Scale-free flocking and giant fluctuations in epithelial active solids

Abstract

The collective motion of epithelial cells is a fundamental biological process which plays a significant role in embryogenesis, wound healing and tumor metastasis. While it has been broadly investigated for over a decade both in vivo and in vitro, large scale coherent flocking phases remain underexplored and have so far been mostly described as fluid. In this work, we report a mode of large-scale collective motion for different epithelial cell types in vitro with distinctive new features. By tracking individual cells, we show that cells move over long time scales coherently not as a fluid, but as a polar elastic solid with negligible cell rearrangements. Our analysis reveals that this solid flocking phase exhibits signatures of long-range polar order, unprecedented in cellular systems, with scale-free correlations, anomalously large density fluctuations, and shear waves. Based on a general theory of active polar solids, we argue that these features result from massless Goldstone modes, which, in contrast to polar fluids where they are generic, require the decoupling of global rotations of the polarity and in-plane elastic deformations in polar solids. We theoretically show and consistently observe in experiments that the fluctuations of elastic deformations diverge for large system size in such polar active solid phases, leading eventually to rupture and thus potentially loss of tissue integrity at large scales. Significance statementDuring embryonic development and wound healing, epithelial cells usually display in-plane polarity over large spatial scales and move coherently. However, over years, most in vitro studies have examined the fluid-like chaotic dynamics of epithelial cells, in which collective cellular flows self-organize into recurring transient vortices and jets similar to those observed in classical fluid turbulence. Little is known about the large-scale coherent dynamics of epithelial cells. We demonstrate that such coherent motions are not simply turbulent-like flows with larger correlation lengths, but a new mode of collective motion with a solid-like behavior, accompanied by an emergent global order, scale-free correlations, anomalous density fluctuations and propagating Goldstone modes. Our work suggests that such a collective motion of epithelial cells falls outside the scope of traditional active fluids, which may shed new light on the current studies of collective cell migration as well as active matter physics.