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

Institute of Zoology and Center for Molecular Biosciences, University of Innsbruck, Innsbruck, Austria.
PLoS ONE (Impact Factor: 3.23). 02/2009; 4(5):e5502. DOI: 10.1371/journal.pone.0005502
Source: PubMed


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.

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    • "Altogether, acoelomorphs and xenoturbellids are rather simply organized animals, and this is also the reason why their phylogenetic position has been of great interest and is still under debate (Fig. 9.1 ). After the exclusion of Acoelomorpha from the Platyhelminthes (Carranza et al. 1997 ; Ruiz-Trillo et al. 1999 , 2002 ; Jondelius et al. 2002 ; Wallberg et al. 2007 ; Egger et al. 2009 ; Paps et al. 2009 ), molecular phylogenies have produced ambiguous results concerning their defi nite placement within the tree of life. Phylogenomic studies that include Xenoturbella place Acoelomorpha together with Xenoturbella (Xenacoelomorpha) either as sister to all remaining Bilateria (Hejnol et al. 2009 ; Srivastava et al. 2014 ) or as sister to Ambulacraria – i.e., within the deuterostomes (Philippe et al. 2011 ). "
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    ABSTRACT: Acoelomorpha, comprising Acoela and Nemertodermatida, and Xenoturbellida (with one single hitherto described species, Xenoturbella bocki) are simple, aquatic, acoelomate worms that measure between 100 μm and 1 cm. Acoelomorpha and Xenoturbella are found to cluster together as the monophyletic Xenacoelomorpha in some recent molecular phylogenetic analyses. With only few exceptions, all species are marine, with most of them living in the interstitial environment. Xenoturbellids and acoelomorphs possess a simple nervous system that generally is a basiepidermal nerve net; however, in some cases this net is condensed into basiepidermal neurite bundles at different parts of the body or is submerged under the epidermis where condensed brains and submuscular cords are formed. Some Acoela possess eye spots, while most nemertodermatids, Xenoturbella, and Acoela lack eyes. Recent internal phylogenetic analyses suggest that eyes were absent from the ground pattern of Acoelomorpha. A prominent gravitational sensory organ, the statocyst, is present in all xenacoelomorph taxa, albeit with differing ultrastructure.
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    • "Acoels are predominantly marine worms with a contested phylogenetic position. For more than a century, acoels were considered members of the Platyhelminthes based on many morphological similarities (Ehlers, 1985), but a great number of molecular analyses now place them either as sister group of the Bilateria (Ruiz-Trillo et al., 1999, Egger et al., 2009) or, most recently, as deuterostomes (Philippe et al., 2011). Identification of acoels requires careful observation and in many cases sagittal sections of the genital organs of mature animals are required for identification (Westblad, 1948). "
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    ABSTRACT: Aphanostoma pisae sp. nov. is an interstitial acoel found at the coast of the Liguric Sea in Pisa (Tuscany, Italy). It belongs to the large family Isodiametridae, characterised by a male copulatory organ with a cylindrical shape and non-anastomising longitudinal muscle fibers. It is the first recognised species of Aphanostoma in the Mediterranean and it can occur in great abundance at its type locality (several hundred specimens in a spoonful of sand). A. pisae has been cultured in the laboratory for several years with diatoms for food. The embryonic development lasts for just under two days at 20 °C. We provide a description of the new species using live observations, light and electron microscopy of sagittal sections and stainings of the filamentous actin and the serotonergic nervous system, and we discuss and update the genus diagnoses of the genera Aphanostoma and Praeconvoluta.
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    • "In both phyla, adult stem cells located in the parenchyma, known as neoblasts, are the only mitotically active somatic cells. Their presence and importance in development, regeneration and homeostasis is recognised in the acoel families Convolutidae [4-7] and Isodiametridae [3,4]; in the latter, it has been shown that irratiated animals, which have had all their neoblasts eliminated, die soon after the treatment [3,8]. "
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    ABSTRACT: Regeneration is a widespread phenomenon in the animal kingdom, but the capacity to restore damaged or missing tissue varies greatly between different phyla and even within the same phylum. However, the distantly related Acoelomorpha and Platyhelminthes share a strikingly similar stem-cell system and regenerative capacity. Therefore, comparing the underlying mechanisms in these two phyla paves the way for an increased understanding of the evolution of this developmental process.To date, Isodiametra pulchra is the most promising candidate as a model for the Acoelomorpha, as it reproduces steadily under laboratory conditions and is amenable to various techniques, including the silencing of gene expression by RNAi. In order to provide an essential framework for future studies, we report the succession of regeneration events via the use of cytochemical, histological and microscopy techniques, and specify the total number of cells in adult individuals. Isodiametra pulchra is not capable of regenerating a new head, but completely restores all posterior structures within 10 days. Following amputation, the wound closes via the contraction of local muscle fibres and an extension of the dorsal epidermis. Subsequently, stem cells invade the wound area and form a loosely delimited blastema. After two days, the posterior end is re-patterned with the male (and occasionally the female) genital primordium being apparent. Successively, these primordia differentiate into complete copulatory organs. The size of the body and also of the male and female copulatory organs, as well as the distance between the copulatory organs, progressively increase and by nine days copulation is possible. Adult individuals with an average length of 670 mum consist of approximately 8100 cells. Isodiametra pulchra regenerates through a combination of morphallactic and epimorphic processes. Existing structures are "re-modelled" and provide a framework onto which newly differentiating cells are added. Growth proceeds through the intercalary addition of structures, mirroring the embryonic and post-embryonic development of various organ systems. The suitability of Isodiametra pulchra for laboratory techniques, the fact that its transcriptome and genome data will soon be available, as well as its small size and low number of cells, make it a prime candidate subject for research into the cellular mechanisms that underlie regeneration in acoelomorphs.
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