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The anatomy and development of the nervous system in Magelonidae (Annelida) – insights into the evolution of the annelid brain

BACKGROUND: The annelid anterior central nervous system is often described to consist of a dorsal prostomial brain, consisting of several commissures and connected to the ventral ganglionic nerve cord via circumesophageal connectives. In the light of current molecular phylogenies, our assumptions on...

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Autores principales: Beckers, Patrick, Helm, Conrad, Bartolomaeus, Thomas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6714456/
https://www.ncbi.nlm.nih.gov/pubmed/31462293
http://dx.doi.org/10.1186/s12862-019-1498-9
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author Beckers, Patrick
Helm, Conrad
Bartolomaeus, Thomas
author_facet Beckers, Patrick
Helm, Conrad
Bartolomaeus, Thomas
author_sort Beckers, Patrick
collection PubMed
description BACKGROUND: The annelid anterior central nervous system is often described to consist of a dorsal prostomial brain, consisting of several commissures and connected to the ventral ganglionic nerve cord via circumesophageal connectives. In the light of current molecular phylogenies, our assumptions on the primary design of the nervous system in Annelida has to be reconsidered. For that purpose we provide a detailed investigation of the adult nervous system of Magelonidae – a putatively basally branching annelid family - and studied early stages of the development of the latter. RESULTS: Our comparative investigation using an integrative morphological approach shows that the nervous system of Magelonidae is located inside the epidermis. The brain is composed of an anterior compact neuropil and posteriorly encircles the prostomial coelomic cavities. From the brain two lateral medullary cords branch off which fuse caudally. Prominent brain structures such as nuchal organs, ganglia or mushroom bodies are absent and the entire nervous system is medullary. Our investigations also contradict previous investigations and present an updated view on established assumptions and descriptions. CONCLUSION: The comprehensive dataset presented herein enables a detailed investigation of the magelonid anterior central nervous system for the first time. The data reveal that early in annelid evolution complexity of brains and anterior sensory structures rises. Polymorphic neurons in clusters and distinct brain parts, as well as lateral organs - all of which are not present in outgroup taxa and in the putative magelonid sister group Oweniidae - already evolved in Magelonidae. Commissures inside the brain, ganglia and nuchal organs, however, most likely evolved in the stem lineage of Amphinomidae + Sipuncula and Pleistoannelida (Errantia+ Sedentaria). The investigation demonstrates the necessity to continuously question established descriptions and interpretations of earlier publications and the need for transparent datasets. Our results also hint towards a stronger inclusion of larval morphology and developmental investigations in order to understand adult morphological features, not only in Annelida. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-019-1498-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-67144562019-09-04 The anatomy and development of the nervous system in Magelonidae (Annelida) – insights into the evolution of the annelid brain Beckers, Patrick Helm, Conrad Bartolomaeus, Thomas BMC Evol Biol Research Article BACKGROUND: The annelid anterior central nervous system is often described to consist of a dorsal prostomial brain, consisting of several commissures and connected to the ventral ganglionic nerve cord via circumesophageal connectives. In the light of current molecular phylogenies, our assumptions on the primary design of the nervous system in Annelida has to be reconsidered. For that purpose we provide a detailed investigation of the adult nervous system of Magelonidae – a putatively basally branching annelid family - and studied early stages of the development of the latter. RESULTS: Our comparative investigation using an integrative morphological approach shows that the nervous system of Magelonidae is located inside the epidermis. The brain is composed of an anterior compact neuropil and posteriorly encircles the prostomial coelomic cavities. From the brain two lateral medullary cords branch off which fuse caudally. Prominent brain structures such as nuchal organs, ganglia or mushroom bodies are absent and the entire nervous system is medullary. Our investigations also contradict previous investigations and present an updated view on established assumptions and descriptions. CONCLUSION: The comprehensive dataset presented herein enables a detailed investigation of the magelonid anterior central nervous system for the first time. The data reveal that early in annelid evolution complexity of brains and anterior sensory structures rises. Polymorphic neurons in clusters and distinct brain parts, as well as lateral organs - all of which are not present in outgroup taxa and in the putative magelonid sister group Oweniidae - already evolved in Magelonidae. Commissures inside the brain, ganglia and nuchal organs, however, most likely evolved in the stem lineage of Amphinomidae + Sipuncula and Pleistoannelida (Errantia+ Sedentaria). The investigation demonstrates the necessity to continuously question established descriptions and interpretations of earlier publications and the need for transparent datasets. Our results also hint towards a stronger inclusion of larval morphology and developmental investigations in order to understand adult morphological features, not only in Annelida. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-019-1498-9) contains supplementary material, which is available to authorized users. BioMed Central 2019-08-28 /pmc/articles/PMC6714456/ /pubmed/31462293 http://dx.doi.org/10.1186/s12862-019-1498-9 Text en © The Author(s). 2019 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
Beckers, Patrick
Helm, Conrad
Bartolomaeus, Thomas
The anatomy and development of the nervous system in Magelonidae (Annelida) – insights into the evolution of the annelid brain
title The anatomy and development of the nervous system in Magelonidae (Annelida) – insights into the evolution of the annelid brain
title_full The anatomy and development of the nervous system in Magelonidae (Annelida) – insights into the evolution of the annelid brain
title_fullStr The anatomy and development of the nervous system in Magelonidae (Annelida) – insights into the evolution of the annelid brain
title_full_unstemmed The anatomy and development of the nervous system in Magelonidae (Annelida) – insights into the evolution of the annelid brain
title_short The anatomy and development of the nervous system in Magelonidae (Annelida) – insights into the evolution of the annelid brain
title_sort anatomy and development of the nervous system in magelonidae (annelida) – insights into the evolution of the annelid brain
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6714456/
https://www.ncbi.nlm.nih.gov/pubmed/31462293
http://dx.doi.org/10.1186/s12862-019-1498-9
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