Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Acoelomorph flatworms are deuterostomes related to Xenoturbella

Nature volume 470, pages 255–258 (2011)Cite this article

Subjects

Abstract

Xenoturbellida and Acoelomorpha are marine worms with contentious ancestry. Both were originally associated with the flatworms (Platyhelminthes), but molecular data have revised their phylogenetic positions, generally linking Xenoturbellida to the deuterostomes1,2 and positioning the Acoelomorpha as the most basally branching bilaterian group(s)3,4,5,6. Recent phylogenomic data suggested that Xenoturbellida and Acoelomorpha are sister taxa and together constitute an early branch of Bilateria7. Here we assemble three independent data sets—mitochondrial genes, a phylogenomic data set of 38,330 amino-acid positions and new microRNA (miRNA) complements—and show that the position of Acoelomorpha is strongly affected by a long-branch attraction (LBA) artefact. When we minimize LBA we find consistent support for a position of both acoelomorphs and Xenoturbella within the deuterostomes. The most likely phylogeny links Xenoturbella and Acoelomorpha in a clade we call Xenacoelomorpha. The Xenacoelomorpha is the sister group of the Ambulacraria (hemichordates and echinoderms). We show that analyses of miRNA complements8 have been affected by character loss in the acoels and that both groups possess one miRNA and the gene Rsb66 otherwise specific to deuterostomes. In addition, Xenoturbella shares one miRNA with the ambulacrarians, and two with the acoels. This phylogeny makes sense of the shared characteristics of Xenoturbellida and Acoelomorpha, such as ciliary ultrastructure and diffuse nervous system, and implies the loss of various deuterostome characters in the Xenacoelomorpha including coelomic cavities, through gut and gill slits.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Alternative phylogenetic positions of Acoela, Nemertodermatida and Xenoturbellida with implied evolution of different characters.
Figure 2: Animal phylogeny based on mitochondrial proteins reconstructed using the CAT + GTR +  Γ model under a Bayesian analysis.
Figure 3: Phylogeny of 66 animal species based on EST sequences.

Similar content being viewed by others

References

  1. Bourlat, S. et al. Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444, 85–88 (2006)

    Article  ADS  CAS  Google Scholar 

  2. Bourlat, S., Nielsen, C., Lockyer, A., Littlewood, D. T. J. & Telford, M. J. Xenoturbella is a deuterostome that eats molluscs. Nature 424, 925–928 (2003)

    Article  ADS  CAS  Google Scholar 

  3. Egger, B. et al. To be or not to be a flatworm: the acoel controversy. PLoS ONE 4, e5502 (2009)

    Article  ADS  Google Scholar 

  4. Telford, M. J., Lockyer, A. E., Cartwright-Finch, C. & Littlewood, D. T. J. Combined large and small subunit ribosomal RNA phylogenies support a basal position of the acoelomorph flatworms. Proc. R. Soc. Lond. B 270, 1077–1083 (2003)

    Article  CAS  Google Scholar 

  5. Sempere, L. F., Cole, C. N., McPeek, M. A. & Peterson, K. J. The phylogenetic distribution of metazoan microRNAs: insights into evolutionary complexity and constraint. J. Exp. Zool. B 306, 575–588 (2006)

    Article  Google Scholar 

  6. Ruiz Trillo, I., Riutort, M., Littlewood, D. T. J., Herniou, E. A. & Baguñà, J. Acoel flatworms: earliest extant bilaterian metazoans, not members of Platyhelminthes. Science 283, 1919–1923 (1999)

    Article  ADS  CAS  Google Scholar 

  7. Hejnol, A. et al. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc. R. Soc. B 276, 4261–4270 (2009)

    Article  Google Scholar 

  8. Sempere, L. F., Martinez, P., Cole, C., Baguñà, J. & Peterson, K. J. Phylogenetic distribution of microRNAs supports the basal position of acoel flatworms and the polyphyly of Platyhelminthes. Evol. Dev. 9, 409–415 (2007)

    Article  CAS  Google Scholar 

  9. Ruiz-Trillo, I. et al. A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertodermatida are basal bilaterians. Proc. Natl Acad. Sci. USA 99, 11246–11251 (2002)

    Article  ADS  CAS  Google Scholar 

  10. Bourlat, S. J., Rota-Stabelli, O., Lanfear, R. & Telford, M. J. The mitochondrial genome structure of Xenoturbella bocki (phylum Xenoturbellida) is ancestral within the deuterostomes. BMC Evol. Biol. 9, 107 (2009)

    Article  Google Scholar 

  11. Philippe, H., Brinkmann, H., Martinez, P., Riutort, M. & Baguñà, J. Acoel flatworms are not platyhelminthes: evidence from phylogenomics. PLoS ONE 2, e717 (2007)

    Article  ADS  Google Scholar 

  12. Rodríguez-Ezpeleta, N. et al. Detecting and overcoming systematic errors in genome-scale phylogenies. Syst. Biol. 56, 389–399 (2007)

