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      Myogenesis in the basal bilaterian Symsagittifera roscoffensis (Acoela)

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      1 , , 2 , 1
      Frontiers in Zoology
      BioMed Central

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          Abstract

          Background

          In order to increase the weak database concerning the organogenesis of Acoela – a clade regarded by many as the earliest extant offshoot of Bilateria and thus of particular interest for studies concerning the evolution of animal bodyplans – we analyzed the development of the musculature of Symsagittifera roscoffensis using F-actin labelling, confocal laserscanning microscopy, and 3D reconstruction software.

          Results

          At 40% of development between egg deposition and hatching short subepidermal fibres form. Muscle fibre development in the anterior body half precedes myogenesis in the posterior half. At 42% of development a grid of outer circular and inner longitudinal muscles is present in the bodywall. New circular muscles either branch off from present fibres or form adjacent to existing ones. The number of circular muscles is higher than that of the longitudinal muscles throughout all life cycle stages. Diagonal, circular and longitudinal muscles are initially rare but their number increases with time. The ventral side bears U-shaped muscles around the mouth, which in addition is surrounded by a sphincter muscle. With the exception of the region of the statocyst, dorsoventral muscles are present along the entire body of juveniles and adults, while adults additionally exhibit radially oriented internal muscles in the anterior tip. Outer diagonal muscles are present at the dorsal anterior tip of the adult. In adult animals, the male gonopore with its associated sexual organs expresses distinct muscles. No specific statocyst muscles were found. The muscle mantles of the needle-shaped sagittocysts are situated along the lateral edges of the animal and in the posterior end close to the male gonopore. In both juveniles and adults, non-muscular filaments, which stain positively for F-actin, are associated with certain sensory cells outside the bodywall musculature.

          Conclusion

          Compared to the myoanatomy of other acoel taxa, Symsagittifera roscoffensis shows a very complex musculature. Although data on presumably basal acoel clades are still scarce, the information currently available suggests an elaborated musculature with longitudinal, circular and U-shaped muscles as being part of the ancestral acoel bodyplan, thus increasing the possibility that Urbilateria likewise had a relatively complicated muscular ground pattern.

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          Most cited references53

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          Acoel flatworms: earliest extant bilaterian Metazoans, not members of Platyhelminthes.

          Because of their simple organization the Acoela have been considered to be either primitive bilaterians or descendants of coelomates through secondary loss of derived features. Sequence data of 18S ribosomal DNA genes from non-fast evolving species of acoels and other metazoans reveal that this group does not belong to the Platyhelminthes but represents the extant members of the earliest divergent Bilateria, an interpretation that is supported by recent studies on the embryonic cleavage pattern and nervous system of acoels. This study has implications for understanding the evolution of major body plans, and for perceptions of the Cambrian evolutionary explosion.
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            A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertodermatida are basal bilaterians.

            Bilateria are currently subdivided into three superclades: Deuterostomia, Ecdysozoa, and Lophotrochozoa. Within this new taxonomic frame, acoelomate Platyhelminthes, for a long time held to be basal bilaterians, are now considered spiralian lophotrochozoans. However, recent 18S rDNA [small subunit (SSU)] analyses have shown Platyhelminthes to be polyphyletic with two of its orders, the Acoela and the Nemertodermatida, as the earliest extant bilaterians. To corroborate such position and avoid the criticisms of saturation and long-branch effects thrown on the SSU molecule, we have searched for independent molecular data bearing good phylogenetic information at deep evolutionary nodes. Here we report a phylogenetic analysis of DNA sequences from the myosin heavy chain type II (myosin II) gene from a large set of metazoans, including acoels and nemertodermatids. Our study demonstrates, both for the myosin II data set alone and for a combined SSU + myosin II data set, that Platyhelminthes are polyphyletic and that acoels and nemertodermatids are the extant earliest bilaterians. Hence, the common bilaterian ancestor was not, as currently held, large and complex but small, simple, and likely with direct development. This scenario has far-reaching implications for understanding the evolution of major body plans and for perceptions of the Cambrian evolutionary explosion.
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              Are the Platyhelminthes a monophyletic primitive group? An assessment using 18S rDNA sequences.

              In most zoological textbooks, Platyhelminthes are depicted as an early-emerging clade forming the likely sister group of all the other Bilateria. Other phylogenetic proposals see them either as the sister group of most of the Protostomia or as a group derived from protostome coelomate ancestors by progenesis. The main difficulty in their correct phylogenetic placing is the lack of convincing synapomorphies for all Platyhelminthes, which may indicate that they are polyphyletic. Moreover, their internal phylogenetic relationships are still uncertain. To test these hypotheses, new complete 18S rDNA sequences from 13 species of "Turbellaria" have been obtained and compared to published sequences of 2 other "Turbellaria," 3 species of parasitic Platyhelminthes, and several diploblastic and deuterostome and protostome triploblastics. Maximum-parsimony, maximum-likelihood, and neighbor-joining methods were used to infer their phylogeny. The results show the order Catenulida to form an independent early-branching clade and emerge as a potential sister group of the rest of the Bilateria, while the rest of Platyhelminthes (Rhabditophora), which includes the parasites, form a clear monophyletic group closely related to the protostomes. The order Acoela, morphologically considered as candidates to be ancestral, are shown to be fast-clock organisms for the 18S rDNA gene. Hence, long-branching of acoels and insufficient sampling of catenulids and acoels leave their position still unresolved and call for further studies. Within the Rhabditophora, our analyses suggest (1) a close relationship between orders Macrostomida and Polycladida, forming a clear sister group to the rest of orders; (2) that parasitic platyhelminthes appeared early in the evolution of the group and form a sister group to a still-unresolved clade made by Nemertodermatida, Lecithoepitheliata, Prolecithophora, Proseriata, Tricladida, and Rhabdocoela; and (3) that Seriata is paraphyletic.
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                Author and article information

                Journal
                Front Zool
                Frontiers in Zoology
                BioMed Central
                1742-9994
                2008
                19 September 2008
                : 5
                : 14
                Affiliations
                [1 ]University of Copenhagen, Department of Biology, Research Group for Comparative Zoology, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark
                [2 ]Station Station Biologique de Roscoff, Place Georges Teissier BP74, F-29682 Roscoff Cedex, France
                Article
                1742-9994-5-14
                10.1186/1742-9994-5-14
                2562460
                18803837
                a0a91b56-043e-4a01-b330-50e5690d4f83
                Copyright © 2008 Semmler et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 5 May 2008
                : 19 September 2008
                Categories
                Research

                Animal science & Zoology
                Animal science & Zoology

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