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The nervous system of the lophophore in the ctenostome Amathia gracilis provides insight into the morphology of ancestral ectoprocts and the monophyly of the lophophorates

BACKGROUND: The Bryozoa (=Ectoprocta) is a large group of bilaterians that exhibit great variability in the innervation of tentacles and in the organization of the cerebral ganglion. Investigations of bryozoans from different groups may contribute to the reconstruction of the bryozoan nervous system...

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Autores principales: Temereva, Elena N., Kosevich, Igor A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5012098/
https://www.ncbi.nlm.nih.gov/pubmed/27600336
http://dx.doi.org/10.1186/s12862-016-0744-7
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author Temereva, Elena N.
Kosevich, Igor A.
author_facet Temereva, Elena N.
Kosevich, Igor A.
author_sort Temereva, Elena N.
collection PubMed
description BACKGROUND: The Bryozoa (=Ectoprocta) is a large group of bilaterians that exhibit great variability in the innervation of tentacles and in the organization of the cerebral ganglion. Investigations of bryozoans from different groups may contribute to the reconstruction of the bryozoan nervous system bauplan. A detailed investigation of the polypide nervous system of the ctenostome bryozoan Amathia gracilis is reported here. RESULTS: The cerebral ganglion displays prominent zonality and has at least three zones: proximal, central, and distal. The proximal zone is the most developed and contains two large perikarya giving rise to the tentacle sheath nerves. The neuroepithelial organization of the cerebral ganglion is revealed. The tiny lumen of the cerebral ganglion is represented by narrow spaces between the apical projections of the perikarya of the central zone. The cerebral ganglion gives rise to five groups of main neurite bundles of the lophophore and the tentacle sheath: the circum-oral nerve ring, the lophophoral dorso-lateral nerves, the pharyngeal and visceral neurite bundles, the outer nerve ring, and the tentacle sheath nerves. Serotonin-like immunoreactive nerve system of polypide includes eight large perikarya located between tentacles bases. There are two analmost and six oralmost perikarya with prominent serotonergic “gap” between them. Based on the characteristics of their innervations, the tentacles can be subdivided into two groups: four that are near the anus and six that are near the mouth. Two longitudinal neurite bundles - medio-frontal and abfrontal - extend along each tentacle. CONCLUSION: The zonality of the cerebral ganglion, the presence of three commissures, and location of the main nerves emanating from each zone might have caused by directive innervation of the various parts of the body: the tentacles sheath, the lophohpore, and the digestive tract. Two alternative scenarios of bryozoan lophophore evolution are discussed. The arrangement of large serotonin-like immunoreactive perikarya differs from the pattern previously described in ctenostome bryozoans. In accordance with its position relative to the same organs (tentacles, anus, and mouth), the lophophore outer nerve ring corresponds to the brachiopod lower brachial nerve and to the phoronid tentacular nerve ring. The presence of the outer nerve ring makes the lophophore innervation within the group (clade) of lophophorates similar and provides additional morphological evidence of the lophophore homology and monophyly of the lophophorates. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0744-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-50120982016-09-07 The nervous system of the lophophore in the ctenostome Amathia gracilis provides insight into the morphology of ancestral ectoprocts and the monophyly of the lophophorates Temereva, Elena N. Kosevich, Igor A. BMC Evol Biol Research Article BACKGROUND: The Bryozoa (=Ectoprocta) is a large group of bilaterians that exhibit great variability in the innervation of tentacles and in the organization of the cerebral ganglion. Investigations of bryozoans from different groups may contribute to the reconstruction of the bryozoan nervous system bauplan. A detailed investigation of the polypide nervous system of the ctenostome bryozoan Amathia gracilis is reported here. RESULTS: The cerebral ganglion displays prominent zonality and has at least three zones: proximal, central, and distal. The proximal zone is the most developed and contains two large perikarya giving rise to the tentacle sheath nerves. The neuroepithelial organization of the cerebral ganglion is revealed. The tiny lumen of the cerebral ganglion is represented by narrow spaces between the apical projections of the perikarya of the central zone. The cerebral ganglion gives rise to five groups of main neurite bundles of the lophophore and the tentacle sheath: the circum-oral nerve ring, the lophophoral dorso-lateral nerves, the pharyngeal and visceral neurite bundles, the outer nerve ring, and the tentacle sheath nerves. Serotonin-like immunoreactive nerve system of polypide includes eight large perikarya located between tentacles bases. There are two analmost and six oralmost perikarya with prominent serotonergic “gap” between them. Based on the characteristics of their innervations, the tentacles can be subdivided into two groups: four that are near the anus and six that are near the mouth. Two longitudinal neurite bundles - medio-frontal and abfrontal - extend along each tentacle. CONCLUSION: The zonality of the cerebral ganglion, the presence of three commissures, and location of the main nerves emanating from each zone might have caused by directive innervation of the various parts of the body: the tentacles sheath, the lophohpore, and the digestive tract. Two alternative scenarios of bryozoan lophophore evolution are discussed. The arrangement of large serotonin-like immunoreactive perikarya differs from the pattern previously described in ctenostome bryozoans. In accordance with its position relative to the same organs (tentacles, anus, and mouth), the lophophore outer nerve ring corresponds to the brachiopod lower brachial nerve and to the phoronid tentacular nerve ring. The presence of the outer nerve ring makes the lophophore innervation within the group (clade) of lophophorates similar and provides additional morphological evidence of the lophophore homology and monophyly of the lophophorates. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0744-7) contains supplementary material, which is available to authorized users. BioMed Central 2016-09-06 /pmc/articles/PMC5012098/ /pubmed/27600336 http://dx.doi.org/10.1186/s12862-016-0744-7 Text en © The Author(s). 2016 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
Temereva, Elena N.
Kosevich, Igor A.
The nervous system of the lophophore in the ctenostome Amathia gracilis provides insight into the morphology of ancestral ectoprocts and the monophyly of the lophophorates
title The nervous system of the lophophore in the ctenostome Amathia gracilis provides insight into the morphology of ancestral ectoprocts and the monophyly of the lophophorates
title_full The nervous system of the lophophore in the ctenostome Amathia gracilis provides insight into the morphology of ancestral ectoprocts and the monophyly of the lophophorates
title_fullStr The nervous system of the lophophore in the ctenostome Amathia gracilis provides insight into the morphology of ancestral ectoprocts and the monophyly of the lophophorates
title_full_unstemmed The nervous system of the lophophore in the ctenostome Amathia gracilis provides insight into the morphology of ancestral ectoprocts and the monophyly of the lophophorates
title_short The nervous system of the lophophore in the ctenostome Amathia gracilis provides insight into the morphology of ancestral ectoprocts and the monophyly of the lophophorates
title_sort nervous system of the lophophore in the ctenostome amathia gracilis provides insight into the morphology of ancestral ectoprocts and the monophyly of the lophophorates
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5012098/
https://www.ncbi.nlm.nih.gov/pubmed/27600336
http://dx.doi.org/10.1186/s12862-016-0744-7
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