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A physical theory of larval Drosophila behaviour

View ORCID ProfileJane Loveless, Alastair Garner, View ORCID ProfileAbdul Raouf Issa, View ORCID ProfileRuairí J. V. Roberts, View ORCID ProfileBarbara Webb, View ORCID ProfileLucia L. Prieto-Godino, View ORCID ProfileTomoko Ohyama, View ORCID ProfileClaudio R. Alonso
doi: https://doi.org/10.1101/2020.08.25.266163
Jane Loveless
1Sussex Neuroscience, School of Life Sciences, University of Sussex, Brighton, BN1 9QG, United Kingdom
2Integrated Program in Neuroscience, Department of Biology, McGill University, Montreal, QC, H3A 1B1, Canada
4Insect Robotics Laboratory, School of Informatics, University of Edinburgh, Edinburgh, EH8 9AB, United Kingdom
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  • For correspondence: jane.loveless@protonmail.com tomoko.ohyama@mcgill.ca C.Alonso@sussex.ac.uk
Alastair Garner
2Integrated Program in Neuroscience, Department of Biology, McGill University, Montreal, QC, H3A 1B1, Canada
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Abdul Raouf Issa
1Sussex Neuroscience, School of Life Sciences, University of Sussex, Brighton, BN1 9QG, United Kingdom
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Ruairí J. V. Roberts
3Neural Circuits and Evolution Laboratory, The Francies Crick Institute, London, NW1 1AT, UK
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Barbara Webb
4Insect Robotics Laboratory, School of Informatics, University of Edinburgh, Edinburgh, EH8 9AB, United Kingdom
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Lucia L. Prieto-Godino
3Neural Circuits and Evolution Laboratory, The Francies Crick Institute, London, NW1 1AT, UK
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Tomoko Ohyama
2Integrated Program in Neuroscience, Department of Biology, McGill University, Montreal, QC, H3A 1B1, Canada
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  • For correspondence: jane.loveless@protonmail.com tomoko.ohyama@mcgill.ca C.Alonso@sussex.ac.uk
Claudio R. Alonso
1Sussex Neuroscience, School of Life Sciences, University of Sussex, Brighton, BN1 9QG, United Kingdom
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  • For correspondence: jane.loveless@protonmail.com tomoko.ohyama@mcgill.ca C.Alonso@sussex.ac.uk
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Abstract

All animal behaviour must ultimately be governed by physical laws. As a basis for understanding the physics of behaviour in fruit fly larvae, we here develop an effective theory for the animals’ motion in three dimensions.

We first define a set of fields which quantify stretching, bending, and twisting along the larva’s anteroposterior axis, then perform a search in the space of possible theories that could govern these fields’ long-wavelength physics. Guided by symmetry considerations and stability requirements, we arrive at a unique, analytically tractable free-field theory with a minimum of free parameters.

Surprisingly, we are able to explain many features of larval behaviour by applying equilibrium statistical mechanics to this model. Our theory closely predicts the animals’ postural modes (eigenmaggots) as well as distributions and trajectories in the postural mode space, across several behaviours (crawling, rolling, self-righting, unbiased exploration).

We explain the low-dimensionality of postural dynamics via Boltzmann suppression of high frequency modes, and also propose and experimentally test novel predictions on the relationships between different behaviours. We show that crawling and rolling are dominated by similar symmetry properties, leading to identical dynamics/statistics in mode space, while rolling and unbiased exploration have a common dominant timescale. Together, our results demonstrate that relatively simple effective physics can be used to explain and predict animal behaviour.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • author list & author roles and acknowledgements updated; minor typographical errors fixed throughout; cosmetic changes to abstract; methods section updated to include details of self-righting behaviour experiments and analysis

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted December 22, 2020.
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A physical theory of larval Drosophila behaviour
Jane Loveless, Alastair Garner, Abdul Raouf Issa, Ruairí J. V. Roberts, Barbara Webb, Lucia L. Prieto-Godino, Tomoko Ohyama, Claudio R. Alonso
bioRxiv 2020.08.25.266163; doi: https://doi.org/10.1101/2020.08.25.266163
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A physical theory of larval Drosophila behaviour
Jane Loveless, Alastair Garner, Abdul Raouf Issa, Ruairí J. V. Roberts, Barbara Webb, Lucia L. Prieto-Godino, Tomoko Ohyama, Claudio R. Alonso
bioRxiv 2020.08.25.266163; doi: https://doi.org/10.1101/2020.08.25.266163

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