How Short-Range Forces Generate Long Range Order in Extreme Tissue Deformations

Extreme deformations in epithelial tissues play a key role in animal development and physiology. Tissue deformations have long range order and often arise from stochastic, short-range forces that must be coordinated in the absence of a master regulator. We use Hydra mouth opening as an in vivo biomechanics model for extreme tissue deformations. The mouth opening is tens of cell diameters wide, radially symmetric and occurs within 1-2 minutes. This extreme deformation is produced by stochastic contractile forces (tugs) acting over 2-3 cell diameters. Using Hydra’s regenerative capabilities, we employ tissue excision, grafting, and live imaging to identify the organizing “feature” that coordinates the tugs. Our experiments suggest that mechanical cell-cell coupling coordinate the tugs that pull the mouth open and that the boundary conditions control symmetry. Modelling the epithelial tissue as an active viscoelastic continuum, we identify how the stochastic force and tissue mechanical properties must be tuned to produce the observed opening behavior. We then relax the parameter space to identify regions that permit global order to arise from stochastic local forces more generally.