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Xenacoelomorpha Is the Sister Group to Nephrozoa

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Xenacoelomorpha Is the Sister Group to Nephrozoa LETTER doi:10.1038/nature16520 Xenacoelomorpha is the sister group to Nephrozoa Johanna Taylor Cannon1, Bruno Cossermelli Vellutini2, Julian Smith III3, Fredrik Ronquist1, Ulf Jondelius1 & Andreas Hejnol2 The position of Xenacoelomorpha in the tree of life remains a major as sister taxon to remaining Bilateria19 (Fig. 1b–e). The deuterostome unresolved question in the study of deep animal relationships1. affiliation derives support from three lines of evidence4: an analysis Xenacoelomorpha, comprising Acoela, Nemertodermatida, and of mitochondrial gene sequences, microRNA complements, and a Xenoturbella, are bilaterally symmetrical marine worms that lack phylogenomic data set. Analyses of mitochondrial genes recovered several features common to most other bilaterians, for example Xenoturbella within deuterostomes18. However, limited mitochon- an anus, nephridia, and a circulatory system. Two conflicting drial data (typically ~16 kilobase total nucleotides, 13 protein-coding hypotheses are under debate: Xenacoelomorpha is the sister group genes) are less efficient in recovering higher-level animal relationships to all remaining Bilateria (= Nephrozoa, namely protostomes than phylogenomic approaches, especially in long-branching taxa1. and deuterostomes)2,3 or is a clade inside Deuterostomia4. Thus, The one complete and few partial mitochondrial genomes for acoelo- determining the phylogenetic position of this clade is pivotal for morphs are highly divergent in terms of both gene order and nucleotide understanding the early evolution of bilaterian features, or as a sequence19,20. Analyses of new complete mitochondrial genomes of case of drastic secondary loss of complexity. Here we show robust Xenoturbella spp. do not support any phylogenetic hypothesis for this phylogenomic support for Xenacoelomorpha as the sister taxon taxon21. Ref. 4 proposes that microRNA data support Xenacoelomorpha of Nephrozoa. Our phylogenetic analyses, based on 11 novel within the deuterostomes; however, microRNA distribution is better xenacoelomorph transcriptomes and using different models of explained by a sister relationship between Xenacoelomorpha and evolution under maximum likelihood and Bayesian inference Nephrozoa both under parsimony4,22 and under Bayesian inference22. analyses, strongly corroborate this result. Rigorous testing of Phylogenomic analyses recovering xenacoelomorph taxa within 25 experimental data sets designed to exclude data partitions and Deuterostomia show branching patterns that differ significantly taxa potentially prone to reconstruction biases indicates that long- branch attraction, saturation, and missing data do not influence a these results. The sister group relationship between Nephrozoa and Xenacoelomorpha 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 Nemertodermatida Acoela Xenoturbella gut, and that excretory organs, coelomic cavities, and nerve cords evolved after xenacoelomorphs separated from the stem lineage of Nephrozoa. Acoela have an essential role in hypotheses of bilaterian body plan evolution5. Acoels have been compared to cnidarian planula larvae because they possess characters such as a blind gut, a net-like nervous bc system, and they lack nephridia. However, they also share apomorphies Xenacoelomorpha Protostomia with Bilateria such as bilateral symmetry and a mesodermal germ layer Protostomia Chordata Bilateria Bilateria that gives rise to circular and longitudinal muscles. Classic systematics Chordata Xenacoelomorpha placed acoels in Platyhelminthes6, or as a separate early bilaterian lin- Nephrozoa Deuterostomia Deuterostomia Ambulacraria Xenambulacraria Ambulacraria eage7,8. When nucleotide sequence data became available, Acoela were placed as the sister group of Nephrozoa9. Nemertodermatida were orig- deAcoelomorpha inally classified within Acoela, but were soon recognized as a separate Protostomia 10 Protostomia clade on morphological grounds . Subsequently, nucleotide sequence Xenacoelomorpha Bilateria Bilateria Chordata data fuelled a debate on whether nemertodermatids and acoels form a Chordata Nephrozoa Deuterostomia Xenoturbella monophyletic group, the Acoelomorpha, or if nemertodermatids and Ambulacraria Deuterostomia acoels are independent early bilaterian lineages as suggested by several Xenambulacraria Ambulacraria studies, for example refs 11 and 12. The enigmatic Xenoturbella was Figure 1 | Phylogenetic hypotheses concerning Xenacoelomorpha from first placed together with Acoela and Nemertodermatida13,14; then an previous molecular studies. a, Relationships among Xenacoelomorpha. ultrastructural appraisal supported its