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In silico evo-devo: reconstructing stages in the evolution of animal segmentation

BACKGROUND: The evolution of animal segmentation is a major research focus within the field of evolutionary–developmental biology. Most studied segmented animals generate their segments in a repetitive, anterior-to-posterior fashion coordinated with the extension of the body axis from a posterior gr...

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Autores principales: Vroomans, Renske M. A., Hogeweg, Paulien, ten Tusscher, Kirsten H. W. J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4968448/
https://www.ncbi.nlm.nih.gov/pubmed/27482374
http://dx.doi.org/10.1186/s13227-016-0052-8
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author Vroomans, Renske M. A.
Hogeweg, Paulien
ten Tusscher, Kirsten H. W. J.
author_facet Vroomans, Renske M. A.
Hogeweg, Paulien
ten Tusscher, Kirsten H. W. J.
author_sort Vroomans, Renske M. A.
collection PubMed
description BACKGROUND: The evolution of animal segmentation is a major research focus within the field of evolutionary–developmental biology. Most studied segmented animals generate their segments in a repetitive, anterior-to-posterior fashion coordinated with the extension of the body axis from a posterior growth zone. In the current study we ask which selection pressures and ordering of evolutionary events may have contributed to the evolution of this specific segmentation mode. RESULTS: To answer this question we extend a previous in silico simulation model of the evolution of segmentation by allowing the tissue growth pattern to freely evolve. We then determine the likelihood of evolving oscillatory sequential segmentation combined with posterior growth under various conditions, such as the presence or absence of a posterior morphogen gradient or selection for determinate growth. We find that posterior growth with sequential segmentation is the predominant outcome of our simulations only if a posterior morphogen gradient is assumed to have already evolved and selection for determinate growth occurs secondarily. Otherwise, an alternative segmentation mechanism dominates, in which divisions occur in large bursts through the entire tissue and all segments are created simultaneously. CONCLUSIONS: Our study suggests that the ancestry of a posterior signalling centre has played an important role in the evolution of sequential segmentation. In addition, it suggests that determinate growth evolved secondarily, after the evolution of posterior growth. More generally, we demonstrate the potential of evo-devo simulation models that allow us to vary conditions as well as the onset of selection pressures to infer a likely order of evolutionary innovations. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13227-016-0052-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-49684482016-08-02 In silico evo-devo: reconstructing stages in the evolution of animal segmentation Vroomans, Renske M. A. Hogeweg, Paulien ten Tusscher, Kirsten H. W. J. EvoDevo Research BACKGROUND: The evolution of animal segmentation is a major research focus within the field of evolutionary–developmental biology. Most studied segmented animals generate their segments in a repetitive, anterior-to-posterior fashion coordinated with the extension of the body axis from a posterior growth zone. In the current study we ask which selection pressures and ordering of evolutionary events may have contributed to the evolution of this specific segmentation mode. RESULTS: To answer this question we extend a previous in silico simulation model of the evolution of segmentation by allowing the tissue growth pattern to freely evolve. We then determine the likelihood of evolving oscillatory sequential segmentation combined with posterior growth under various conditions, such as the presence or absence of a posterior morphogen gradient or selection for determinate growth. We find that posterior growth with sequential segmentation is the predominant outcome of our simulations only if a posterior morphogen gradient is assumed to have already evolved and selection for determinate growth occurs secondarily. Otherwise, an alternative segmentation mechanism dominates, in which divisions occur in large bursts through the entire tissue and all segments are created simultaneously. CONCLUSIONS: Our study suggests that the ancestry of a posterior signalling centre has played an important role in the evolution of sequential segmentation. In addition, it suggests that determinate growth evolved secondarily, after the evolution of posterior growth. More generally, we demonstrate the potential of evo-devo simulation models that allow us to vary conditions as well as the onset of selection pressures to infer a likely order of evolutionary innovations. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13227-016-0052-8) contains supplementary material, which is available to authorized users. BioMed Central 2016-08-01 /pmc/articles/PMC4968448/ /pubmed/27482374 http://dx.doi.org/10.1186/s13227-016-0052-8 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
Vroomans, Renske M. A.
Hogeweg, Paulien
ten Tusscher, Kirsten H. W. J.
In silico evo-devo: reconstructing stages in the evolution of animal segmentation
title In silico evo-devo: reconstructing stages in the evolution of animal segmentation
title_full In silico evo-devo: reconstructing stages in the evolution of animal segmentation
title_fullStr In silico evo-devo: reconstructing stages in the evolution of animal segmentation
title_full_unstemmed In silico evo-devo: reconstructing stages in the evolution of animal segmentation
title_short In silico evo-devo: reconstructing stages in the evolution of animal segmentation
title_sort in silico evo-devo: reconstructing stages in the evolution of animal segmentation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4968448/
https://www.ncbi.nlm.nih.gov/pubmed/27482374
http://dx.doi.org/10.1186/s13227-016-0052-8
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