Broad phylogenomic sampling improves resolution of the animal tree of life (original) (raw)

Nature volume 452, pages 745–749 (2008)Cite this article

Abstract

Long-held ideas regarding the evolutionary relationships among animals have recently been upended by sometimes controversial hypotheses based largely on insights from molecular data1,2. These new hypotheses include a clade of moulting animals (Ecdysozoa)3 and the close relationship of the lophophorates to molluscs and annelids (Lophotrochozoa)4. Many relationships remain disputed, including those that are required to polarize key features of character evolution, and support for deep nodes is often low. Phylogenomic approaches, which use data from many genes, have shown promise for resolving deep animal relationships, but are hindered by a lack of data from many important groups. Here we report a total of 39.9 Mb of expressed sequence tags from 29 animals belonging to 21 phyla, including 11 phyla previously lacking genomic or expressed-sequence-tag data. Analysed in combination with existing sequences, our data reinforce several previously identified clades that split deeply in the animal tree (including Protostomia, Ecdysozoa and Lophotrochozoa), unambiguously resolve multiple long-standing issues for which there was strong conflicting support in earlier studies with less data (such as velvet worms rather than tardigrades as the sister group of arthropods5), and provide molecular support for the monophyly of molluscs, a group long recognized by morphologists. In addition, we find strong support for several new hypotheses. These include a clade that unites annelids (including sipunculans and echiurans) with nemerteans, phoronids and brachiopods, molluscs as sister to that assemblage, and the placement of ctenophores as the earliest diverging extant multicellular animals. A single origin of spiral cleavage (with subsequent losses) is inferred from well-supported nodes. Many relationships between a stable subset of taxa find strong support, and a diminishing number of lineages remain recalcitrant to placement on the tree.

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Acknowledgements

We thank all participants in the Protostome Assembling the Tree of Life (AToL) Project as well as E. J. Edwards, T. Dubuc, A. Stamatakis, J. Q. Henry and S. Maslakova. A.H. received support from the Deutsche Forschungsgemeinschaft, and M.O. received support from the Swedish Taxonomy Initiative and the Royal Swedish Academy of Sciences. The Capitella sp. EST data were produced by the US Department of Energy Joint Genome Institute (http://www.jgi.doe.gov/Capitella), as were the Mnemiopsis dbEST (http://www.ncbi.nlm.nih.gov/dbEST/) data. This work was funded by two consecutive collaborative grants from the AToL program from the US National Science Foundation. Ctenophore sequencing was supported by NASA.

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Author notes

  1. Casey W. Dunn
    Present address: Present address: Department of Ecology and Evolutionary Biology, Brown University, 80 Waterman Street, Providence, Rhode Island 02912, USA.,

Authors and Affiliations

  1. Kewalo Marine Laboratory, PBRC, University of Hawaii, 41 Ahui Street, Honolulu, Hawaii 96813, USA,
    Casey W. Dunn, Andreas Hejnol, David Q. Matus, Kevin Pang, William E. Browne, Elaine Seaver & Mark Q. Martindale
  2. Department of Ecology and Evolutionary Biology, Yale University, PO Box 208105, New Haven, Connecticut 06520, USA,
    Stephen A. Smith
  3. Scripps Institution of Oceanography, University of California San Diego, 9500 Gilman Drive 0202, La Jolla, California 92093, USA,
    Greg W. Rouse
  4. Kristineberg Marine Research Station, Kristineberg 566, 450 34 Fiskebäckskil, Sweden,
    Matthias Obst
  5. Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK,
    Gregory D. Edgecombe
  6. Ancient DNA and Evolution Group, Biological Institute, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark,
    Martin V. Sørensen
  7. Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, California 95039, USA,
    Steven H. D. Haddock
  8. Zoological Museum, University of Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany,
    Andreas Schmidt-Rhaesa
  9. Biology Department, Simmons College, The Fenway, Boston, Massachusetts 02115, USA,
    Akiko Okusu
  10. Zoological Museum, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark,
    Reinhardt Møbjerg Kristensen
  11. Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024, USA,
    Ward C. Wheeler
  12. Department of Organismic and Evolutionary Biology,,
    Gonzalo Giribet
  13. Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138, USA,
    Gonzalo Giribet

Authors

  1. Casey W. Dunn
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  2. Andreas Hejnol
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  3. David Q. Matus
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  4. Kevin Pang
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  5. William E. Browne
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  6. Stephen A. Smith
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  7. Elaine Seaver
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  8. Greg W. Rouse
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  9. Matthias Obst
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  10. Gregory D. Edgecombe
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  11. Martin V. Sørensen
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  12. Steven H. D. Haddock
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  13. Andreas Schmidt-Rhaesa
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  14. Akiko Okusu
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  15. Reinhardt Møbjerg Kristensen
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  16. Ward C. Wheeler
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  17. Mark Q. Martindale
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  18. Gonzalo Giribet
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Corresponding author

Correspondence toCasey W. Dunn.

Additional information

The concatenated sequence matrix has been deposited at TreeBase (http://www.treebase.org). The raw sequence data are available at the NCBI Trace Archives (http://www.ncbi.nlm.nih.gov/Traces), and can be retrieved with the query ‘center_name = 'KML-UH'’.

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Supplementary Information

This file contains the Supplementary Discussions, Supplementary Tables 1-4, and Supplementary Figures 1-10 with Legends and additional references. (PDF 1800 kb)

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Dunn, C., Hejnol, A., Matus, D. et al. Broad phylogenomic sampling improves resolution of the animal tree of life.Nature 452, 745–749 (2008). https://doi.org/10.1038/nature06614

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Editorial Summary

Improved relations

The accumulation of molecular data is reshaping our understanding of the evolutionary relationships between the major groups of animals. Early work in the field relied upon data from a small number of genes, but the availability of fully sequenced genomes and expressed sequence tags (ESTs, short sub-sequences obtained from large numbers of complementary DNA clones), means that huge swathes of the animal kingdom can now be subjected to such analysis. A new study describes and discusses almost 40 megabases-worth of ESTs from animals of 21 phyla, including 11 animals for which no genomic or EST data were previously available. The conclusions confirm ideas long established by anatomy, including the monophyletic nature of the molluscs, deriving from a common ancestor despite their remarkable variety. New and interesting evolutionary relationships are also uncovered, including a single origin for spiral cleavage of the early embryo. The cover illustrates animal diversity, including acorn, ribbon, arrow and velvet worms, jellyfish and sea spider.