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Dynamical systems approach to evolution–development congruence: Revisiting Haeckel's recapitulation theory

It is acknowledged that embryonic development has a tendency to proceed from common toward specific. Ernst Haeckel raised the question of why that tendency prevailed through evolution, and the question remains unsolved. Here, we revisit Haeckel's recapitulation theory, that is, the parallelism...

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Autores principales: Kohsokabe, Takahiro, Kaneko, Kunihiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9291011/
https://www.ncbi.nlm.nih.gov/pubmed/33600605
http://dx.doi.org/10.1002/jez.b.23031
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author Kohsokabe, Takahiro
Kaneko, Kunihiko
author_facet Kohsokabe, Takahiro
Kaneko, Kunihiko
author_sort Kohsokabe, Takahiro
collection PubMed
description It is acknowledged that embryonic development has a tendency to proceed from common toward specific. Ernst Haeckel raised the question of why that tendency prevailed through evolution, and the question remains unsolved. Here, we revisit Haeckel's recapitulation theory, that is, the parallelism between evolution and development through numerical evolution and dynamical systems theory. By using intracellular gene expression dynamics with cell‐to‐cell interaction over spatially aligned cells to represent the developmental process, gene regulation networks (GRN) that govern these dynamics evolve under the selection pressure to achieve a prescribed spatial gene expression pattern. For most numerical evolutionary experiments, the evolutionary pattern changes over generations, as well as the developmental pattern changes governed by the evolved GRN exhibit remarkable similarity. Changes in both patterns consisted of several epochs where stripes are formed in a short time, whereas for other temporal regimes, the pattern hardly changes. In evolution, these quasi‐stationary generations are needed to achieve relevant mutations, whereas, in development, they are due to some gene expressions that vary slowly and control the pattern change. These successive epochal changes in development and evolution are represented as common bifurcations in dynamical systems theory, regulating working network structure from feedforward subnetwork to those containing feedback loops. The congruence is the correspondence between successive acquisitions of subnetworks through evolution and changes in working subnetworks in development. Consistency of the theory with the segmentation gene‐expression dynamics is discussed. Novel outlook on recapitulation and heterochrony are provided, testable experimentally by the transcriptome and network analysis.
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spelling pubmed-92910112022-07-20 Dynamical systems approach to evolution–development congruence: Revisiting Haeckel's recapitulation theory Kohsokabe, Takahiro Kaneko, Kunihiko J Exp Zool B Mol Dev Evol Reviews It is acknowledged that embryonic development has a tendency to proceed from common toward specific. Ernst Haeckel raised the question of why that tendency prevailed through evolution, and the question remains unsolved. Here, we revisit Haeckel's recapitulation theory, that is, the parallelism between evolution and development through numerical evolution and dynamical systems theory. By using intracellular gene expression dynamics with cell‐to‐cell interaction over spatially aligned cells to represent the developmental process, gene regulation networks (GRN) that govern these dynamics evolve under the selection pressure to achieve a prescribed spatial gene expression pattern. For most numerical evolutionary experiments, the evolutionary pattern changes over generations, as well as the developmental pattern changes governed by the evolved GRN exhibit remarkable similarity. Changes in both patterns consisted of several epochs where stripes are formed in a short time, whereas for other temporal regimes, the pattern hardly changes. In evolution, these quasi‐stationary generations are needed to achieve relevant mutations, whereas, in development, they are due to some gene expressions that vary slowly and control the pattern change. These successive epochal changes in development and evolution are represented as common bifurcations in dynamical systems theory, regulating working network structure from feedforward subnetwork to those containing feedback loops. The congruence is the correspondence between successive acquisitions of subnetworks through evolution and changes in working subnetworks in development. Consistency of the theory with the segmentation gene‐expression dynamics is discussed. Novel outlook on recapitulation and heterochrony are provided, testable experimentally by the transcriptome and network analysis. John Wiley and Sons Inc. 2021-02-18 2022-01 /pmc/articles/PMC9291011/ /pubmed/33600605 http://dx.doi.org/10.1002/jez.b.23031 Text en © 2021 The Authors. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution Published by Wiley Periodicals LLC https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Reviews
Kohsokabe, Takahiro
Kaneko, Kunihiko
Dynamical systems approach to evolution–development congruence: Revisiting Haeckel's recapitulation theory
title Dynamical systems approach to evolution–development congruence: Revisiting Haeckel's recapitulation theory
title_full Dynamical systems approach to evolution–development congruence: Revisiting Haeckel's recapitulation theory
title_fullStr Dynamical systems approach to evolution–development congruence: Revisiting Haeckel's recapitulation theory
title_full_unstemmed Dynamical systems approach to evolution–development congruence: Revisiting Haeckel's recapitulation theory
title_short Dynamical systems approach to evolution–development congruence: Revisiting Haeckel's recapitulation theory
title_sort dynamical systems approach to evolution–development congruence: revisiting haeckel's recapitulation theory
topic Reviews
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9291011/
https://www.ncbi.nlm.nih.gov/pubmed/33600605
http://dx.doi.org/10.1002/jez.b.23031
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