Phylogenomic analyses unravel annelid evolution

Journal name:
Date published:
Published online

Annelida, the ringed worms, is a highly diverse animal phylum that includes more than 15,000 described species and constitutes the dominant benthic macrofauna from the intertidal zone down to the deep sea. A robust annelid phylogeny would shape our understanding of animal body-plan evolution and shed light on the bilaterian ground pattern. Traditionally, Annelida has been split into two major groups: Clitellata (earthworms and leeches) and polychaetes (bristle worms), but recent evidence suggests that other taxa that were once considered to be separate phyla (Sipuncula, Echiura and Siboglinidae (also known as Pogonophora)) should be included in Annelida1, 2, 3, 4. However, the deep-level evolutionary relationships of Annelida are still poorly understood, and a robust reconstruction of annelid evolutionary history is needed. Here we show that phylogenomic analyses of 34 annelid taxa, using 47,953 amino acid positions, recovered a well-supported phylogeny with strong support for major splits. Our results recover chaetopterids, myzostomids and sipunculids in the basal part of the tree, although the position of Myzostomida remains uncertain owing to its long branch. The remaining taxa are split into two clades: Errantia (which includes the model annelid Platynereis), and Sedentaria (which includes Clitellata). Ancestral character trait reconstructions indicate that these clades show adaptation to either an errant or a sedentary lifestyle, with alteration of accompanying morphological traits such as peristaltic movement, parapodia and sensory perception. Finally, life history characters in Annelida seem to be phylogenetically informative.

At a glance


  1. Reconstruction of the Annelida phylogenetic tree.
    Figure 1: Reconstruction of the Annelida phylogenetic tree.

    Majority rule consensus trees of the Bayesian inference analysis using the site-heterogeneous CAT model of the data set with 39 taxa and 47,953 amino acid positions. Only PP (top of branch or alone) and BS (bottom) values0.70 or 70, respectively, are shown. The branch leading to Myzostomida is reduced by 75%. Annelida are highlighted in red, with Sedentaria in blue and Errantia in green. Grey bars indicate additional annelid groups. *, BS value for the monophyly of Annelida without Myzostomida in the maximum likelihood analysis is 99.

  2. Ancestral reconstructions of body and parapodial characters.
    Figure 2: Ancestral reconstructions of body and parapodial characters.

    a, Annelida and clade 1. b, Errantia. c, Sedentaria. Body characters (left) and parapodial characters (right) are depicted. The state of several parapodial characters in Annelida and clade 1 is uncertain, so we depict the two most extreme possibilities. Dashed lines or question marks indicate that the state of the character is uncertain. bie, bicellular eyes; doc, dorsal cirrus; grp, grooved palps; isc, internalized supporting chaetae; laa, lateral antenna; mue, multicellular eyes; nuo, nuchal organ; pyc, pygidial cirrus; sic, simple chaetae; sop, solid palps; un/h, uncini/hooks; vec, ventral cirrus.


