Acoelomorph flatworms are deuterostomes related to Xenoturbella

Abstract

The acoel flatworms are among the simplest animal forms, so simple that they have neither a through-gut nor a body cavity. But new molecular research has pulled them from their basal position in animal evolution, uniting them with creatures such as echinoderms (starfish, sea urchins and the like) and placing them much closer to the chordates, the group that includes humans. This follows previous revelations that Xenoturbella, a simple flatworm with mysterious evolutionary connections, also belonged to this group. The research implies that acoels are not primitively simple, as had been thought, but have become simpler with time, losing features such as a body cavity, anus and gill slits. New molecular research has pulled acoel flatworms from their basal position in animal evolution, uniting them with creatures such as echinoderms (starfish, sea urchins and allies) — indeed, very much closer to the chordates, the group that includes ourselves. The work follows previous revelations that Xenoturbella, a simple flatworm of mysterious evolutionary connections, also belonged to this group. The research implies that acoels are not primitively simple, as had been thought, but have lost features such as a body cavity, anus and gill slits. 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 deuterostomes1,2 and positioning the Acoelomorpha as the most basally branching bilaterian group(s)3,4,5,6. 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.