, 535:277 | Cite as

Reconstructing the phylogeny of the Sipuncula

  • Anja SchulzeEmail author
  • Edward B. Cutler
  • Gonzalo Giribet


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.


Sipuncula phylogeny 18S rRNA 28S rRNA histone H3 Spiralia cladistic analysis 


  1. Åkesson, B. 1958A study of the nervous system of the Sipunculoideae, with some remarks on the development of the two species Phascolion strombi Montagu and Golfingia minuta KefersteinUndersokningar over Oresund381249Google Scholar
  2. Backeljau, T., Winnepenninckx, B., De Bruyn, L. 1993Cladistic analysis of metazoan relationships: a reappraisalCladistics9167181CrossRefGoogle Scholar
  3. Banta, W.C., Rice, M.E. 1976A restudy of the Middle Cambrian Burgess Shale fossil worm, Ottoia prolificaRice, M.E.Todorovic, M. eds. Proceedings of the International Symposioum on the Biology of the Sipuncula and EchiuraNauçno Delo PressBelgrade7990Google Scholar
  4. Boore, J.L., Staton, J.L. 2002The mitochondrial genome of the sipunculid Phascolopsis gouldii supports its association with Annelida rather than MolluscaMolecular Biology and Evolution19127137PubMedGoogle Scholar
  5. Brett, C.E., Cottrell, J.F. 1982Substrate specificity in the Devonian tabulate coral Pleurodictyum Lethaia15247262Google Scholar
  6. Brett, C.E., Liddell, W.D., Derstler, K.L. 1983Late Cambrian hard substrate communities from Montana/Wyoming: the oldest known hardground encrustersLethaia16281289Google Scholar
  7. Brusca, R.C., Brusca, G.J. 1990InvertebratesSinauer AssociatesSunderlandGoogle Scholar
  8. Brusca, R.C., Brusca, G.J. 2003Invertebrates. Second editionSinauer AssociatesSunderlandGoogle Scholar
  9. Conway Morris, S. 1989Burgess Shale faunas and the Cambrian explosionScience246339346PubMedGoogle Scholar
  10. Conway Morris, S. 1998The Crucible of CreationThe Burgess Shale and the Rise of Animals.Oxford University PressOxford242Google Scholar
  11. Cutler, E.B. 1994The Sipuncula. Their Systematics, Biology and EvolutionCornell University PressIthaca, NY453Google Scholar
  12. Cutler, E.B., Gibbs, P.E. 1985A phylogenetic analysis of higher taxa in the phylum SipunculaSystematic Zoology34162173Google Scholar
  13. Cuvier, B. 1830Le 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. 3DetervilleParis1244Google Scholar
  14. Dybas, L. 1981Sipunculans and echiuroidsRatcliff, N.A.Rowley, A.F. eds. Invertebrate Blood CellsAcademic PressNew York161188Google Scholar
  15. Edmonds, S.J. 2000Phylum SipunculaBeesley, P.L.Ross, G.J.B.Glasby, C.J. eds. Fauna of Australia 4, Polychaetes & Allies: The Southern SynthesisCSIRO PublishingMelbourne375400Google Scholar
  16. Eernisse, D.J., Albert, J.S., Anderson, F.E. 1992Annelida and Arthropoda are not sister taxa: a phylogenetic analysis of spiralian metazoan morphologySystematic Biology41305330Google Scholar
  17. Erber, A., Riemer, D., Bovenschulte, M., Weber, K. 1998Molecular phylogeny of metazoan intermediate filament proteinsJournal of Molecular Evolution47751762PubMedGoogle Scholar
  18. Eriksson, T., 1998. AutoDecay. Stockholm, Distributed by the Author. Department of Botany, Stockholm UniversityGoogle Scholar
  19. Ferrier, D.E., Holland, P.W. 2001Sipunculan ParaHox genesEvolution & Development3263270Google Scholar
  20. Florkin, M. 1975Biochemical evidence for the phylogenetic relationships of the SipunculaRice, M.E.Todorovic, M. eds. Proceedings of the International Symposium on the biology of the Sipuncula and EchiuraNaucno Delo PressBelgrade95110Google Scholar
  21. Frey, R.W., Pemberton, G., Fagerstrom, J.A. 1984Morphological, ethological and environmental significance of the ichnogenera Scoyenia and Ancorichnus Journal of Paleontology58511528Google Scholar
