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Acoelomorph Flatworms Are Deuterostomes Related to Xenoturbella

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Acoelomorph Flatworms Are Deuterostomes Related to Xenoturbella

Hervé Philippe et al. Nature.

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 deuterostomes and positioning the Acoelomorpha as the most basally branching bilaterian group(s). Recent phylogenomic data suggested that Xenoturbellida and Acoelomorpha are sister taxa and together constitute an early branch of Bilateria. 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 complements 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.

Figures

Figure 1
Figure 1. Alternative phylogenetic positions of Acoela, Nemertodermatida and Xenoturbellida with implied evolution of different characters
a, Tree based on refs and for positions of nemertodermatids and acoels, and refs and for position of Xenoturbella. b, Tree based on analyses of ref. . c, Tree based on the results from this paper. Protein RSB66 and deuterostome mitochondrial gene order are also indicated. miRNAs representing possible synapomorphies of Deuterostomia, Xenambulacraria and Xenacoelomorpha are shown in red. The minimum number of total steps to explain miRNA distribution is shown above trees. Losses and gains of miRNAs are shown on each branch. Complete trees are shown in Supplementary Figs 10–14. Bottom left, X. bocki and H. miamia (photographs by M.J.T. and A.W.).
Figure 2
Figure 2. Animal phylogeny based on mitochondrial proteins reconstructed using the CAT + GTR + Γ model under a Bayesian analysis
Xenoturbella and the four acoel species are sister taxa (PP = 0.99). This clade is grouped with the deuterostomes (PP = 0.99), but is excluded from within the clade with weak support (PP = 0.47). Cross-validation demonstrates that the GTR + Γ model has a better fit than the CAT + Γ model, albeit without statistical significance (ΔlnL = 20 ± 24), and that the CAT + GTR + Γ model has a significantly better fit than the GTR + Γ model (ΔlnL = 96 ± 21). Using less fit models (GTR + Γ and CAT + Γ), the support for association with the deuterostomes decreases (Supplementary Fig. 1). Scale bar, substitutions per position.
Figure 3
Figure 3. Phylogeny of 66 animal species based on EST sequences
Analysis of 197 genes, 38,330 unambiguously aligned positions, 30% missing data. Tree was reconstructed using the CAT + Γ model under a Bayesian analysis. Major accepted metazoan clades (for example, Lophotrochozoa, Ecdysozoa, Protostomia) are supported. Acoela and Nemertodermatida are sister groups (Acoelomorpha). Xenoturbella and Acoelomorpha are sister groups (phylum Xenacoelomorpha). Xenacoelomorpha is the sister taxon of Ambulacraria (Xenambulacraria) within the deuterostomes. Level of bootstrap support is indicated. Similar support is obtained when jack-knifing 50% of the genes (Supplementary Fig. 9). Scale bar, substitutions per position.

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