Acoelomorph flatworms are deuterostomes related to Xenoturbella

Abstract

Xenoturbellida and Acoelomorpha are marine worms with contentious ancestry. Both were originally associated with the flatworms (Platyhelminthes), but molecular data haverevised their phylogenetic positions, generally linking Xenoturbellida to the deuterostomes1,2 and positioning the Acoelomorpha as the most basally branching bilaterian group(s)3–6. Recent phylogenomic data suggested that Xenoturbellida and Acoelomorpha are sister taxa and together constitute an early branch of Bilateria7. 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 complements8 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.

Genomic data do not support comb jellies as the sister group to all other animals

“…We investigated whether previous studies supporting Ctenophora-sister were conducted using adequately fitting substitution models. Using three exemplar datasets, which we call Ryan-Choano, Moroz-3D, and Whelan-6-Choano (details are provided below and in Methods), we compared the relative fit of site-homogeneous and siteheterogeneous models using Bayesian cross-validation (36, 37), a routine statistical technique used to evaluate the predictive performance of a probabilistic model, which has been commonly used in the context of phylogenetics (23,24,(38)(39)(40)(41). Using 10 cross-validation replicates, we found that in all cases, site-heterogeneous models fit these data significantly better than the site-homogeneous models that previous studies mostly relied upon ( Table 1).…”

“…To address this issue, site-heterogeneous models have been developed (22), which relax the homogeneity assumption to account for site-specific biochemical constraints. Although computationally more demanding, their increased capacity to identify convergent evolution is reflected in the better statistical fit these models generally provide to many empirical datasets (e.g., 23,24). Here, we used a common statistical technique, Bayesian cross-validation, to compare the fit of site-homogeneous and site-heterogeneous models, and investigate whether previous studies that recovered Ctenophora-sister were influenced by the use of poorly fitting substitution models.…”

Acoelomorpha: earliest branching bilaterians or deuterostomes?

“…A definitive break from the line of studies suggesting acoelomorphs as the sister group to the rest of bilaterians came with a complete phylogenomic analyses that concluded that both Xenoturbella and Acoelomorpha (named the Xenacoelomorpha clade) were deuterostomes (Philippe et al 2011a). This study considered four different lines of evidence: mitochondrial protein coding genes, nuclear-coding phylogenomic analyses (a subset of the genes used by Hejnol et al 2009), microRNA content, and the absence/ presence of the gene Rsb66.…”

“…c Summary of the first molecular phylogenies with a significative taxon sampling for Acoelomorpha and applying methodologies to overcome long-brach attraction (LBA) problems, based on diverse markers such as 18S rRNA, multiple genes, or phylogenomic approaches (see text for references). d Alternative phylogenomic hypothesis, placing acoelomorphs as sister to deuterostomes or within them, supported by Philippe et al (2011a) by molecular qualitative traits such as Hox genes (Cook et al 2004;Jimenez-Guri et al 2006), changes in the mitochondrial genetic code (Telford et al 2000), miRNAs (Pasquinelli et al 2003) and mtDNA gene rearrangements (Ruiz-Trillo et al 2004). These compelling emerging data lead some authors to define Acoelomorpha and Platyhelminthes as two different metazoan phyla (Baguñà and Riutort 2004a).…”

Phylogeny: Rewriting evolution

“…library to resolve relationships within and between an assortment of evolutionary lineages, from jawless fishes 5 and reptiles 6 to fruitflies 7 and acoelomorph worms 8 .…”