Scale-free flocking and giant fluctuations in epithelial active solids

TL;DR

This paper uncovers a novel large-scale collective motion in epithelial cell layers, characterized as a polar elastic solid with scale-free correlations and giant fluctuations, challenging the fluid paradigm of cellular flocking.

Contribution

It introduces the concept of epithelial cell layers behaving as polar active solids with unique long-range order and fluctuation properties, supported by both experimental data and theoretical modeling.

Findings

Cells move coherently as a polar elastic solid, not a fluid.

The phase exhibits scale-free correlations and giant density fluctuations.

Elastic deformation fluctuations diverge with system size, risking tissue rupture.

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, such as 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.