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Computational exploration of treadmilling and protrusion growth observed in fire ant rafts

Collective living systems regularly achieve cooperative emergent functions that individual organisms could not accomplish alone. The rafts of fire ants (Solenopsis invicta) are often studied in this context for their ability to create aggregated structures comprised entirely of their own bodies, inc...

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Autores principales: Wagner, Robert J., Vernerey, Franck J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8890740/
https://www.ncbi.nlm.nih.gov/pubmed/35176019
http://dx.doi.org/10.1371/journal.pcbi.1009869
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author Wagner, Robert J.
Vernerey, Franck J.
author_facet Wagner, Robert J.
Vernerey, Franck J.
author_sort Wagner, Robert J.
collection PubMed
description Collective living systems regularly achieve cooperative emergent functions that individual organisms could not accomplish alone. The rafts of fire ants (Solenopsis invicta) are often studied in this context for their ability to create aggregated structures comprised entirely of their own bodies, including tether-like protrusions that facilitate exploration of and escape from flooded environments. While similar protrusions are observed in cytoskeletons and cellular aggregates, they are generally dependent on morphogens or external gradients leaving the isolated role of local interactions poorly understood. Here we demonstrate through an ant-inspired, agent-based numerical model how protrusions in ant rafts may emerge spontaneously due to local interactions. The model is comprised of a condensed structural network of agents that represents the monolayer of interconnected worker ants, which floats on the water and gives ant rafts their form. Experimentally, this layer perpetually contracts, which we capture through the pairwise contraction of all neighboring structural agents at a strain rate of [Image: see text] . On top of the structural layer, we model a dispersed, on-lattice layer of motile agents that represents free ants, which walk on top of the floating network. Experimentally, these self-propelled free ants walk with some mean persistence length and speed that we capture through an ant-inspired phenomenological model. Local interactions occur between neighboring free ants within some radius of detection, R, and the persistence length of freely active agents is tuned through a noise parameter, η as introduced by the Vicsek model. Both R and η where fixed to match the experimental trajectories of free ants. Treadmilling of the raft occurs as agents transition between the structural and free layers in accordance with experimental observations. Ultimately, we demonstrate how phases of exploratory protrusion growth may be induced by increased ant activity as characterized by a dimensionless parameter, [Image: see text] . These results provide an example in which functional morphogenesis of a living system may emerge purely from local interactions at the constituent length scale, thereby providing a source of inspiration for the development of decentralized, autonomous active matter and swarm robotics.
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spelling pubmed-88907402022-03-03 Computational exploration of treadmilling and protrusion growth observed in fire ant rafts Wagner, Robert J. Vernerey, Franck J. PLoS Comput Biol Research Article Collective living systems regularly achieve cooperative emergent functions that individual organisms could not accomplish alone. The rafts of fire ants (Solenopsis invicta) are often studied in this context for their ability to create aggregated structures comprised entirely of their own bodies, including tether-like protrusions that facilitate exploration of and escape from flooded environments. While similar protrusions are observed in cytoskeletons and cellular aggregates, they are generally dependent on morphogens or external gradients leaving the isolated role of local interactions poorly understood. Here we demonstrate through an ant-inspired, agent-based numerical model how protrusions in ant rafts may emerge spontaneously due to local interactions. The model is comprised of a condensed structural network of agents that represents the monolayer of interconnected worker ants, which floats on the water and gives ant rafts their form. Experimentally, this layer perpetually contracts, which we capture through the pairwise contraction of all neighboring structural agents at a strain rate of [Image: see text] . On top of the structural layer, we model a dispersed, on-lattice layer of motile agents that represents free ants, which walk on top of the floating network. Experimentally, these self-propelled free ants walk with some mean persistence length and speed that we capture through an ant-inspired phenomenological model. Local interactions occur between neighboring free ants within some radius of detection, R, and the persistence length of freely active agents is tuned through a noise parameter, η as introduced by the Vicsek model. Both R and η where fixed to match the experimental trajectories of free ants. Treadmilling of the raft occurs as agents transition between the structural and free layers in accordance with experimental observations. Ultimately, we demonstrate how phases of exploratory protrusion growth may be induced by increased ant activity as characterized by a dimensionless parameter, [Image: see text] . These results provide an example in which functional morphogenesis of a living system may emerge purely from local interactions at the constituent length scale, thereby providing a source of inspiration for the development of decentralized, autonomous active matter and swarm robotics. Public Library of Science 2022-02-17 /pmc/articles/PMC8890740/ /pubmed/35176019 http://dx.doi.org/10.1371/journal.pcbi.1009869 Text en © 2022 Wagner, Vernerey https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Wagner, Robert J.
Vernerey, Franck J.
Computational exploration of treadmilling and protrusion growth observed in fire ant rafts
title Computational exploration of treadmilling and protrusion growth observed in fire ant rafts
title_full Computational exploration of treadmilling and protrusion growth observed in fire ant rafts
title_fullStr Computational exploration of treadmilling and protrusion growth observed in fire ant rafts
title_full_unstemmed Computational exploration of treadmilling and protrusion growth observed in fire ant rafts
title_short Computational exploration of treadmilling and protrusion growth observed in fire ant rafts
title_sort computational exploration of treadmilling and protrusion growth observed in fire ant rafts
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8890740/
https://www.ncbi.nlm.nih.gov/pubmed/35176019
http://dx.doi.org/10.1371/journal.pcbi.1009869
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