  1. Dordel, J., Fisse, F., Purschke, G. & Struck, T. H. Phylogenetic position of Sipuncula derived from multi-gene and phylogenomic data and its implication for the evolution of segmentation. J. Zool. Syst. Evol. Res. 48, 197207 (2010)
  2. Struck, T. H., Nesnidal, M. P., Purschke, G. & Halanych, K. M. Detecting possibly saturated positions in 18S and 28S sequences and their influence on phylogenetic reconstruction of Annelida (Lophotrochozoa). Mol. Phylogenet. Evol. 48, 628645 (2008)
  3. Struck, T. H. et al. Annelida phylogeny and the status of Sipuncula and Echiura. BMC Evol. Biol. 7, 57 (2007)
  4. McHugh, D. Molecular evidence that echiurans and pogonophorans are derived annelids. Proc. Natl Acad. Sci. USA 94, 80068009 (1997)
  5. Raible, F. et al. Vertebrate-type intron-rich genes in the marine annelid Platynereis dumerilii. Science 310, 13251326 (2005)
  6. Tessmar-Raible, K. & Arendt, D. Emerging systems: between vertebrates and arthropods, the Lophotrochozoa. Curr. Opin. Genet. Dev. 13, 331340 (2003)
  7. Rivera, A. & Weisblat, D. And Lophotrochozoa makes three: Notch/Hes signaling in annelid segmentation. Dev. Genes Evol. 219, 3743 (2009)
  8. Shain, D. H. Annelids in Modern Biology (Wiley, 2009)
  9. Erséus, C. Phylogeny of oligochaetous Clitellata. Hydrobiologia 535–536, 357372 (2005)
  10. McHugh, D. Molecular systematics of polychaetes (Annelida). Hydrobiologia 535–536, 309318 (2005)
  11. Fauvel, P. Polychètes errantes. Faune de France 5, 1488 (1923)
  12. Fauvel, P. Polychètes sédentaires. Faune de France 16, 1494 (1927)
  13. de Quatrefages, A. M. Histoire Naturelle des Annelides, Marine et d'Eau Douce. Annelides et Gephyriens Vol. 1 (Librairie Encyclopédique de Roret, 1866)
  14. Day, J. H. A Monograph on the Polychaeta of Southern Africa. Part 1. Errantia (British Museum (Natural History), 1967)
  15. Rouse, G. W. & Fauchald, K. Cladistics and polychaetes. Zool. Scr. 26, 139204 (1997)
  16. Eibye-Jacobsen, D. A reevaluation of Wiwaxia and the polychaetes of the Burgess Shale. Lethaia 37, 317335 (2004)
  17. Rouse, G. W. & Pleijel, F. Polychaetes (Oxford Univ. Press, 2001)
  18. Bleidorn, C. et al. On the phylogenetic position of Myzostomida: can 77 genes get it wrong? BMC Evol. Biol. 9, 150 (2009)
  19. Bleidorn, C. et al. Mitochondrial genome and nuclear sequence data support Myzostomida as part of the annelid radiation. Mol. Biol. Evol. 24, 16901701 (2007)
  20. Eeckhaut, I., Fievez, L. & Müller, M. C. M. Larval development of Myzostoma cirriferum (Myzostomida). J. Morphol. 258, 269283 (2003)
  21. Westheide, W. The direction of evolution within the Polychaeta. J. Nat. Hist. 31, 115 (1997)
  22. Suschenko, D. & Purschke, G. Ultrastructure of pigmented adult eyes in errant polychaetes (Annelida): implications for annelid evolution. Zoomorphology 128, 7596 (2009)
  23. Fauchald, K. & Jumars, P. A. The diet of worms: a study of polychaete feedings guilds. Oceanogr. Mar. Biol. Annu. Rev. 17, 193284 (1979)
  24. Christodoulou, F. et al. Ancient animal microRNAs and the evolution of tissue identity. Nature 463, 10841088 (2010)
  25. Hausdorf, B. et al. Spiralian phylogenomics supports the resurrection of Bryozoa comprising Ectoprocta and Entoprocta. Mol. Biol. Evol. 24, 27232729 (2007)
  26. Ebersberger, I., Strauss, S. & von Haeseler, A. HaMStR: profile Hidden Markov Model based search for orthologs in ESTs. BMC Evol. Biol. 9, 157 (2009)
  27. Birney, E., Clamp, M. & Durbin, R. GeneWise and Genomewise. Genome Res. 14, 988995 (2004)
  28. Katoh, K., Kuma, K.-i., Toh, H. & Miyata, T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511518 (2005)
