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Growth produces coordination trade-offs in Trichoplax adhaerens, an animal lacking a central nervous system

How collectives remain coordinated as they grow in size is a fundamental challenge affecting systems ranging from biofilms to governments. This challenge is particularly apparent in multicellular organisms, where coordination among a vast number of cells is vital for coherent animal behavior. Howeve...

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Autores principales: Davidescu, Mircea R., Romanczuk, Pawel, Gregor, Thomas, Couzin, Iain D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10089153/
https://www.ncbi.nlm.nih.gov/pubmed/36897970
http://dx.doi.org/10.1073/pnas.2206163120
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author Davidescu, Mircea R.
Romanczuk, Pawel
Gregor, Thomas
Couzin, Iain D.
author_facet Davidescu, Mircea R.
Romanczuk, Pawel
Gregor, Thomas
Couzin, Iain D.
author_sort Davidescu, Mircea R.
collection PubMed
description How collectives remain coordinated as they grow in size is a fundamental challenge affecting systems ranging from biofilms to governments. This challenge is particularly apparent in multicellular organisms, where coordination among a vast number of cells is vital for coherent animal behavior. However, the earliest multicellular organisms were decentralized, with indeterminate sizes and morphologies, as exemplified by Trichoplax adhaerens, arguably the earliest-diverged and simplest motile animal. We investigated coordination among cells in T. adhaerens by observing the degree of collective order in locomotion across animals of differing sizes and found that larger individuals exhibit increasingly disordered locomotion. We reproduced this effect of size on order through a simulation model of active elastic cellular sheets and demonstrate that this relationship is best recapitulated across all body sizes when the simulation parameters are tuned to a critical point in the parameter space. We quantify the trade-off between increasing size and coordination in a multicellular animal with a decentralized anatomy that shows evidence of criticality and hypothesize as to the implications of this on the evolution hierarchical structures such as nervous systems in larger organisms.
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spelling pubmed-100891532023-04-12 Growth produces coordination trade-offs in Trichoplax adhaerens, an animal lacking a central nervous system Davidescu, Mircea R. Romanczuk, Pawel Gregor, Thomas Couzin, Iain D. Proc Natl Acad Sci U S A Biological Sciences How collectives remain coordinated as they grow in size is a fundamental challenge affecting systems ranging from biofilms to governments. This challenge is particularly apparent in multicellular organisms, where coordination among a vast number of cells is vital for coherent animal behavior. However, the earliest multicellular organisms were decentralized, with indeterminate sizes and morphologies, as exemplified by Trichoplax adhaerens, arguably the earliest-diverged and simplest motile animal. We investigated coordination among cells in T. adhaerens by observing the degree of collective order in locomotion across animals of differing sizes and found that larger individuals exhibit increasingly disordered locomotion. We reproduced this effect of size on order through a simulation model of active elastic cellular sheets and demonstrate that this relationship is best recapitulated across all body sizes when the simulation parameters are tuned to a critical point in the parameter space. We quantify the trade-off between increasing size and coordination in a multicellular animal with a decentralized anatomy that shows evidence of criticality and hypothesize as to the implications of this on the evolution hierarchical structures such as nervous systems in larger organisms. National Academy of Sciences 2023-03-10 2023-03-14 /pmc/articles/PMC10089153/ /pubmed/36897970 http://dx.doi.org/10.1073/pnas.2206163120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Davidescu, Mircea R.
Romanczuk, Pawel
Gregor, Thomas
Couzin, Iain D.
Growth produces coordination trade-offs in Trichoplax adhaerens, an animal lacking a central nervous system
title Growth produces coordination trade-offs in Trichoplax adhaerens, an animal lacking a central nervous system
title_full Growth produces coordination trade-offs in Trichoplax adhaerens, an animal lacking a central nervous system
title_fullStr Growth produces coordination trade-offs in Trichoplax adhaerens, an animal lacking a central nervous system
title_full_unstemmed Growth produces coordination trade-offs in Trichoplax adhaerens, an animal lacking a central nervous system
title_short Growth produces coordination trade-offs in Trichoplax adhaerens, an animal lacking a central nervous system
title_sort growth produces coordination trade-offs in trichoplax adhaerens, an animal lacking a central nervous system
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10089153/
https://www.ncbi.nlm.nih.gov/pubmed/36897970
http://dx.doi.org/10.1073/pnas.2206163120
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