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Ethology of morphogenesis reveals the design principles of cnidarian size and shape development

Anniek Stokkermans, Aditi Chakrabarti, Ling Wang, Prachiti Moghe, Kaushikaram Subramanian, Petrus Steenbergen, View ORCID ProfileGregor Mönke, View ORCID ProfileTakashi Hiiragi, View ORCID ProfileRobert Prevedel, View ORCID ProfileL. Mahadevan, View ORCID ProfileAissam Ikmi
doi: https://doi.org/10.1101/2021.08.19.456976
Anniek Stokkermans
1Developmental biology unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
2Collaboration for joint PhD degree between EMBL and Heidelberg University, Faculty of Biosciences
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Aditi Chakrabarti
3School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138, USA
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Ling Wang
1Developmental biology unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
4Cell biology and biophysics unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
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Prachiti Moghe
1Developmental biology unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
2Collaboration for joint PhD degree between EMBL and Heidelberg University, Faculty of Biosciences
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Kaushikaram Subramanian
1Developmental biology unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
4Cell biology and biophysics unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
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Petrus Steenbergen
1Developmental biology unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
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Gregor Mönke
1Developmental biology unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
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Takashi Hiiragi
1Developmental biology unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
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  • ORCID record for Takashi Hiiragi
Robert Prevedel
1Developmental biology unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
4Cell biology and biophysics unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
5Epigenetics & Neurobiology Unit, European Molecular Biology Laboratory, Monterotondo, Italy
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L. Mahadevan
3School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138, USA
6Departments of Physics, and Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA
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  • For correspondence: lmahadev@g.harvard.edu aissam.ikmi@embl.de
Aissam Ikmi
1Developmental biology unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
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  • For correspondence: lmahadev@g.harvard.edu aissam.ikmi@embl.de
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Summary

During development, organisms interact with their natural habitats while undergoing morphological changes, yet it remains unclear whether the interplay between developing systems and their environments impacts animal morphogenesis. Here, we use the cnidarian Nematostella vectensis as a developmental model to uncover a mechanistic link between organism size, shape and behavior. Using quantitative live imaging, including extensive behavioral profiling, combined with molecular and biophysical experiments, we demonstrate that the muscular hydraulic machinery that controls body movement directly drives larva-polyp morphogenesis. Unexpectedly, size and shape development are differentially controlled by antagonistic muscles. A simple theoretical model shows how a combination of slow-priming and fast-pumping pressures generated by muscular hydraulics acts as a global mechanical regulator that coordinates tissue remodeling. Altogether, our findings illuminate how dynamic behavioral modes in the environment can be harnessed to drive morphogenetic trajectories, establishing ethology as a critical component of organismal morphogenesis – termed ethology of morphogenesis.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • In the abstract, "habits" should be "habitats".

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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Posted August 23, 2021.
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Ethology of morphogenesis reveals the design principles of cnidarian size and shape development
Anniek Stokkermans, Aditi Chakrabarti, Ling Wang, Prachiti Moghe, Kaushikaram Subramanian, Petrus Steenbergen, Gregor Mönke, Takashi Hiiragi, Robert Prevedel, L. Mahadevan, Aissam Ikmi
bioRxiv 2021.08.19.456976; doi: https://doi.org/10.1101/2021.08.19.456976
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Ethology of morphogenesis reveals the design principles of cnidarian size and shape development
Anniek Stokkermans, Aditi Chakrabarti, Ling Wang, Prachiti Moghe, Kaushikaram Subramanian, Petrus Steenbergen, Gregor Mönke, Takashi Hiiragi, Robert Prevedel, L. Mahadevan, Aissam Ikmi
bioRxiv 2021.08.19.456976; doi: https://doi.org/10.1101/2021.08.19.456976

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