Letter | Published:

Xenacoelomorpha is the sister group to Nephrozoa

Nature volume 530, pages 8993 (04 February 2016) | Download Citation

Abstract

The position of Xenacoelomorpha in the tree of life remains a major unresolved question in the study of deep animal relationships1. Xenacoelomorpha, comprising Acoela, Nemertodermatida, and Xenoturbella, are bilaterally symmetrical marine worms that lack several features common to most other bilaterians, for example an anus, nephridia, and a circulatory system. Two conflicting hypotheses are under debate: Xenacoelomorpha is the sister group to all remaining Bilateria (= Nephrozoa, namely protostomes and deuterostomes)2,3 or is a clade inside Deuterostomia4. Thus, determining the phylogenetic position of this clade is pivotal for understanding the early evolution of bilaterian features, or as a case of drastic secondary loss of complexity. Here we show robust phylogenomic support for Xenacoelomorpha as the sister taxon of Nephrozoa. Our phylogenetic analyses, based on 11 novel xenacoelomorph transcriptomes and using different models of evolution under maximum likelihood and Bayesian inference analyses, strongly corroborate this result. Rigorous testing of 25 experimental data sets designed to exclude data partitions and taxa potentially prone to reconstruction biases indicates that long-branch attraction, saturation, and missing data do not influence these results. The sister group relationship between Nephrozoa and Xenacoelomorpha supported by our phylogenomic analyses implies that the last common ancestor of bilaterians was probably a benthic, ciliated acoelomate worm with a single opening into an epithelial gut, and that excretory organs, coelomic cavities, and nerve cords evolved after xenacoelomorphs separated from the stem lineage of Nephrozoa.

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Acknowledgements

The Swedish Research Council provided funding for U.J. and J.T.C. (grant 2012-3913) and F.R. (grant 2014-5901). A.H. received support from the Sars Core budget and Marie Curie Innovative Training Networks ‘NEPTUNE’ (FP7-PEOPLE-2012-ITN 317172) and FP7-PEOPLE-2009-RG 256450. We thank N. Lartillot and K. Kocot for discussions. Hejnol laboratory members K. Pang and A. Børve assisted with RNA extraction; A. Boddington, J. Bengtsen and A. Elde assisted with culture for Isodiametra pulchra and Convolutriloba macropyga. Thanks to W. Sterrer for collection of Sterreria sp. and Ascoparia sp., and to R. Janssen for finding X. bocki. The Sven Lovén Centre of Marine Sciences Kristineberg, University of Gothenburg, and the Interuniversity Institute of Marine Sciences in Eilat provided logistical support for field collection. S. Baldauf assisted with laboratory space and resources for complementary DNA synthesis. We thank K. Larsson for the original illustrations. Computations were performed on resources provided by the Swedish National Infrastructure for Computing (SNIC). Transcriptome assembly, data set construction, RAxML and PhyloBayes analyses were performed using resources provided through Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) under project b2013077, and MrBayes analyses were run under project snic2014-1-323.

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  1. Naturhistoriska Riksmuseet, PO Box 50007, SE-104 05 Stockholm, Sweden

    • Johanna Taylor Cannon
    • , Fredrik Ronquist
    •  & Ulf Jondelius
  2. Sars International Centre for Marine Molecular Biology, University of Bergen, Thormøhlensgate 55, 5008 Bergen, Norway

    • Bruno Cossermelli Vellutini
    •  & Andreas Hejnol
  3. Department of Biology, Winthrop University, 701 Oakland Avenue, Rock Hill, South Carolina 29733, USA

    • Julian Smith

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Contributions

J.T.C., U.J., B.C.V., and A.H. conceived and designed the study. U.J. and A.H. collected several specimens and J.S. III collected Diopisthoporus gymnopharyngeus specimens. J.T.C. and B.C.V. performed molecular work and RNA sequencing assembly. J.T.C. assembled the datasets and performed phylogenetic analyses. F.R. conducted Bayesian phylogenetic analyses using MrBayes. All authors contributed to writing the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Johanna Taylor Cannon or Andreas Hejnol.

Sequence data have been deposited in the NCBI Sequence Read Archive under BioProject PRJNA295688. Data matrices and trees from this study are available from the Dryad Digital Repository (http://datadryad.org) under DOI 10.5061/dryad.493b7.

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    Supplementary Information

    This file contains a Supplementary Discussion, Supplementary Tables 1-3 and Supplementary Figures 1-22.

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https://doi.org/10.1038/nature16520

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