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Phylogenomic analyses unravel annelid evolution

Abstract

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.

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Figure 1: Reconstruction of the Annelida phylogenetic tree.
Figure 2: Ancestral reconstructions of body and parapodial characters.

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Data deposits

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 http://www.treebase.org.

References

  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, 197–207 (2010)

    Google Scholar 

  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, 628–645 (2008)

    Article  CAS  Google Scholar 

  3. Struck, T. H. et al. Annelida phylogeny and the status of Sipuncula and Echiura. BMC Evol. Biol. 7, 57 (2007)

    Article  Google Scholar 

  4. McHugh, D. Molecular evidence that echiurans and pogonophorans are derived annelids. Proc. Natl Acad. Sci. USA 94, 8006–8009 (1997)

    Article  ADS  CAS  Google Scholar 

  5. Raible, F. et al. Vertebrate-type intron-rich genes in the marine annelid Platynereis dumerilii. Science 310, 1325–1326 (2005)

    Article  ADS  CAS  Google Scholar 

  6. Tessmar-Raible, K. & Arendt, D. Emerging systems: between vertebrates and arthropods, the Lophotrochozoa. Curr. Opin. Genet. Dev. 13, 331–340 (2003)

    Article  CAS  Google Scholar 

  7. Rivera, A. & Weisblat, D. And Lophotrochozoa makes three: Notch/Hes signaling in annelid segmentation. Dev. Genes Evol. 219, 37–43 (2009)

    Article  CAS  Google Scholar 

  8. Shain, D. H. Annelids in Modern Biology (Wiley, 2009)

    Book  Google Scholar 

  9. Erséus, C. Phylogeny of oligochaetous Clitellata. Hydrobiologia 535–536, 357–372 (2005)

    Google Scholar 

  10. McHugh, D. Molecular systematics of polychaetes (Annelida). Hydrobiologia 535–536, 309–318 (2005)

    Google Scholar 

  11. Fauvel, P. Polychètes errantes. Faune de France 5, 1–488 (1923)

    Google Scholar 

  12. Fauvel, P. Polychètes sédentaires. Faune de France 16, 1–494 (1927)

    Google Scholar 

  13. de Quatrefages, A. M. Histoire Naturelle des Annelides, Marine et d'Eau Douce. Annelides et Gephyriens Vol. 1 (Librairie Encyclopédique de Roret, 1866)

    Google Scholar 

  14. Day, J. H. A Monograph on the Polychaeta of Southern Africa. Part 1. Errantia (British Museum (Natural History), 1967)

    Google Scholar 

  15. Rouse, G. W. & Fauchald, K. Cladistics and polychaetes. Zool. Scr. 26, 139–204 (1997)

    Article  Google Scholar 

  16. Eibye-Jacobsen, D. A reevaluation of Wiwaxia and the polychaetes of the Burgess Shale. Lethaia 37, 317–335 (2004)

    Article  Google Scholar 

  17. Rouse, G. W. & Pleijel, F. Polychaetes (Oxford Univ. Press, 2001)

    Google Scholar 

  18. Bleidorn, C. et al. On the phylogenetic position of Myzostomida: can 77 genes get it wrong? BMC Evol. Biol. 9, 150 (2009)

    Article  Google Scholar 

  19. Bleidorn, C. et al. Mitochondrial genome and nuclear sequence data support Myzostomida as part of the annelid radiation. Mol. Biol. Evol. 24, 1690–1701 (2007)

    Article  CAS  Google Scholar 

  20. Eeckhaut, I., Fievez, L. & Müller, M. C. M. Larval development of Myzostoma cirriferum (Myzostomida). J. Morphol. 258, 269–283 (2003)

    Article  Google Scholar 

  21. Westheide, W. The direction of evolution within the Polychaeta. J. Nat. Hist. 31, 1–15 (1997)

    Article  Google Scholar 

  22. Suschenko, D. & Purschke, G. Ultrastructure of pigmented adult eyes in errant polychaetes (Annelida): implications for annelid evolution. Zoomorphology 128, 75–96 (2009)

    Article  Google Scholar 

  23. Fauchald, K. & Jumars, P. A. The diet of worms: a study of polychaete feedings guilds. Oceanogr. Mar. Biol. Annu. Rev. 17, 193–284 (1979)

    Google Scholar 

  24. Christodoulou, F. et al. Ancient animal microRNAs and the evolution of tissue identity. Nature 463, 1084–1088 (2010)

    Article  ADS  CAS  Google Scholar 

  25. Hausdorf, B. et al. Spiralian phylogenomics supports the resurrection of Bryozoa comprising Ectoprocta and Entoprocta. Mol. Biol. Evol. 24, 2723–2729 (2007)

    Article  CAS  Google Scholar 

  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)

    Article  Google Scholar 

  27. Birney, E., Clamp, M. & Durbin, R. GeneWise and Genomewise. Genome Res. 14, 988–995 (2004)

    Article  CAS  Google Scholar 

  28. Katoh, K., Kuma, K.-i., Toh, H. & Miyata, T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511–518 (2005)

    Article  CAS  Google Scholar 

  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)