    Article  Google Scholar 

  13. Lartillot, N. & Philippe, H. Improvement of molecular phylogenetic inference and the phylogeny of Bilateria. Phil. Trans. R. Soc. B 363, 1463–1472 (2008)

    Article  Google Scholar 

  14. Ruiz Trillo, I., Riutort, M., Fourcade, H. M., Baguña, J. & Boore, J. Mitochondrial genome data support the basal position of Acoelomorpha and the polyphyly of the Platyhelminthes. Mol. Phyl. Evol. 33, 321–332 (2004)

    Article  CAS  Google Scholar 

  15. Papillon, D., Perez, Y., Caubit, X. & Le Parco, Y. Identification of chaetognaths as protostomes is supported by the analysis of their mitochondrial genome. Mol. Biol. Evol. 21, 2122–2129 (2004)

    Article  CAS  Google Scholar 

  16. Sperling, E. A. & Peterson, K. J. in Animal Evolution. Genomes, Fossils and Trees (eds Telford, M. J. & Littlewood, D. T. J. ) Ch. 15, 157–170 (Oxford Univ. Press, 2009)

    Book  Google Scholar 

  17. Lundin, K. Degenerating epidermal cells in Xenoturbella bocki (phylum uncertain), Nemertodermatida and Acoela (Platyhelminthes). Belg. J. Zool. 131, 153–157 (2001)

    Google Scholar 

  18. Westblad, E. Xenoturbella bocki n.g, n.sp, a peculiar, primitive turbellarian type. Arkiv Zool 1, 3–29 (1949)

    Google Scholar 

  19. Nielsen, C. After all: Xenoturbella is an acoelomorph!. Evol. Dev. 12, 241–243 (2010)

    Article  Google Scholar 

  20. Franzen, A. & Afzelius, B. A. The ciliated epidermis of Xenoturbella bocki (Platyhelminthes, Xenoturbellida) with some phylogenetic considerations. Zool. Scr. 16, 9–17 (1987)

    Article  Google Scholar 

  21. Pardos, F. Fine structure and function of pharynx cilia in Glossobalanus minutus Kowalewsky (Entropneusta). Acta Zool. 69, 1–12 (1988)

    Article  Google Scholar 

  22. Tyler, S. in Interrelationships of the Platyhelminthes (eds Littlewood, D. T. J. & Bray, R. A. ) 3–12 (Taylor & Francis, 2001)

    Google Scholar 

  23. Telford, M. J. Xenoturbellida: the fourth deuterostome phylum and the diet of worms. Genesis 46, 580–586 (2008)

    Article  Google Scholar 

  24. Baguña, J., Martinez, P., Paps, J. & Riutort, M. Back in time: a new systematic proposal for the Bilateria. Proc. R. Soc. B 363, 1481–1491 (2008)

    Google Scholar 

  25. Hejnol, A. & Martindale, M. Q. M. Acoel development supports a simple planula-like urbilaterian. Phil. Trans. R. Soc. B 363, 1493–1501 (2008)

    Article  Google Scholar 

  26. Peterson, K. J., McPeek, M. A. & Evans, D. A. Tempo and mode of early animal evolution: inferences from rocks, Hox, and molecular clocks. Paleobiology 31, 36–55 (2005)

    Article  Google Scholar 

  27. Ruppert, E. E. Key characters uniting hemichordates and chordates: homologies or homoplasies? Can. J. Zool. 83, 8–23 (2005)

    Article  Google Scholar 

  28. Philippe, H. et al. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 706–712 (2009)

    Article  CAS  Google Scholar 

  29. 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 

  30. Wheeler, B. et al. The deep evolution of metazoan microRNAs. Evol. Dev. 11, 50–68 (2009)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  32. Huang, X. & Madan, A. CAP3: a DNA assembly programme. Genome Res. 9, 868–877 (1999)

    Article  CAS  Google Scholar 

  33. Abascal, F., Zardoya, R. & Telford, M. J. TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res. 38, W7–W13 (2010)

    Article  CAS  Google Scholar 

  34. Jeanmougin, F., Thompson, J. D., Gouy, M., Higgins, D. G. & Gibson, T. J. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23, 403–405 (1998)

    Article  CAS  Google Scholar 

  35. Dunn, C. W. et al. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745–749 (2008)

    Article  ADS  CAS  Google Scholar 

  36. Philippe, H. MUST, a computer package of management utilities for sequences and trees. Nucleic Acids Res. 21, 5264–5272 (1993)

    Article  CAS  Google Scholar 

  37. Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552 (2000)

    Article  CAS  Google Scholar 

  38. Roure, B., Rodriguez-Ezpeleta, N. & Philippe, H. SCaFoS: a tool for selection, concatenation and fusion of sequences for phylogenomics. BMC Evol. Biol. 7 (Suppl. 1). S2 (2007)

    Article  Google Scholar 

  39. Schmidt, H. A., Strimmer, K., Vingron, M. & von Haeseler, A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502–504 (2002)

    Article  CAS  Google Scholar 

  40. Lartillot, N., Lepage, T. & Blanquart, S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25, 2286–2288 (2009)

    Article  CAS  Google Scholar 

  41. 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 (Suppl. 1). S4 (2007)

