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Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles

BACKGROUND: Simple life cycles arise from complex life cycles when one or more developmental stages are lost. This raises a fundamental question - how can an intermediate stage, such as a larva, be removed, and development still produce a normal adult? To address this question, we examined the devel...

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Autores principales: Helm, Rebecca R, Tiozzo, Stefano, Lilley, Martin K S, Lombard, Fabien, Dunn, Casey W
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4415277/
https://www.ncbi.nlm.nih.gov/pubmed/25932322
http://dx.doi.org/10.1186/s13227-015-0005-7
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author Helm, Rebecca R
Tiozzo, Stefano
Lilley, Martin K S
Lombard, Fabien
Dunn, Casey W
author_facet Helm, Rebecca R
Tiozzo, Stefano
Lilley, Martin K S
Lombard, Fabien
Dunn, Casey W
author_sort Helm, Rebecca R
collection PubMed
description BACKGROUND: Simple life cycles arise from complex life cycles when one or more developmental stages are lost. This raises a fundamental question - how can an intermediate stage, such as a larva, be removed, and development still produce a normal adult? To address this question, we examined the development in several species of pelagiid jellyfish. Most members of Pelagiidae have a complex life cycle with a sessile polyp that gives rise to ephyrae (juvenile medusae); but one species within Pelagiidae, Pelagia noctiluca, spends its whole life in the water column, developing from a larva directly into an ephyra. In many complex life cycles, adult features develop from cell populations that remain quiescent in larvae, and this is known as life cycle compartmentalization and may facilitate the evolution of direct life cycles. A second type of metamorphic processes, known as remodeling, occurs when adult features are formed through modification of already differentiated larval structures. We examined muscle morphology to determine which of these alternatives may be present in Pelagiidae. RESULTS: We first examined the structure and development of polyp and ephyra musculature in Chrysaora quinquecirrha, a close relative of P. noctiluca with a complex life cycle. Using phallotoxin staining and confocal microscopy, we verified that polyps have four to six cord muscles that persist in strobilae and discovered that cord muscles is physically separated from ephyra muscle. When cord muscle is removed from ephyra segments, normal ephyra muscle still develops. This suggests that polyp cord muscle is not necessary for ephyra muscle formation. We also found no evidence of polyp-like muscle in P. noctiluca. In both species, we discovered that ephyra muscle arises de novo in a similar manner, regardless of the life cycle. CONCLUSIONS: The separate origins of polyp and ephyra muscle in C. quinquecirrha and the absence of polyp-like muscle in P. noctiluca suggest that polyp muscle is not remodeled to form ephyra muscle in Pelagiidae. Life cycle stages in Scyphozoa may instead be compartmentalized. Because polyp muscle is not directly remodeled, this may have facilitated the loss of the polyp stage in the evolution of P. noctiluca. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13227-015-0005-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-44152772015-05-01 Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles Helm, Rebecca R Tiozzo, Stefano Lilley, Martin K S Lombard, Fabien Dunn, Casey W EvoDevo Research BACKGROUND: Simple life cycles arise from complex life cycles when one or more developmental stages are lost. This raises a fundamental question - how can an intermediate stage, such as a larva, be removed, and development still produce a normal adult? To address this question, we examined the development in several species of pelagiid jellyfish. Most members of Pelagiidae have a complex life cycle with a sessile polyp that gives rise to ephyrae (juvenile medusae); but one species within Pelagiidae, Pelagia noctiluca, spends its whole life in the water column, developing from a larva directly into an ephyra. In many complex life cycles, adult features develop from cell populations that remain quiescent in larvae, and this is known as life cycle compartmentalization and may facilitate the evolution of direct life cycles. A second type of metamorphic processes, known as remodeling, occurs when adult features are formed through modification of already differentiated larval structures. We examined muscle morphology to determine which of these alternatives may be present in Pelagiidae. RESULTS: We first examined the structure and development of polyp and ephyra musculature in Chrysaora quinquecirrha, a close relative of P. noctiluca with a complex life cycle. Using phallotoxin staining and confocal microscopy, we verified that polyps have four to six cord muscles that persist in strobilae and discovered that cord muscles is physically separated from ephyra muscle. When cord muscle is removed from ephyra segments, normal ephyra muscle still develops. This suggests that polyp cord muscle is not necessary for ephyra muscle formation. We also found no evidence of polyp-like muscle in P. noctiluca. In both species, we discovered that ephyra muscle arises de novo in a similar manner, regardless of the life cycle. CONCLUSIONS: The separate origins of polyp and ephyra muscle in C. quinquecirrha and the absence of polyp-like muscle in P. noctiluca suggest that polyp muscle is not remodeled to form ephyra muscle in Pelagiidae. Life cycle stages in Scyphozoa may instead be compartmentalized. Because polyp muscle is not directly remodeled, this may have facilitated the loss of the polyp stage in the evolution of P. noctiluca. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13227-015-0005-7) contains supplementary material, which is available to authorized users. BioMed Central 2015-04-17 /pmc/articles/PMC4415277/ /pubmed/25932322 http://dx.doi.org/10.1186/s13227-015-0005-7 Text en © Helm et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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
Helm, Rebecca R
Tiozzo, Stefano
Lilley, Martin K S
Lombard, Fabien
Dunn, Casey W
Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles
title Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles
title_full Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles
title_fullStr Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles
title_full_unstemmed Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles
title_short Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles
title_sort comparative muscle development of scyphozoan jellyfish with simple and complex life cycles
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4415277/
https://www.ncbi.nlm.nih.gov/pubmed/25932322
http://dx.doi.org/10.1186/s13227-015-0005-7
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