    Article  Google Scholar 

  30. Smith, S. A. & Dunn, C. W. Phyutility: a phyloinformatics tool for trees, alignments and molecular data. Bioinformatics 24, 715–716 (2008)

    Article  CAS  Google Scholar 

  31. NCBI dbEST (Expressed Sequence Tags Database)http://www.ncbi.nlm.nih.gov/projects/dbEST/〉 (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, 1927–1933 (2008)

    Article  Google Scholar 

  33. Struck, T. H. & Fisse, F. Phylogenetic position of Nemertea derived from phylogenomic data. Mol. Biol. Evol. 25, 728–736 (2008)

    Article  CAS  Google Scholar 

  34. Ribosomal Protein Gene Databasehttp://ribosome.med.miyazaki-u.ac.jp〉 (2010)

  35. InParanoid: Eukaryotic Ortholog Groups (100 organisms: 1687023 sequences)http://inparanoid.sbc.su.se/cgi-bin/index.cgi〉 (2010)

  36. Abascal, F., Zardoya, R. & Posada, D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105 (2005)

    Article  CAS  Google Scholar 

  37. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006)

    Article  CAS  Google Scholar 

  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.) 184–200 (Springer, 2009)

    Google Scholar 

  39. Lartillot, N. & Philippe, H. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol. Biol. Evol. 21, 1095–1109 (2004)

    Article  CAS  Google Scholar 

  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)

    Article  Google Scholar 

  41. Rambaut, A. & Drummond, A. J. Tracer v1. 4http://beast.bio.ed.ac.uk/Tracer〉 (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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  44. Rouse, G. W. Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. Biol. J. Linn. Soc. 66, 411–464 (1999)

    Article  Google Scholar 

  45. Hartmann-Schröder, G. Teil 58. Annelida, Borstenwürmer, Polychaeta 2nd edn (Gustav Fischer, 1996)

    Google Scholar 

  46. Westheide, W. & Rieger, R. M. Spezielle Zoologie. Erster Teil: Einzeller und Wirbellose Tiere (Gustav Fischer, 1996)

    Google Scholar 

  47. Purschke, G., Arendt, D., Hausen, H. & Müller, M. C. M. Photoreceptor cells and eyes in Annelida. Arthropod Struct. Dev. 35, 211–230 (2006).

    Article  Google Scholar 

  48. Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis. Version 2.71. Mesquite Projecthttp://mesquiteproject.org〉 (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, 165–173 (2000)

    Article  Google Scholar 

  50. Wiens, J. J. Does adding characters with missing data increase or decrease phylogenetic accuracy? Syst. Biol. 47, 625–640 (1998)

    Article  CAS  Google Scholar 

  51. Wiens, J. J., Bonett, R. M. & Chippindale, P. T. Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships. Syst. Biol. 54, 91–110 (2005)

    Article  Google Scholar 

  52. Bleidorn, C. The role of character loss in phylogenetic reconstruction as exemplified for the Annelida. J. Zool. Syst. Evol. Res. 45, 299–307 (2007)

    Article  Google Scholar 

  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, 57–69 (2009)

    Article  CAS  Google Scholar 

  54. Struck, T. H. Progenetic species in polychaetes (Annelida) and problems assessing their phylogenetic affiliation. Integr. Comp. Biol. 46, 558–568 (2006)

    Article  Google Scholar 

  55. Struck, T. H. Data congruence, paedomorphosis and salamanders. Front. Zool. 4, 22 (2007)

    Article  Google Scholar 

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Acknowledgements

We are grateful to I. Ebersberger, S. Strauss and A. von Haeseler for the processing of our raw EST libraries. We also thank M. Aguado for species identification of Typosyllis pigmentata, as well as K. M. Halanych and P. A. Ramey-Balci for suggestions. T.H.S. and C.B. acknowledge support from the marine biological stations in Bamfield, Helgoland, List and Roscoff for collection of annelids. This work was funded by the priority programme ‘Deep Metazoan Phylogeny’ of the Deutsche Forschungsgemeinschaft by grants DFG-STR 683/5-2 (T.H.S.), DFG-Pu-84/5-1 (G.P. and T.H.S.), DFG-TI-349/4-1 (R.T.), DFG Li 998/3-1 (B.L.), DFG-HA 5744/1-1 (S.H.) and DFG-BL-787/2-1 (C.B.).

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Authors

Contributions

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.

Corresponding authors

Correspondence to Torsten H. Struck or Christoph Bleidorn.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Results, additional references, Supplementary Figures 1-8 with legends and Supplementary Tables 1-6. (PDF 1926 kb)

Supplementary Data Set

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. (RTF 33 kb)

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Struck, T., Paul, C., Hill, N. et al. Phylogenomic analyses unravel annelid evolution. Nature 471, 95–98 (2011). https://doi.org/10.1038/nature09864

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