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Nature
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Xenacoelomorpha is the sister group to Nephrozoa

Naturevolume 530, pages89–93 (2016)Cite this article

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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, andXenoturbella, 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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Figure 1: Phylogenetic hypotheses concerning Xenacoelomorpha from previous molecular studies.
Figure 2: Maximum likelihood topology of metazoan relationships inferred from 212 genes.
Figure 3: Bayesian inference topology of metazoan relationships inferred from 212 genes under the CAT + GTR + Γ model.
Figure 4: Summary of metazoan relationships as inferred in this study.

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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 forIsodiametra pulchra andConvolutriloba macropyga. Thanks to W. Sterrer for collection ofSterreria sp. andAscoparia sp., and to R. Janssen for findingX. 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.

Author information

Authors and Affiliations

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

    Johanna Taylor Cannon, Fredrik Ronquist & Ulf Jondelius

  2. Sars International Centre for Marine Molecular Biology, University of Bergen, Thormøhlensgate 55, Bergen, 5008, Norway

    Bruno Cossermelli Vellutini & Andreas Hejnol

  3. Department of Biology, Winthrop University, 701 Oakland Avenue, Rock Hill, 29733, South Carolina, USA

    Julian Smith

Authors
  1. Johanna Taylor Cannon
  2. Bruno Cossermelli Vellutini
  3. Julian Smith
  4. Fredrik Ronquist
  5. Ulf Jondelius
  6. Andreas Hejnol

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 collectedDiopisthoporus 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.

Corresponding authors

Correspondence toJohanna Taylor Cannon orAndreas Hejnol.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Sequence data have been deposited in the NCBI Sequence Read Archive under BioProjectPRJNA295688. Data matrices and trees from this study are available from the Dryad Digital Repository (http://datadryad.org) under DOI10.5061/dryad.493b7.

Extended data figures and tables

Extended Data Figure 1 Maximum likelihood topology of metazoan relationships inferred from 336 genes from the best-sampled 56 taxa.

Maximum likelihood tree is shown as inferred using the LG + I + Γ model for each gene partition, and 100 bootstrap replicates. Filled blue circles represent 100% bootstrap support. The length of the matrix is 81,451 amino acids and overall matrix completeness is 89%.

Extended Data Figure 2 Maximum likelihood topology of metazoan relationships inferred from 881 genes and 77 taxa.

Maximum likelihood tree is shown as inferred using the LG + I + Γ model for each gene partition, and 100 bootstrap replicates. Filled blue circles represent 100% bootstrap support. The length of the matrix is 337,954 amino acids and overall matrix completeness is 62%.

Extended Data Figure 3 Maximum likelihood topology of metazoan relationships inferred from 212 genes with Acoelomorpha removed.

Maximum likelihood tree is shown as inferred using the LG + I + Γ model for each gene partition, and 100 bootstrap replicates. Filled blue circles represent 100% bootstrap support. The length of the matrix is 43,942 amino acids and overall matrix completeness is 70%.

Extended Data Figure 4 ASTRAL species tree, constructed from 212 input partial gene trees inferred in RAxML version 8.0.20.

Nodal support values reflect the frequency of splits in trees constructed by ASTRAL from 100 bootstrap replicate gene trees.

Extended Data Figure 5 Bayesian inference topology of metazoan relationships inferred on the basis of 212 genes and 78 taxa.

Results are shown from MrBayes analyses of four independent Metropolis-coupled chains run for 4,000,000 generations, with sampling every 500 generations. Amino-acid data were back-translated to nucleotides and analysed under an independent substitution model.

Extended Data Table 1 Summary of data sets analysed in this study and support for monophyly of major groups

Supplementary information

Supplementary Information

This file contains a Supplementary Discussion, Supplementary Tables 1-3 and Supplementary Figures 1-22. (PDF 5072 kb)

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Cannon, J., Vellutini, B., Smith, J.et al. Xenacoelomorpha is the sister group to Nephrozoa.Nature530, 89–93 (2016). https://doi.org/10.1038/nature16520

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Editorial Summary

Solving theXenoturbella puzzle

Lacking a centralized nervous system, coelom, anus and reproductive organs, the deep-sea flatwormXenoturbella presents problems when it comes to its classification and teasing out its evolutionary history. Despite its simplicity, some ofXenoturbella's features appear to align it among the deuterostomes, the group of animals that includes ourselves. If true, this implies either a radical simplification of the body plan or the acquisition of many key deuterostome features independently by the various deuterostome groups. Two papers in this issue tackle different aspects ofXenoturbella, but together, move the field on a notch. Greg Rouseet al. add four new deep-sea species ofXenoturbella from the eastern Pacific Ocean to the two already known from the Atlantic. Phylogenomic analysis aligns them at the base of the Protostomia or even as basal bilaterians — much as would be expected from their simple morphology and not invoking radical simplification. Andreas Hejnol and colleagues come to a broadly similar conclusion based on robust phylogenetic analysis using eleven transcriptomes ofXeonturbella and acoel worms.

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