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From complex to simple: myogenesis in an aplacophoran mollusk reveals key traits in aculiferan evolution
BACKGROUND: Recent studies suggest a bifurcation at the base of Mollusca, resulting in the primarily single-shelled Conchifera (Bivalvia, Gastropoda, Scaphopoda, Monoplacophora, Cephalopoda) and the spicule-bearing Aculifera (Polyplacophora, Neomeniomorpha, Chaetodermomorpha). A recent study reveale...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4575435/ https://www.ncbi.nlm.nih.gov/pubmed/26385077 http://dx.doi.org/10.1186/s12862-015-0467-1 |
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author | Scherholz, Maik Redl, Emanuel Wollesen, Tim Todt, Christiane Wanninger, Andreas |
author_facet | Scherholz, Maik Redl, Emanuel Wollesen, Tim Todt, Christiane Wanninger, Andreas |
author_sort | Scherholz, Maik |
collection | PubMed |
description | BACKGROUND: Recent studies suggest a bifurcation at the base of Mollusca, resulting in the primarily single-shelled Conchifera (Bivalvia, Gastropoda, Scaphopoda, Monoplacophora, Cephalopoda) and the spicule-bearing Aculifera (Polyplacophora, Neomeniomorpha, Chaetodermomorpha). A recent study revealed a complex larval musculature exclusively shared by Neomeniomorpha and Polyplacophora, supporting a close relationship of both taxa. However, the ontogenetic transition from the complex larval to the simple adult neomeniomorph musculature, which mainly consists of a three-layered body-wall musculature and serially iterated dorsoventral muscles, remains unknown. To close this gap in knowledge, we studied remodeling of the larval musculature during metamorphosis in the neomeniomorph Wirenia argentea. A comparative analysis with a novel data set of a polyplacophoran, Leptochiton asellus, allows us to infer the morphology of the last common ancestor of Aculifera and the evolution of its subclades therefrom. RESULTS: The complex larval musculature of Wirenia argentea persists through metamorphosis and becomes modified to form two of the three muscle layers of the adult body wall. The innermost longitudinal layer of the three-layered body wall musculature is generated by transformation and expansion of distinct larval longitudinal muscle bundles. The larval ventrolateral muscle strands are remodeled and eventually become the most ventral part of the adult longitudinal layer of the body wall musculature. The paired larval enrolling muscle forms the lateral parts and the former rectus muscle is destined to become the most dorsal part of the longitudinal layer of the body wall musculature. The transient ventromedian muscle is lost during postmetamorphic development. CONCLUSIONS: Postmetamorphic remodeling in W. argentea supports the hypothesis of a complex myoanatomy rather than a three-layered body wall musculature at the base of Aculifera, and thus argues against homology of the body wall musculature of adult Neomeniomorpha and other potential molluscan sister groups. Our data show that the neomeniomorph body wall musculature is a derived condition and not an aculiferan or molluscan plesiomorphy. |
format | Online Article Text |
id | pubmed-4575435 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-45754352015-09-20 From complex to simple: myogenesis in an aplacophoran mollusk reveals key traits in aculiferan evolution Scherholz, Maik Redl, Emanuel Wollesen, Tim Todt, Christiane Wanninger, Andreas BMC Evol Biol Research Article BACKGROUND: Recent studies suggest a bifurcation at the base of Mollusca, resulting in the primarily single-shelled Conchifera (Bivalvia, Gastropoda, Scaphopoda, Monoplacophora, Cephalopoda) and the spicule-bearing Aculifera (Polyplacophora, Neomeniomorpha, Chaetodermomorpha). A recent study revealed a complex larval musculature exclusively shared by Neomeniomorpha and Polyplacophora, supporting a close relationship of both taxa. However, the ontogenetic transition from the complex larval to the simple adult neomeniomorph musculature, which mainly consists of a three-layered body-wall musculature and serially iterated dorsoventral muscles, remains unknown. To close this gap in knowledge, we studied remodeling of the larval musculature during metamorphosis in the neomeniomorph Wirenia argentea. A comparative analysis with a novel data set of a polyplacophoran, Leptochiton asellus, allows us to infer the morphology of the last common ancestor of Aculifera and the evolution of its subclades therefrom. RESULTS: The complex larval musculature of Wirenia argentea persists through metamorphosis and becomes modified to form two of the three muscle layers of the adult body wall. The innermost longitudinal layer of the three-layered body wall musculature is generated by transformation and expansion of distinct larval longitudinal muscle bundles. The larval ventrolateral muscle strands are remodeled and eventually become the most ventral part of the adult longitudinal layer of the body wall musculature. The paired larval enrolling muscle forms the lateral parts and the former rectus muscle is destined to become the most dorsal part of the longitudinal layer of the body wall musculature. The transient ventromedian muscle is lost during postmetamorphic development. CONCLUSIONS: Postmetamorphic remodeling in W. argentea supports the hypothesis of a complex myoanatomy rather than a three-layered body wall musculature at the base of Aculifera, and thus argues against homology of the body wall musculature of adult Neomeniomorpha and other potential molluscan sister groups. Our data show that the neomeniomorph body wall musculature is a derived condition and not an aculiferan or molluscan plesiomorphy. BioMed Central 2015-09-18 /pmc/articles/PMC4575435/ /pubmed/26385077 http://dx.doi.org/10.1186/s12862-015-0467-1 Text en © Scherholz et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Scherholz, Maik Redl, Emanuel Wollesen, Tim Todt, Christiane Wanninger, Andreas From complex to simple: myogenesis in an aplacophoran mollusk reveals key traits in aculiferan evolution |
title | From complex to simple: myogenesis in an aplacophoran mollusk reveals key traits in aculiferan evolution |
title_full | From complex to simple: myogenesis in an aplacophoran mollusk reveals key traits in aculiferan evolution |
title_fullStr | From complex to simple: myogenesis in an aplacophoran mollusk reveals key traits in aculiferan evolution |
title_full_unstemmed | From complex to simple: myogenesis in an aplacophoran mollusk reveals key traits in aculiferan evolution |
title_short | From complex to simple: myogenesis in an aplacophoran mollusk reveals key traits in aculiferan evolution |
title_sort | from complex to simple: myogenesis in an aplacophoran mollusk reveals key traits in aculiferan evolution |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4575435/ https://www.ncbi.nlm.nih.gov/pubmed/26385077 http://dx.doi.org/10.1186/s12862-015-0467-1 |
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