  22. Gibbs, P.E., Cutler, E.B. 1987A classification of the phylum SipunculaBulletin of the British Museum of Natural History (Zoology)524358Google Scholar
  23. Gill, G.A., Coates, A.G. 1977Mobility, growth patterns and substrate in some fossil and Recent coralsLethaia10119134Google Scholar
  24. Giribet, G. 2002Current advances in the phylogenetic reconstruction of metazoan evolution. A new paradigm for the Cambrian explosion?Molecular Phylogenetics and Evolution24345357CrossRefPubMedGoogle Scholar
  25. Giribet, G., Distel, D.L., Polz, M., Sterrer, W., Wheeler, W.C. 2000Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Platyhelminthes, and Chaetognatha: a combined approach of 18S rDNA sequences and morphologySystematic Biology49539562PubMedGoogle Scholar
  26. Green, C.R., Berquist, P.R. 1982Phylogenetic relationships within the Invertebrata in relation to the structure of septate junctions and the development of occluding junctional typesJournal of Cell Science53279306Google Scholar
  27. Guralnick, R. 2002A recapitulation of the rise and fall of the cell lineage research program: the evolutionary developmental relationship of cleavage to homology, body plans and life historyJournal of History of Biology35527567Google Scholar
  28. Guralnick, R.P., Lindberg, D.R. 2001Reconnecting cell and animal lineages: what do cell lineages tell us about the evolution and development of Spiralia?Evolution5515011519PubMedGoogle Scholar
  29. Henry, R.P. 1987Invertebrate red blood cell carbonic anhydraseJournal of Experimental Zoology242113116CrossRefPubMedGoogle Scholar
  30. Holland, P.W.H. 1998Major transitions in animal evolution: A developmental genetic perspectiveAmerican Zoology38878887Google Scholar
  31. Huang, D., Chen, J., Vannier, J., Saiz Salinas, J.I. 2004Early Cambrian sipunculan worms from southwest ChinaProceedings of the Royal Society of London, Series B27116711676CrossRefGoogle Scholar
  32. Hyman, L.H. 1959The Invertebrates 5, Smaller Coelomate GroupsMcGraw-HillNew York783Google Scholar
  33. Ionescu-Varo, M., Tufescu, M. 1982Quantitative remarks on immune evolution in the animal seriesRev. Roumaine Biol. série Biol. Animale272939Google Scholar
  34. Keferstein, W. 1863Beiträge sur Kenntnis der Gattung Phascolosoma F.S. Leuck. Untersuchungen über niedere SeethiereZeitschrift für Wissenschaftliche Zoologie123551Google Scholar
  35. Keferstein, W. 1865aBeiträge zur anatomischen und systematischen Kenntnis der SipunculidenNachrichten der Gesellschaft der Wissenschaften, Göttingen1865189209Google Scholar
  36. Keferstein, W. 1865bBeiträge zur anatomischen und systematischen Kenntniss der SipunculidenZeitschrift für Wissenschaftliche Zoologie15404445Google Scholar
  37. Keferstein, W. 1866Untersuchungen uber einige amerikanische SipunculidenNachrichten von der Königlichen Gesellschaft der Wissenschaften und der Georg-August-Universität zu Göttingen14215228Google Scholar
  38. Keferstein, W. 1867Untersuchungen über einige amerikanische SipunculidenZeitschrift Fur Wissenschaftliche Zoologie174455Google Scholar
  39. Klepal, W. 1987The anchoring fiber apparatus in the sperm of Aspidosiphon sp. (Sipunculida)European Journal of Cell Biology Suppl018Google Scholar
  40. Kotetskii, E.Y. 1984The phospholipid composition of Spongia, Coelenterata and free living Platyhelminthes, Nemertini, Annelida, Sipunculida and EchiuridaBiologiya Morya04653Google Scholar
  41. Lake, J.A. 1990Origin of the MetazoaProceedings of the National Academy of Sciences of the United State of America87763766CrossRefGoogle Scholar
  42. Lamarck, J. P. B. A., de M., 1816. Histoire naturelle des animaux sans vertébrés. Vol. 3. Verdière: Paris, 683 ppGoogle Scholar