position as sister group of all Xenoturbella is sister to Acoelomorpha (Acoela + Nemertodermatida). other bilaterians15. The first molecular study suggested Xenoturbella Illustrated species from left to right: Flagellophora apelti, Diopisthoporus to be closely related to molluscs16, whereas other analyses proposed psammophilus, X. bocki. b, Xenacoelomorpha is sister taxon to 17,18 Nephrozoa (phylogenomic analyses2,3). c, Xenacoelomorpha is sister a deuterostome affiliation . Recent analyses of molecular data reu- 4 nited Xenoturbella with acoels and nemertodermatids2–4 to form a clade taxon to Ambulacraria within deuterostomes (phylogenomic analyses ). d, Xenacoelomorpha is sister taxon to Ambulacraria + Chordata called Xenacoelomorpha (Fig. 1a). (mitochondrial protein analyses4,19). e, Xenoturbella is within Current conflicting hypotheses suggest that Xenacoelomorpha are Deuterostomia, while Acoelomorpha form two separate clades outside 4 4 the sister group of Deuterostomia , are nested within Deuterostomia , Nephrozoa (molecular systematic analyses11), or its sister group 2,3 are the sister group of Nephrozoa , or are polyphyletic, with (some mitochondrial protein analyses19). Colours in b–e indicate Xenoturbella included within Deuterostomia and the Acoelomorpha Xenacoelomorpha (red), Protostomia (blue), Deuterostomia (green). 1Naturhistoriska Riksmuseet, PO Box 50007, SE-104 05 Stockholm, Sweden. 2Sars International Centre for Marine Molecular Biology, University of Bergen, Thormøhlensgate 55, 5008 Bergen, Norway. 3Department of Biology, Winthrop University, 701 Oakland Avenue, Rock Hill, South Carolina 29733, USA. 4 FEBRUARY 2016 | VOL 530 | NATURE | 89 © 2016 Macmillan Publishers Limited. All rights reserved RESEARCH LETTER Xenacoelomorpha Xenoturbella bocki Diopisthoporus gymnopharyngeus Diopisthoporus longitubus Acoela Hofstenia miamia 63/76/63 Isodiametra pulchra Eumecynostomum macrobursalium Convolutriloba macropyga 92/96/92 Childia submaculatum Ascoparia sp. Meara stichopi Nemertodermatida Sterreria sp. Nemertoderma westbladi Priapulus caudatus Halicryptus spinulosus Priapulida Ecdysozoa Peripatopsis capensis Onychophora Drosophila melanogaster Daphnia pulex Strigamia maritima Arthropoda Bilateria 47/65/47 Ixodes scapularis Helobdella robusta Pomatoceros lamarckii Annelida Spiralia Capitella teleta Phoronis psammophila Terebratalia transversa Lophophorata Hemithiris psittacea (Phoronida + Brachiopoda) Novocrania anomala 78/85/78 Lineus longissimus Cephalothrix hongkongiensis Nemertea 71/60/71 Leptochiton rugatus Crassostrea gigas Mollusca Lottia gigantea Adineta ricciae Adineta vaga Rotifera Platyhelminthes 96/100/96 Brachionus calyciflorus Nephrozoa Schmidtea mediterranea 99/ Schistosoma mansoni 100/ 98/98/98 Taenia pisiformes 99 Prostheceraeus vittatus 66/78/66 Macrostomum lignano Lepidodermella squamata 39/43/39 70/ Megadasys sp. Gastrotricha 74/ Macrodasys sp. 70 Membranipora membranacea Bryozoa 95/99/95 Loxosoma pectinaricola Barentsia gracilis Entoprocta Branchiostoma floridae 95/99/95 Botryllus schlosseri Deuterostomia Ciona intestinalis Chordata Homo sapiens Gallus gallus Petromyzon marinus Dumetocrinus sp. 67/--/67 Labidiaster annulatus 77/52/77 89/97/89 Astrotomma agassizi Leptosynapta clarki Ambulacraria 86/76/86 Strongylocentrotus purpuratus (Echinodermata Cephalodiscus gracilis +Hemichordata) 67/--/67 Saccoglossus mereschkowskii Ptychodera bahamensis Schizocardium braziliense Eunicella cavolinii Nematostella vectensis Acropora digitifera Stomolophus meleagris Cnidaria Craspedacusta sowerby Agalma elegans Trichoplax adhaerens Placozoa Oscarella carmela 87/83/87 Leucosolenia complicata 55/53/55 Sycon ciliatum Aphrocallistes vastus Porifera Cliona varians Amphimedon queenslandica Mnemiopsis leidyi Pleurobrachia bachei Ctenophora Euplokamis dunlapae Monosiga brevicollis Salpingoeca rosetta Choanoagellata BS support =100% all models, ProtTest/LG4X/LG 0.2 Figure 2 | Maximum likelihood topology of metazoan relationships model for each orthologous group selected by ProtTest/LG4X across inferred from 212 genes. Maximum likelihood tree is shown as inferred all partitions/LG + I + Γ across all partitions, 100 bootstrap replicates). using the best-fitting amino-acid substitution model for each gene. Filled blue circles represent 100% bootstrap support under all models of Bootstrap support values from analyses inferred under alternative evolution. Species indicated in bold are new transcriptomes published models of amino-acid substitution are indicated at the nodes (best-fitting with this study. between alternative models of evolution4. Conflicting results in stud- diverse metazoans (Supplementary Table 1). Acoel and nemertoder- ies that used the same expressed sequence tag data for xenacoelo- matid species
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