Tuning collective behaviour in zebrafish with genetic modification.

Zebrafish collective behaviour is widely used to assess their physical and mental state, serving as a valuable tool to assess the impact of ageing, disease genetics, and the effect of drugs. The essence of these macroscopic phenomena can be represented by active matter models, where the individuals...

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Main Authors: Yushi Yang, Abdelwahab Kawafi, Qiao Tong, Erika Kague, Chrissy L Hammond, C Patrick Royall
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-10-01
Series:PLoS Computational Biology
Online Access:https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1012034&type=printable
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author Yushi Yang
Abdelwahab Kawafi
Qiao Tong
Erika Kague
Chrissy L Hammond
C Patrick Royall
author_facet Yushi Yang
Abdelwahab Kawafi
Qiao Tong
Erika Kague
Chrissy L Hammond
C Patrick Royall
author_sort Yushi Yang
collection DOAJ
description Zebrafish collective behaviour is widely used to assess their physical and mental state, serving as a valuable tool to assess the impact of ageing, disease genetics, and the effect of drugs. The essence of these macroscopic phenomena can be represented by active matter models, where the individuals are abstracted as interactive self-propelling agents. The behaviour of these agents depends on a set of parameters in a manner reminiscent of those between the constituents of physical systems. In a few cases, the system may be controlled at the level of the individual constituents such as the interactions between colloidal particles, or the enzymatic behaviour of de novo proteins. Usually, however, while the collective behaviour may be influenced by environmental factors, it typically cannot be changed at will. Here, we challenge this scenario in a biological context by genetically modifying zebrafish. We thus demonstrate the potential of genetic modification in the context of controlling the collective behaviour of biological active matter systems at the level of the constituents, rather than externally. In particular, we probe the effect of the lack of col11a2 gene in zebrafish, which causes the early onset of osteoarthritis. The resulting col11a2 -/- zebrafish exhibited compromised vertebral column properties, bent their body less while swimming, and took longer to change their orientations. Surprisingly, a group of 25 mutant fish exhibited more orderly collective motion than the wildtype. We show that the collective behaviour of wildtype and col11a2 -/- zebrafish are captured with a simple active matter model, in which the mutant fish are modelled by self-propelling agents with a higher orientational noise on average. In this way, we demonstrate the possibility of tuning a biological system, changing the state space it occupies when interpreted with a simple active matter model.
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spelling doaj-art-3eade64344cc4b4bb22103e3bc6c5f342025-08-20T02:46:20ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582024-10-012010e101203410.1371/journal.pcbi.1012034Tuning collective behaviour in zebrafish with genetic modification.Yushi YangAbdelwahab KawafiQiao TongErika KagueChrissy L HammondC Patrick RoyallZebrafish collective behaviour is widely used to assess their physical and mental state, serving as a valuable tool to assess the impact of ageing, disease genetics, and the effect of drugs. The essence of these macroscopic phenomena can be represented by active matter models, where the individuals are abstracted as interactive self-propelling agents. The behaviour of these agents depends on a set of parameters in a manner reminiscent of those between the constituents of physical systems. In a few cases, the system may be controlled at the level of the individual constituents such as the interactions between colloidal particles, or the enzymatic behaviour of de novo proteins. Usually, however, while the collective behaviour may be influenced by environmental factors, it typically cannot be changed at will. Here, we challenge this scenario in a biological context by genetically modifying zebrafish. We thus demonstrate the potential of genetic modification in the context of controlling the collective behaviour of biological active matter systems at the level of the constituents, rather than externally. In particular, we probe the effect of the lack of col11a2 gene in zebrafish, which causes the early onset of osteoarthritis. The resulting col11a2 -/- zebrafish exhibited compromised vertebral column properties, bent their body less while swimming, and took longer to change their orientations. Surprisingly, a group of 25 mutant fish exhibited more orderly collective motion than the wildtype. We show that the collective behaviour of wildtype and col11a2 -/- zebrafish are captured with a simple active matter model, in which the mutant fish are modelled by self-propelling agents with a higher orientational noise on average. In this way, we demonstrate the possibility of tuning a biological system, changing the state space it occupies when interpreted with a simple active matter model.https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1012034&type=printable
spellingShingle Yushi Yang
Abdelwahab Kawafi
Qiao Tong
Erika Kague
Chrissy L Hammond
C Patrick Royall
Tuning collective behaviour in zebrafish with genetic modification.
PLoS Computational Biology
title Tuning collective behaviour in zebrafish with genetic modification.
title_full Tuning collective behaviour in zebrafish with genetic modification.
title_fullStr Tuning collective behaviour in zebrafish with genetic modification.
title_full_unstemmed Tuning collective behaviour in zebrafish with genetic modification.
title_short Tuning collective behaviour in zebrafish with genetic modification.
title_sort tuning collective behaviour in zebrafish with genetic modification
url https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1012034&type=printable
work_keys_str_mv AT yushiyang tuningcollectivebehaviourinzebrafishwithgeneticmodification
AT abdelwahabkawafi tuningcollectivebehaviourinzebrafishwithgeneticmodification
AT qiaotong tuningcollectivebehaviourinzebrafishwithgeneticmodification
AT erikakague tuningcollectivebehaviourinzebrafishwithgeneticmodification
AT chrissylhammond tuningcollectivebehaviourinzebrafishwithgeneticmodification
AT cpatrickroyall tuningcollectivebehaviourinzebrafishwithgeneticmodification