  43. Lehman, W., Szent-Györgyi, A.G. 1975Regulation of muscular contraction: distribution of actin control and myosin control in the animal kingdomJournal of General Physiology66130CrossRefPubMedGoogle Scholar
  44. Livingstone, D.R., Dezwaan, A., Leopold, M., Marteijn, E. 1983Studies on the phylogenetic distribution of pyruvate oxidoreductasesBiochem. Syst. Ecol1415425Google Scholar
  45. Maddison, D.R., Maddison, W.P. 2001MacCladeSinauer AssociatesSunderland, MAGoogle Scholar
  46. Mangum, C.P. 1990The role of physiology and biochemistry in understanding animal phylogenyProceedings of the Biological Society of Washington103235247Google Scholar
  47. Marti Mus, M., Bergstrom, J. 2001The skeleton-muscular system of hyolithidsAmerican Zoologist411514Google Scholar
  48. Maxmen, A.B., King, B.F., Cutler, E.B., Giribet, G. 2003Evolutionary relationships within the protostome phylum Sipuncula: a molecular analysis of ribosomal genes and histone H3 sequence dataMolecular Phylogenetics and Evolution27489503CrossRefPubMedGoogle Scholar
  49. McBride, E.F., Picard, M.D. 1991Facies implications of Trichichnus and Chondrites in turbidites and hemipelagites, Marnoso-arenacea formation (Miocene), northern Apennine, ItalyPalaios6281290Google Scholar
  50. Meglitsch, P.A., Schram, F.R. 1991Invertebrate ZoologyOxford University PressOxfordGoogle Scholar
  51. Nichols, D. 1967The origin of echinodermsSymposia of the Zoological Society of London20209229Google Scholar
  52. Nielsen, C., 1987. Structure and function of metazoan ciliary bands and their phylogenetic significance. Acta Zoologica 68Google Scholar
  53. Nielsen, C., Scharff, N., Eibye-Jacobsen, D. 1996Cladistic analyses of the animal kingdomBiological Journal of the Linnean Society57385410CrossRefGoogle Scholar
  54. Ocharan, F.J. 1974Sobre los nefridios de Phascolosoma granulatum (Sipuncula)Separata de la revista de la “Facultad de Ciencias”152140Google Scholar
  55. Pemberton, S.G., Kobluk, D.R., Yeo, R.K., Risk, M.J. 1980Boring Trypanites at the Silurian-Devonian disconformity in southern Ontario, CanadaJournal of Paleontology5412581266Google Scholar
  56. Peterson, K., Eernisse, D.J. 2001Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequencesEvolution & Development3170205CrossRefGoogle Scholar
  57. Pickford, G.E. 1947Sipunculida. In Encyclopedia Britannica, Vol. 20niversity of ChicagoChicago717718bGoogle Scholar
  58. Pilger, J.F., Rice, M.E. 1987Ultrastructural evidence for the contractile vessel of sipunculans as a possible ultrafiltration siteAmerican Zoology27810aGoogle Scholar
  59. Pisera, A. 1987Boring and nestling organisms from Upper Jurassic coral colonies from Northern PolandActa Palaeontologia Polonica3283104Google Scholar
  60. Purschke, G., Wolfrath, F., Westheide, W. 1997Ultrastructure of the nuchal organ and cerebral organ in Onchnesoma squamatum (Sipuncula, Phascolionidae)Zoomorphology1172331CrossRefGoogle Scholar
  61. Qautrefages, A. 1847Mémoires sur l’échine de GaertnerAnnales des Sciences Naturelles, Zoologie, Série3307Google Scholar
  62. Rice, M.E. 1985Sipuncula: developmental evidence for phylogenetic inferenceMorris, S.C.George, J.D.Gibson, R.Platt, H.M. eds. The Origins and Relationships of Lower InvertebratesOxford University PressOxford274296Google Scholar
  63. Rice, M.E. 1993SipunculaHarrison, F.W.Rice, M.E. eds. Microscopic Anatomy of Invertebrates: Onychophora, Chilopoda, and lesser ProtostomataWiley-LissNew York237325Google Scholar
  64. Romero-Wetzel, M.B. 1987Sipunculans as inhabitants of very deep narrow burrows in deep-sea sedimentsMarine Biology968792CrossRefGoogle Scholar
  65. Runnegar, B., Pojeta, B., Morris, N.J., Taylor, J.D., Taylor, M.E., McClung, G. 1975Biology of the Hyolitha Lethaia8181192Google Scholar
