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Tunicates and not cephalochordates are the closest living relatives of vertebrates

Naturevolume 439, pages965–968 (2006)Cite this article

Abstract

Tunicates or urochordates (appendicularians, salps and sea squirts), cephalochordates (lancelets) and vertebrates (including lamprey and hagfish) constitute the three extant groups of chordate animals. Traditionally, cephalochordates are considered as the closest living relatives of vertebrates, with tunicates representing the earliest chordate lineage1,2. This view is mainly justified by overall morphological similarities and an apparently increased complexity in cephalochordates and vertebrates relative to tunicates2. Despite their critical importance for understanding the origins of vertebrates3, phylogenetic studies of chordate relationships have provided equivocal results4,5,6,7. Taking advantage of the genome sequencing of the appendicularianOikopleura dioica, we assembled a phylogenomic data set of 146 nuclear genes (33,800 unambiguously aligned amino acids) from 14 deuterostomes and 24 other slowly evolving species as an outgroup. Here we show that phylogenetic analyses of this data set provide compelling evidence that tunicates, and not cephalochordates, represent the closest living relatives of vertebrates. Chordate monophyly remains uncertain because cephalochordates, albeit with a non-significant statistical support, surprisingly grouped with echinoderms, a hypothesis that needs to be tested with additional data. This new phylogenetic scheme prompts a reappraisal of both morphological and palaeontological data and has important implications for the interpretation of developmental and genomic studies in which tunicates and cephalochordates are used as model animals.

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Figure 1:Phylogenetic analyses of genomic data strongly support the grouping of tunicates and vertebrates into Olfactores.

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Acknowledgements

We thank S. Conway Morris, R. P. S. Jefferies, W. R. Jeffery and J. Mallatt for suggestions, and N. Lartillot and N. Rodrigue for critical readings of early versions of the manuscript.Oikopleura genome data were generated at Génoscope Evry (France) with material and co-funding from the Sars International Centre. We are grateful to P. Wincker and the Génoscope team. We gratefully acknowledge the financial support provided by Génome Québec, the Canadian Research Chair and the Université de Montréal, and the Réseau Québecois de Calcul de Haute Performance for computational resources. Author Contributions H.P. conceived the study. D.C. contributed sequence data from theOikopleura genome project. F.D., H.B. and H.P. assembled the data set and performed phylogenetic analyses. F.D. wrote the first draft of the manuscript and all authors contributed to the writing of its final version.

Author information

Author notes

  1. Frédéric Delsuc

    Present address: Laboratoire de Paléontologie, Phylogénie et Paléobiologie, Institut des Sciences de l'Evolution, UMR 5554-CNRS, Université Montpellier II, France

Authors and Affiliations

  1. Département de Biochimie, Centre Robert-Cedergren, Université de Montréal, Succursale Centre-Ville, Québec, H3C3J7, Montréal, Canada

    Frédéric Delsuc, Henner Brinkmann & Hervé Philippe

  2. Sars Centre for Marine Molecular Biology, Bergen High Technology Centre, University of Bergen, Thormøhlensgaten 55, 5008, Bergen, Norway

    Daniel Chourrout

Authors
  1. Frédéric Delsuc
  2. Henner Brinkmann
  3. Daniel Chourrout
  4. Hervé Philippe

Corresponding author

Correspondence toHervé Philippe.

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Competing interests

Reprints and permissions information is available atnpg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary methods

This file describes the protocol used to assemble the genomic data. More details on the phylogenetic analyses are also provided with investigations of the effects of taxon sampling, compositional bias and heterotachy on tree reconstruction.

Supplementary Table 1

This table provides the list of all 146 gene names and the number of amino acid positions conserved for each gene alignment.

Supplementary Table 2

This table summarizes the amount and occurrence of missing data per taxa in the complete dataset.

Supplementary Figure 1

This figure presents the most parsimonious tree obtained withOikopleura dioica used as the single representative of tunicates.

Supplementary Figure 2

This figure shows the maximum likelihood tree obtained with a reduced dataset usingOikopleura as the single representative of tunicates.

Supplementary Figure 3

This figure presents a principal component analysis (PCA) of amino acid frequencies on the complete dataset.

Supplementary Figure 4

This figure shows the maximum likelihood tree obtained with a reduced dataset where the sea-urchin (Strongylocentrotus) is removed from the complete dataset.

Supplementary Figure 5

This figure shows the most parsimonious tree obtained from the complete dataset recoded into six Dayhoff categories.

Supplementary Figure 6

This figure presents the maximum likelihood topology identified by the partitioned-likelihood analysis on the complete dataset.

Supplementary Figure 7

This figure shows the majority rule consensus tree obtained from Bayesian analysis of the complete dataset under a covarion model.

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Delsuc, F., Brinkmann, H., Chourrout, D.et al. Tunicates and not cephalochordates are the closest living relatives of vertebrates.Nature439, 965–968 (2006). https://doi.org/10.1038/nature04336

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Editorial Summary

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A phylogenetic comparison of the protein sequences of 146 genes from 14 deuterostome species has come up with a result that could alter current thinking on the origin of the vertebrates. Based on overall morphology and on complexity, it was thought that the cephalochordates (marine organisms known as lancelets, or in old textbooks as amphioxus) were the vertebrates' closest living relatives. Closer than the tunicates (appendicularians, salps, and sea squirts), that were regarded as the earliest chordate lineage. But the new data suggest that tunicates, and not cephalochordates, are the closest living relatives of vertebrates. As well as the implications for vertebrate origins, this has a bearing on developmental studies in which tunicates and cephalochordates are used as model animals.

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