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Darwin’s agential materials: evolutionary implications of multiscale competency in developmental biology

A critical aspect of evolution is the layer of developmental physiology that operates between the genotype and the anatomical phenotype. While much work has addressed the evolution of developmental mechanisms and the evolvability of specific genetic architectures with emergent complexity, one aspect...

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Autor principal: Levin, Michael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer International Publishing 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10167196/
https://www.ncbi.nlm.nih.gov/pubmed/37156924
http://dx.doi.org/10.1007/s00018-023-04790-z
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author Levin, Michael
author_facet Levin, Michael
author_sort Levin, Michael
collection PubMed
description A critical aspect of evolution is the layer of developmental physiology that operates between the genotype and the anatomical phenotype. While much work has addressed the evolution of developmental mechanisms and the evolvability of specific genetic architectures with emergent complexity, one aspect has not been sufficiently explored: the implications of morphogenetic problem-solving competencies for the evolutionary process itself. The cells that evolution works with are not passive components: rather, they have numerous capabilities for behavior because they derive from ancestral unicellular organisms with rich repertoires. In multicellular organisms, these capabilities must be tamed, and can be exploited, by the evolutionary process. Specifically, biological structures have a multiscale competency architecture where cells, tissues, and organs exhibit regulative plasticity—the ability to adjust to perturbations such as external injury or internal modifications and still accomplish specific adaptive tasks across metabolic, transcriptional, physiological, and anatomical problem spaces. Here, I review examples illustrating how physiological circuits guiding cellular collective behavior impart computational properties to the agential material that serves as substrate for the evolutionary process. I then explore the ways in which the collective intelligence of cells during morphogenesis affect evolution, providing a new perspective on the evolutionary search process. This key feature of the physiological software of life helps explain the remarkable speed and robustness of biological evolution, and sheds new light on the relationship between genomes and functional anatomical phenotypes.
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spelling pubmed-101671962023-05-10 Darwin’s agential materials: evolutionary implications of multiscale competency in developmental biology Levin, Michael Cell Mol Life Sci Review A critical aspect of evolution is the layer of developmental physiology that operates between the genotype and the anatomical phenotype. While much work has addressed the evolution of developmental mechanisms and the evolvability of specific genetic architectures with emergent complexity, one aspect has not been sufficiently explored: the implications of morphogenetic problem-solving competencies for the evolutionary process itself. The cells that evolution works with are not passive components: rather, they have numerous capabilities for behavior because they derive from ancestral unicellular organisms with rich repertoires. In multicellular organisms, these capabilities must be tamed, and can be exploited, by the evolutionary process. Specifically, biological structures have a multiscale competency architecture where cells, tissues, and organs exhibit regulative plasticity—the ability to adjust to perturbations such as external injury or internal modifications and still accomplish specific adaptive tasks across metabolic, transcriptional, physiological, and anatomical problem spaces. Here, I review examples illustrating how physiological circuits guiding cellular collective behavior impart computational properties to the agential material that serves as substrate for the evolutionary process. I then explore the ways in which the collective intelligence of cells during morphogenesis affect evolution, providing a new perspective on the evolutionary search process. This key feature of the physiological software of life helps explain the remarkable speed and robustness of biological evolution, and sheds new light on the relationship between genomes and functional anatomical phenotypes. Springer International Publishing 2023-05-08 2023 /pmc/articles/PMC10167196/ /pubmed/37156924 http://dx.doi.org/10.1007/s00018-023-04790-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Review
Levin, Michael
Darwin’s agential materials: evolutionary implications of multiscale competency in developmental biology
title Darwin’s agential materials: evolutionary implications of multiscale competency in developmental biology
title_full Darwin’s agential materials: evolutionary implications of multiscale competency in developmental biology
title_fullStr Darwin’s agential materials: evolutionary implications of multiscale competency in developmental biology
title_full_unstemmed Darwin’s agential materials: evolutionary implications of multiscale competency in developmental biology
title_short Darwin’s agential materials: evolutionary implications of multiscale competency in developmental biology
title_sort darwin’s agential materials: evolutionary implications of multiscale competency in developmental biology
topic Review
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10167196/
https://www.ncbi.nlm.nih.gov/pubmed/37156924
http://dx.doi.org/10.1007/s00018-023-04790-z
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