  29. Hartmann, S. & Vision, T. Using ESTs for phylogenomics: can one accurately infer a phylogenetic tree from a gappy alignment? BMC Evol. Biol. 8, 95 (2008)
  30. Smith, S. A. & Dunn, C. W. Phyutility: a phyloinformatics tool for trees, alignments and molecular data. Bioinformatics 24, 715716 (2008)
  31. NCBI dbEST (Expressed Sequence Tags Database) left fence fence (2010)
  32. Helmkampf, M., Bruchhaus, I. & Hausdorf, B. Phylogenomic analyses of lophophorates (brachiopods, phoronids and bryozoans) confirm the Lophotrochozoa concept. Proc. R. Soc. Lond. B 275, 19271933 (2008)
  33. Struck, T. H. & Fisse, F. Phylogenetic position of Nemertea derived from phylogenomic data. Mol. Biol. Evol. 25, 728736 (2008)
  34. Ribosomal Protein Gene Database left fence fence (2010)
  35. InParanoid: Eukaryotic Ortholog Groups (100 organisms: 1687023 sequences) left fence fence (2010)
  36. Abascal, F., Zardoya, R. & Posada, D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 21042105 (2005)
  37. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 26882690 (2006)
  38. Pattengale, N. D., Alipour, M., Bininda-Emonds, O. R. P., Moret, B. M. E. & Stamatakis, A. in RECOMB 2009, LNCS 5541 (ed. Batzoglou, S.) 184200 (Springer, 2009)
  39. Lartillot, N. & Philippe, H. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol. Biol. Evol. 21, 10951109 (2004)
  40. Lartillot, N., Brinkmann, H. & Philippe, H. Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model. BMC Evol. Biol. 7, S4 (2007)
  41. Rambaut, A. & Drummond, A. J. Tracer v1. 4 left fence fence (2007)
  42. Zhou, Y., Rodrigue, N., Lartillot, N. & Philippe, H. Evaluation of the models handling heterotachy in phylogenetic inference. BMC Evol. Biol. 7, 206 (2007)
  43. Zrzavý, J., Riha, P., Pialek, L. & Janouskovec, J. Phylogeny of Annelida (Lophotrochozoa): total-evidence analysis of morphology and six genes. BMC Evol. Biol. 9, 189 (2009)
  44. Rouse, G. W. Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. Biol. J. Linn. Soc. 66, 411464 (1999)
  45. Hartmann-Schröder, G. Teil 58. Annelida, Borstenwürmer, Polychaeta 2nd edn (Gustav Fischer, 1996)
  46. Westheide, W. & Rieger, R. M. Spezielle Zoologie. Erster Teil: Einzeller und Wirbellose Tiere (Gustav Fischer, 1996)
  47. Purschke, G., Arendt, D., Hausen, H. & Müller, M. C. M. Photoreceptor cells and eyes in Annelida. Arthropod Struct. Dev. 35,211230 (2006).
  48. Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis. Version 2.71. Mesquite Project left fencehttp://mesquiteproject.orgright fence (2009)
  49. Purschke, G., Hessling, R. & Westheide, W. The phylogenetic position of the Clitellata and the Echiura — on the problematic assessment of absent characters. J. Zool. Syst. Evol. Res. 38, 165173 (2000)
  50. Wiens, J. J. Does adding characters with missing data increase or decrease phylogenetic accuracy? Syst. Biol. 47, 625640 (1998)
  51. Wiens, J. J., Bonett, R. M. & Chippindale, P. T. Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships. Syst. Biol. 54, 91110 (2005)
  52. Bleidorn, C. The role of character loss in phylogenetic reconstruction as exemplified for the Annelida. J. Zool. Syst. Evol. Res. 45, 299307 (2007)
  53. Bleidorn, C., Hill, N., Erséus, C. & Tiedemann, R. On the role of character loss in orbiniid phylogeny (Annelida): molecules vs. morphology. Mol. Phylogenet. Evol. 52, 5769 (2009)
  54. Struck, T. H. Progenetic species in polychaetes (Annelida) and problems assessing their phylogenetic affiliation. Integr. Comp. Biol. 46, 558568 (2006)
  55. Struck, T. H. Data congruence, paedomorphosis and salamanders. Front. Zool. 4, 22 (2007)

