overbeek C.R. Woese W. Gilbert P.M. Gillevet (1994) ArticleTitleThe Genetic Data Environment: an expandable GUI for multiple sequence analysis Computer Applications in the Biosciences 10 671–675 Occurrence Handle7704666 Occurrence Handle1:CAS:528:DyaK2MXjvVKksLc%3D

    PubMed  CAS  Google Scholar 

  • M.V. Sørensen P. Funch E. Willerslev A.J. Hansen J. Olesen (2000) ArticleTitleOn the phylogeny of Metazoa in the light of Cycliophora and Micrognathozoa Zoologischer Anzeiger 239 297–318

    Google Scholar 

  • A.C. Stephen (1964) ArticleTitleA revision of the classification of the phylum Sipuncula Annals and Magazine of Natural History 7 457–462

    Google Scholar 

  • A.C. Stephen S.J. Edmonds (1972) The phyla Sipuncula and Echiura Trustees British Mus. (Nat. Hist.) London 528

    Google Scholar 

  • D.L. Swofford (2000) PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods) Sinauer Associates Sunderland, MA

    Google Scholar 

  • M.F. Voss-Foucart S. Barzin C. Jeuniaux J.C. Bussers (1977) ArticleTitleÉtude comparée de la composition chimique des régions souples et durcies de la cuticule de quatre espèces de sipunculiens Cahiers de Biologie Marine 18 135–145

    Google Scholar 

  • A. Wetzel F. Werner (1981) ArticleTitleMorphology and ecological significance of Zoophycos in deep-sea sediments off northwest Africa Palaeogeogr. Palaeoclimatology Palaeoecology 32 185–212

    Google Scholar 

  • W.C. Wheeler (1996) ArticleTitleOptimization alignment: the end of multiple sequence alignment in phylogenetics? Cladistics 12 1–9 Occurrence Handle10.1111/j.1096-0031.1996.tb00189.x

    Article  Google Scholar 

  • Wheeler, W. C., D. Gladstein & J. DeLaet, 2002. POY: the Optimization of Alignment Characters, version 3.0. Program and documentaition available from ftp.amnh.org/pub/molecular

  • M.L. Wilheim F.X. Wilheim (1978) ArticleTitleSubunit structure of erythroid cells chromatin Studia Biophysica 67 105–106

    Google Scholar 

  • B. Winnepenninckx T. Backeljau R. De Wachter (1995) ArticleTitlePhylogeny of protostome worms derived from 18SrRNA sequences Molecular Biology and Evolution 12 641–649 Occurrence Handle7659019 Occurrence Handle1:CAS:528:DyaK2MXmsVOqs7Y%3D

    PubMed  CAS  Google Scholar 

  • J. Zrzavý V. Hypša D.F. Tietz (2001) ArticleTitleMyzostomida are not annelids: molecular and morphological support for a clade of animals with anterior sperm flagella Cladistics 17 170–198

    Google Scholar 

  • J. Zrzavý S. Mihulka P. Kepka A. Bezdek D. Tietz (1998) ArticleTitlePhylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidence Cladistics 14 249–285

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anja Schulze.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schulze, A., Cutler, E.B. & Giribet, G. Reconstructing the phylogeny of the Sipuncula. Hydrobiologia 535, 277–296 (2005). https://doi.org/10.1007/s10750-004-4404-3

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-004-4404-3

Keywords

Navigation