To Be or Not to Be a Flatworm: The Acoel Controversy

Bernhard Egger,Robert Gschwentner,Daniela Pfister,Georg Kuales,Kiyokazu Agata,Gaëtan Borgonie,Detlev Arendt,Seth Tyler,Sachiko Ishida,Martina Hrouda,Bert Hobmayer,Willi Salvenmoser,Osamu Nishimura,Volker Hartenstein,Noriko Funayama,Chiyoko Kobayashi,Walter Salzburger,Katrien De Mulder,Ulrich Technau,Peter Ladurner,Dirk Steinke,Hiroshi Tarui,Julian P Smith ,Reinhard M Rieger ,Matthew D Hooge

doi:10.1371/journal.pone.0005502

Abstract

Since first described, acoels were considered members of the flatworms (Platyhelminthes). However, no clear synapomorphies among the three large flatworm taxa - the Catenulida, the Acoelomorpha and the Rhabditophora - have been characterized to date. Molecular phylogenies, on the other hand, commonly positioned acoels separate from other flatworms. Accordingly, our own multi-locus phylogenetic analysis using 43 genes and 23 animal species places the acoel flatworm Isodiametra pulchra at the base of all Bilateria, distant from other flatworms. By contrast, novel data on the distribution and proliferation of stem cells and the specific mode of epidermal replacement constitute a strong synapomorphy for the Acoela plus the major group of flatworms, the Rhabditophora. The expression of a piwi-like gene not only in gonadal, but also in adult somatic stem cells is another unique feature among bilaterians. These two independent stem-cell-related characters put the Acoela into the Platyhelminthes-Lophotrochozoa clade and account for the most parsimonious evolutionary explanation of epidermal cell renewal in the Bilateria. Most available multigene analyses produce conflicting results regarding the position of the acoels in the tree of life. Given these phylogenomic conflicts and the contradiction of developmental and morphological data with phylogenomic results, the monophyly of the phylum Platyhelminthes and the position of the Acoela remain unresolved. By these data, both the inclusion of Acoela within Platyhelminthes, and their separation from flatworms as basal bilaterians are well-supported alternatives.

Highlights

IntroductionFlatworms (phylum Platyhelminthes) have long been considered the most basal bilaterians, and they have served as models for the bilaterian ancestor in a variety of phylogenetic hypotheses
Flatworms have long been considered the most basal bilaterians, and they have served as models for the bilaterian ancestor in a variety of phylogenetic hypotheses
Morphological data place the Acoela within the Platyhelminthes based on a combination of weak characters: an acoelomate body structure, a densely multiciliated monolayered epidermis leading to a common habitus, a frontal organ, neoblasts, hermaphroditic reproduction with similar reproductive-organ morphology, biflagellate sperms with inverted axonemes, and lack of hindgut and anus [1,2,3]

Summary

Introduction

Flatworms (phylum Platyhelminthes) have long been considered the most basal bilaterians, and they have served as models for the bilaterian ancestor in a variety of phylogenetic hypotheses. In molecular phylogenetic analyses the position of acoels remained unresolved as well: Acoels are placed well outside the Platyhelminthes as a sister group to the other bilaterians based on data from a single gene or a few loci only, such as 18S and 28S rDNA, Hox and ParaHox genes, myosin II, or microRNA [5,6,7,8,9,10,11]. Because morphological characters are incongruent with the various molecular phylogenetic hypotheses, the placement of Acoela remains controversial; previous attempts to subsume molecular and morphological data proved unsatisfactory (reviewed in [9])

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