Download references

Author information


  1. University of Osnabrück, FB05 Biology/Chemistry, AG Zoology, Barbarastrasse 11, 49069 Osnabrück, Germany

    • Torsten H. Struck,
    • Christoph Hösel &
    • Günter Purschke
  2. University of Potsdam, Institute of Biochemistry and Biology, Unit of Evolutionary Biology/Systematic Zoology, Karl-Liebknecht-Strasse 24-25, Haus 26, 14476 Potsdam, Germany

    • Christiane Paul,
    • Ralph Tiedemann &
    • Christoph Bleidorn
  3. University of Potsdam, Institute of Biochemistry and Biology, Unit of Bioinformatics, Karl-Liebknecht-Strasse 24-25, Haus 14, 14476 Potsdam, Germany

    • Natascha Hill &
    • Stefanie Hartmann
  4. Max Planck Institute for Molecular Genetics, Ihnestrasse 63–73, 14195 Berlin, Germany

    • Michael Kube
  5. Johannes Gutenberg University, Institute of Zoology, Müllerweg 6, 55099 Mainz, Germany

    • Bernhard Lieb &
    • Achim Meyer
  6. University of Leipzig, Institute for Biology II, Molecular Evolution and Systematics of Animals, Talstrasse 33, 04103 Leipzig, Germany

    • Christoph Bleidorn


T.H.S., G.P., R.T. and C.B. conceived this study. T.H.S. took the lead on data collection of sedentary polychaetes, and writing. T.H.S. and S.H. performed phylogenomic analyses. C.H. aided in the data collection of Sedentaria. C.B. and C.P. took the lead on data collection of errant polychaetes, and C.B., S.H. and N.H. on compilation of the data sets from the EST libraries. A.M. and B.L. generated the EST library of Sipunculus nudus, and M.K. was responsible for the sequencing of the EST libraries. T.H.S., G.P., R.T. and C.B. were the main contributors to the writing of the manuscript.

Competing financial interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to:

Sequence data have been deposited in the NCBI Expressed Sequence Tag database (dbEST) under accession numbers FN424437–FN428571, FR754554–FR771822, HQ729923–HQ729975. The largest aligned data set has been deposited at

Author details

Supplementary information

PDF files

  1. Supplementary Information (1.8M)

    The file contains Supplementary Results, additional references, Supplementary Figures 1-8 with legends and Supplementary Tables 1-6.

Rich text format

  1. Supplementary Data Set (33K)

    This file contains the morphological data matrix used in the ancestral reconstructions. Modifications in the character matrix in comparison to Zrzavy et al (2009) are in bold. Converting it to a plain text file allows opening it with Mesquite to show the results of our ancestral reconstructions.


  1. Report this comment #59257

    Peter Gibson said:

    This comment is a bit late now but I feel might be worth making. The invertebrate macro species are generally thought to be a success of benthic species that have diversified to exploit the environment. What is a little odd is that there is such a variety of groups. This would suggest that they have found still greater numbers of niches into which to evolve. It suggests an ever growing number of exploitable niches. This is possible if one considers that the environment varies over distance so that no two places are the same. However animals evolve to accommodate to this variability. More likely is that many species are exploiting exactly the same niches. If that is the case then one might have difficulty in arguing that these species can sustain the completion. This is assuming that species form an evolutionary linear success. Species are in effect treading one another?s territory. There is constant unsustainable turf warfare. A way of getting around this is to suppose that the benthic species were not always benthic but dropped out of the plankton. This is not new. So evolution and radiation took place in the plankton at a time the benthos was uninhabitable due low oxygen levels. With increased levels plankton descended to take advantage of the under exploited high organic levels. The species increased in size, fecundity and the ability to prey on smaller competitors. The point, although perhaps obscure, is that species had completed their radiation. All they had to do now was to eat their competitors into extinction. The emphasis was then a matter of varying feeding structures. This was an argument put forward for the evolution of polychaetes by Dales a while ago. With the advent of molecular biology people became a bit sniffy about his structural argument. I feel, however, there is something to be said in his favour.

Subscribe to comments

Additional data