    Article  Google Scholar 

  42. Felsenstein, J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791 (1985)

    Article  Google Scholar 

  43. Felsenstein, J. PHYLIP (Phylogeny Inference Package) version 3.69 (Department of Genome Sciences, Univ. Washington, Seattle, 2005)

    Google Scholar 

  44. 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 

  45. Blanquart, S. & Lartillot, N. A site- and time-heterogeneous model of amino acid replacement. Mol. Biol. Evol. 25, 842–858 (2008)

    Article  CAS  Google Scholar 

  46. Hrdy, I. et al. Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432, 618–622 (2004)

    Article  ADS  CAS  Google Scholar 

  47. Roure, B. & Philippe, H. Site-specific time heterogeneity of the substitution process and its impact on phylogenetic inference. BMC Evol. Biol (in the press)

Download references

Acknowledgements

We thank N. Lartillot for reading the manuscript, W. Sterrer for helping collect material, and E. Sperling for help with small RNA library construction. H.P. is funded by Canada Research Chairs, Natural Sciences and Engineering Research Council and Réseau Québécois de Calcul de Haute Performance for computational resources: more than 220,000 central processing unit (CPU)–hours were used producing at least 7 tonnes of CO2 excluding grey energy. R.R.C. and M.J.T. were part-funded by the Biotechnology and Biological Sciences Research Council SYNTAX scheme. K.J.P. is supported by the National Science Foundation and NASA Ames. R.R.C. was also supported by a Wellcome Trust core award, grant number 075491/Z/04. A.J.P. was supported by the Max-Planck Society for the Advancement of Sciences e.V. A.W. was funded by Inez Johanssons Stiftelse and Stiftelsen Lars Hiertas Minne.

Author information

Author notes

  1. Hiroaki Nakano

    Present address: Present address: Shimoda Marine Research Center, University of Tsukuba, Shimoda, Shizuoka, 415-0025, Japan.,

Authors and Affiliations

  1. Département de Biochimie, Centre Robert-Cedergren, Université de Montréal, Succursale Centre-Ville, Montréal, Québec H3C 3J7, Canada

    Hervé Philippe & Henner Brinkmann

  2. Wellcome Trust Centre for Human Genetics, Roosevelt Drive, Oxford OX3 7BN, UK

    Richard R. Copley

  3. The Whitney Laboratory for Marine Biosciences and Department of Neuroscience, University of Florida, St Augustine and Gainesville, 32080, Florida, USA

    Leonid L. Moroz

  4. Department of Marine Ecology- Kristineberg, University of Gothenburg, 450 34 Fiskebäckskil, Sweden

    Hiroaki Nakano

  5. Evolution and Development Group, Max-Planck Institut für Molekulare Genetik, Ihnestrasse 73, Berlin, 14195, Germany

    Albert J. Poustka

  6. Department of Systematic Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, Uppsala, Sweden

    Andreas Wallberg

  7. Department of Biology, Dartmouth College, Hanover, 03755, New Hampshire, USA

    Kevin J. Peterson

  8. Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London WC1E 6BT, UK

    Maximilian J. Telford

Authors
  1. Hervé Philippe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Henner Brinkmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richard R. Copley
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leonid L. Moroz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hiroaki Nakano
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Albert J. Poustka
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Andreas Wallberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kevin J. Peterson
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Maximilian J. Telford
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

H.P. and M.J.T. conceived and designed the study. M.J.T. assembled mitochondrial data. H.P. and H.B. assembled EST data and performed phylogenetic analyses of ESTs and mitochondrial genomes. M.J.T., L.L.M. and R.R.C. performed preliminary phylogenomic analyses. H.N. collected Xenoturbella for genomic and miRNA data. A.W. collected Hofstenia. K.J.P. and A.W. produced Xenoturbella and Hofstenia miRNA libraries. K.J.P. assembled and analysed the miRNA matrix. M.J.T., R.R.C. and A.J.P. produced Xenoturbella genomic data. M.J.T. drafted the paper with H.P. and K.J.P. All authors commented on the manuscript.

Corresponding author

Correspondence to Maximilian J. Telford.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

MicroRNA sequences are deposited in http://www.mirbase.org and can be found in the Supplementary Information.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-16 with legends and Supplementary Tables 1-3. (PDF 1404 kb)

Supplementary Information

This file contains the aligned and concatenated mitochondrial genes used in phylogenetic analyses. (TXT 66 kb)

Supplementary Information

This file contains the aligned and concatenated nuclear genes used in phylogenetic analyses. (TXT 2471 kb)

Supplementary Information

This file contains the aligned and concatenated nuclear genes used in phylogenetic analyses derived from the data sets of Hejnol et al. (TXT 2262 kb)

Supplementary Information

This file contains the matrix of presence absence for microRNAs used in phylogenetic analyses. (TXT 7 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Philippe, H., Brinkmann, H., Copley, R. et al. Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470, 255–258 (2011). https://doi.org/10.1038/nature09676

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature09676

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing