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Specialisation and plasticity in a primitively social insect

S. Patalano, View ORCID ProfileA. Alsina, C. Gregorio-Rodriguez, M. Bachman, S. Dreier, I. Hernando-Herraez, P. Nana, S. Balasubramanian, S. Sumner, W. Reik, View ORCID ProfileS. Rulands
doi: https://doi.org/10.1101/2020.03.31.007492
S. Patalano
1The Babraham Institute, Cambridge CB22 3AT, United Kingdom
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  • For correspondence: patalano@fleming.gr rulands@pks.mpg.de wolf.reik@babraham.ac.uk
A. Alsina
2Max Planck Institute for the Physics of Complex Systems, Noethnitzer Str. 38, 01187 Dresden, Germany
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  • ORCID record for A. Alsina
C. Gregorio-Rodriguez
3Departamento de Sistemas Informáticos y Computación, Universidad Complutense de Madrid, Plaza de Ciencias, 3, 28040 Madrid, Spain
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M. Bachman
4Discovery Science and Technology, Medicines Discovery Catapult, Alderley Park, Chelshire SK10 4GT, United Kingdom
5Cancer Research UK Cambridge Institute, University of Cambridge, Li Ka Shing Centre Cambridge CB2 ORE, United Kingdom
6Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom
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S. Dreier
7Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, United Kingdom
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I. Hernando-Herraez
1The Babraham Institute, Cambridge CB22 3AT, United Kingdom
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P. Nana
8Faculty of Agronomy and Agricultural Sciences, School of Wood, Water and Natural Resources, University of Dschang, Ebolowa Campus, P. O. Box 786, Ebolowa, Cameroon
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S. Balasubramanian
5Cancer Research UK Cambridge Institute, University of Cambridge, Li Ka Shing Centre Cambridge CB2 ORE, United Kingdom
6Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom
9School of Clinical Medicine, University of Cambridge, CB2 0SP, Cambridge, United Kingdom
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S. Sumner
10Centre for Biodiversity and Environmental Research, Department of Genetics Evolution and Environment, Division of Biosciences, University College London, Gower Street, London WC1E 6BT, United Kingdom
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W. Reik
1The Babraham Institute, Cambridge CB22 3AT, United Kingdom
11Wellcome Trust Sanger Institute, Hinxton CB10 1SA, United Kingdom
12Centre for Trophoblast Research, University of Cambridge, Cambridge CB2 3EG, United Kingdom
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  • For correspondence: patalano@fleming.gr rulands@pks.mpg.de wolf.reik@babraham.ac.uk
S. Rulands
2Max Planck Institute for the Physics of Complex Systems, Noethnitzer Str. 38, 01187 Dresden, Germany
13Center for Systems Biology Dresden, Pfotenhauer Str. 108, 01307 Dresden, Germany
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  • ORCID record for S. Rulands
  • For correspondence: patalano@fleming.gr rulands@pks.mpg.de wolf.reik@babraham.ac.uk
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Abstract

Biological systems not only have the remarkable capacity to build and maintain complex spatio-temporal structures in noisy environments, they can also rapidly break up and rebuild such structures. How such systems can simultaneously achieve both robust specialisation and plasticity is poorly understood. Here we use primitive societies of Polistes wasps as a model system where we experimentally perturb the social structure by removing the queen and follow the re-establishment of the social steady state over time. We combine a unique experimental strategy correlating time-resolved measurements across vastly different scales with a theoretical approach. We show that Polistes integrates antagonistic processes on multiple scales to distinguish between extrinsic and intrinsic perturbations and thereby achieve both robust specialisation and rapid plasticity. The long-term stability of the social structure relies on dynamic DNA methylation which controls transcriptional noise. Such dynamics provide a general principle of how both specialization and plasticity can be achieved in biological systems.

One Sentence Summary A primitive social insect simultaneously achieves specialisation and plasticity by integrating antagonistic dynamics on different scales.

Highlights

  • We employ a unique experimental approach correlating dynamics of societies, individuals, and epigenetic gene regulation

  • A social insect simultaneously achieves specialisation and plasticity by integrating antagonistic processes on different spatial scales

  • Regulation of population-level noise by DNA methylation ensures long-term stability of phenotypic specialisation

Footnotes

  • ↵# Joint senior authors

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-NC-ND 4.0 International license.
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Specialisation and plasticity in a primitively social insect
S. Patalano, A. Alsina, C. Gregorio-Rodriguez, M. Bachman, S. Dreier, I. Hernando-Herraez, P. Nana, S. Balasubramanian, S. Sumner, W. Reik, S. Rulands
bioRxiv 2020.03.31.007492; doi: https://doi.org/10.1101/2020.03.31.007492
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Specialisation and plasticity in a primitively social insect
S. Patalano, A. Alsina, C. Gregorio-Rodriguez, M. Bachman, S. Dreier, I. Hernando-Herraez, P. Nana, S. Balasubramanian, S. Sumner, W. Reik, S. Rulands
bioRxiv 2020.03.31.007492; doi: https://doi.org/10.1101/2020.03.31.007492

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