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The cephalopod arm crown: appendage formation and differentiation in the Hawaiian bobtail squid Euprymna scolopes

BACKGROUND: Cephalopods are a highly derived class of molluscs that adapted their body plan to a more active and predatory lifestyle. One intriguing adaptation is the modification of the ventral foot to form a bilaterally symmetric arm crown, which constitutes a true morphological novelty in evoluti...

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Autores principales: Nödl, Marie-Therese, Kerbl, Alexandra, Walzl, Manfred G., Müller, Gerd B., de Couet, Heinz Gert
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5041568/
https://www.ncbi.nlm.nih.gov/pubmed/27708680
http://dx.doi.org/10.1186/s12983-016-0175-8
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author Nödl, Marie-Therese
Kerbl, Alexandra
Walzl, Manfred G.
Müller, Gerd B.
de Couet, Heinz Gert
author_facet Nödl, Marie-Therese
Kerbl, Alexandra
Walzl, Manfred G.
Müller, Gerd B.
de Couet, Heinz Gert
author_sort Nödl, Marie-Therese
collection PubMed
description BACKGROUND: Cephalopods are a highly derived class of molluscs that adapted their body plan to a more active and predatory lifestyle. One intriguing adaptation is the modification of the ventral foot to form a bilaterally symmetric arm crown, which constitutes a true morphological novelty in evolution. In addition, this structure shows many diversifications within the class of cephalopods and therefore offers an interesting opportunity to study the molecular underpinnings of the emergence of phenotypic novelties and their diversification. Here we use the sepiolid Euprymna scolopes as a model to study the formation and differentiation of the decabrachian arm crown, which consists of four pairs of sessile arms and one pair of retractile tentacles. We provide a detailed description of arm crown formation in order to understand the basic morphology and the developmental dynamics of this structure. RESULTS: We show that the morphological formation of the cephalopod appendages occurs during distinct phases, including outgrowth, elongation, and tissue differentiation. Early outgrowth is characterized by uniform cell proliferation, while the elongation of the appendages initiates tissue differentiation. The latter progresses in a gradient from proximal to distal, whereas cell proliferation becomes restricted to the distal-most end of the arm. Differences in the formation of arms and tentacles exist, with the tentacles showing an expedite growth rate and higher complexity at younger stages. CONCLUSION: The early outgrowth and differentiation of the E. scolopes arm crown shows similarities to the related, yet derived cephalopod Octopus vulgaris. Parallels in the growth and differentiation of appendages seem to exist throughout the animal kingdom, raising the question of whether these similarities reflect a recruitment of similar molecular patterning pathways. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-016-0175-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-50415682016-10-05 The cephalopod arm crown: appendage formation and differentiation in the Hawaiian bobtail squid Euprymna scolopes Nödl, Marie-Therese Kerbl, Alexandra Walzl, Manfred G. Müller, Gerd B. de Couet, Heinz Gert Front Zool Research BACKGROUND: Cephalopods are a highly derived class of molluscs that adapted their body plan to a more active and predatory lifestyle. One intriguing adaptation is the modification of the ventral foot to form a bilaterally symmetric arm crown, which constitutes a true morphological novelty in evolution. In addition, this structure shows many diversifications within the class of cephalopods and therefore offers an interesting opportunity to study the molecular underpinnings of the emergence of phenotypic novelties and their diversification. Here we use the sepiolid Euprymna scolopes as a model to study the formation and differentiation of the decabrachian arm crown, which consists of four pairs of sessile arms and one pair of retractile tentacles. We provide a detailed description of arm crown formation in order to understand the basic morphology and the developmental dynamics of this structure. RESULTS: We show that the morphological formation of the cephalopod appendages occurs during distinct phases, including outgrowth, elongation, and tissue differentiation. Early outgrowth is characterized by uniform cell proliferation, while the elongation of the appendages initiates tissue differentiation. The latter progresses in a gradient from proximal to distal, whereas cell proliferation becomes restricted to the distal-most end of the arm. Differences in the formation of arms and tentacles exist, with the tentacles showing an expedite growth rate and higher complexity at younger stages. CONCLUSION: The early outgrowth and differentiation of the E. scolopes arm crown shows similarities to the related, yet derived cephalopod Octopus vulgaris. Parallels in the growth and differentiation of appendages seem to exist throughout the animal kingdom, raising the question of whether these similarities reflect a recruitment of similar molecular patterning pathways. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-016-0175-8) contains supplementary material, which is available to authorized users. BioMed Central 2016-09-29 /pmc/articles/PMC5041568/ /pubmed/27708680 http://dx.doi.org/10.1186/s12983-016-0175-8 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
Nödl, Marie-Therese
Kerbl, Alexandra
Walzl, Manfred G.
Müller, Gerd B.
de Couet, Heinz Gert
The cephalopod arm crown: appendage formation and differentiation in the Hawaiian bobtail squid Euprymna scolopes
title The cephalopod arm crown: appendage formation and differentiation in the Hawaiian bobtail squid Euprymna scolopes
title_full The cephalopod arm crown: appendage formation and differentiation in the Hawaiian bobtail squid Euprymna scolopes
title_fullStr The cephalopod arm crown: appendage formation and differentiation in the Hawaiian bobtail squid Euprymna scolopes
title_full_unstemmed The cephalopod arm crown: appendage formation and differentiation in the Hawaiian bobtail squid Euprymna scolopes
title_short The cephalopod arm crown: appendage formation and differentiation in the Hawaiian bobtail squid Euprymna scolopes
title_sort cephalopod arm crown: appendage formation and differentiation in the hawaiian bobtail squid euprymna scolopes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5041568/
https://www.ncbi.nlm.nih.gov/pubmed/27708680
http://dx.doi.org/10.1186/s12983-016-0175-8
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