  66. Ruppert, E.E., Rice, M.E. 1995A functional organization of dermal coelomic canals in Sipunculus nudus (Sipuncula) with a discussion of respiratory designs in sipunculansInvertebrate Zoology1145163Google Scholar
  67. Scheltema, A.H. 1993Aplacophora as progenetic aculiferans and the coelomate origin of mollusks as the sister taxon of SipunculaBiological Bulletin1845778Google Scholar
  68. Sedgwick, A. 1898A student’s textbook of zoologyS. Sonnenschein, London; MacmillanNew York783Google Scholar
  69. Selenka, E. 1875Eifurchung und Larvenbildung von Phascolosoma elongatum Zeitschrift für Wissenschaftliche Zoologie25442450Google Scholar
  70. Selenka, E. 1885Report on the Gephyrea collected by H. M. S. Challenger during 1873–76Report of scientific results of the Voyage of Challenger Zoology13125Google Scholar
  71. Selenka, E. 1888On the Gephyrea of the Mergui Archipelago collected for the Trustees of the Indian MuseumJ. Linn. Soc. London, Zool21220222Google Scholar
  72. Selenka, E. 1897Die Sipunculiden-Gattung Phymosoma Zoologischer Anzeiger20460Google Scholar
  73. Selenka, E., Man, J.G., Bülow, C. 1883Die Sipunculiden, eine systematische MonographieSemper Reisen im Archipel der Phillippinen II41131Google Scholar
  74. Smith, S.W., Overbeek, R., Woese, C.R., Gilbert, W., Gillevet, P.M. 1994The Genetic Data Environment: an expandable GUI for multiple sequence analysisComputer Applications in the Biosciences10671675PubMedGoogle Scholar
  75. Sørensen, M.V., Funch, P., Willerslev, E., Hansen, A.J., Olesen, J. 2000On the phylogeny of Metazoa in the light of Cycliophora and MicrognathozoaZoologischer Anzeiger239297318Google Scholar
  76. Stephen, A.C. 1964A revision of the classification of the phylum SipunculaAnnals and Magazine of Natural History7457462Google Scholar
  77. Stephen, A.C., Edmonds, S.J. 1972The phyla Sipuncula and EchiuraTrustees British Mus. (Nat. Hist.)London528Google Scholar
  78. Swofford, D.L. 2000PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods)Sinauer AssociatesSunderland, MAGoogle Scholar
  79. Voss-Foucart, M.F., Barzin, S., Jeuniaux, C., Bussers, J.C. 1977Étude comparée de la composition chimique des régions souples et durcies de la cuticule de quatre espèces de sipunculiensCahiers de Biologie Marine18135145Google Scholar
  80. Wetzel, A., Werner, F. 1981Morphology and ecological significance of Zoophycos in deep-sea sediments off northwest AfricaPalaeogeogr. Palaeoclimatology Palaeoecology32185212Google Scholar
  81. Wheeler, W.C. 1996Optimization alignment: the end of multiple sequence alignment in phylogenetics?Cladistics1219CrossRefGoogle Scholar
  82. Wheeler, W. C., D. Gladstein & J. DeLaet, 2002. POY: the Optimization of Alignment Characters, version 3.0. Program and documentaition available from Scholar
  83. Wilheim, M.L., Wilheim, F.X. 1978Subunit structure of erythroid cells chromatinStudia Biophysica67105106Google Scholar
  84. Winnepenninckx, B., Backeljau, T., De Wachter, R. 1995Phylogeny of protostome worms derived from 18SrRNA sequencesMolecular Biology and Evolution12641649PubMedGoogle Scholar
  85. Zrzavý, J., Hypša, V., Tietz, D.F. 2001Myzostomida are not annelids: molecular and morphological support for a clade of animals with anterior sperm flagellaCladistics17170198Google Scholar
  86. Zrzavý, J., Mihulka, S., Kepka, P., Bezdek, A., Tietz, D. 1998Phylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidenceCladistics14249285Google Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Anja Schulze
    • 1
    Email author
  • Edward B. Cutler
    • 1
  • Gonzalo Giribet
    • 1
    • 2
  1. 1.Department of Invertebrate Zoology, Museum of Comparative ZoologyHarvard UniversityCambridgeUSA
  2. 2.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA

Personalised recommendations