Periodic Fracture of Active Tissues

Fracture typically signifies mechanical failure in engineering materials, whereas controlled cracking may actively sculpt tissues through precise biological regulation. Here, we establish a multiscale nonlinear peridynamic theory that accounts for cellular mechanosensing to decipher the spontaneous fracture of active tissues. We show that tissues cultured in a ring-shaped domain can undergo periodic fracture to generate multicellular aggregates with regular spacing, recapitulating prior morphogenetic experiments on avian dermal cell collectives. It is found that the number of cracks varies nonmonotonically with the substrate stiffness. We predict that a narrow tissue favors equally spaced radial cracking, while such ordered cracks deflect, branch, and randomize increasingly as the tissue broadens, attributable to the anisotropy-isotropy transition of tissue stresses induced by the interplay of active contraction and domain geometry. Backed by energetic arguments, we identify the factors that control the characteristic size of tissue fracture. Our Letter reveals a synergy of physics, geometry, and cellular mechanosensing in controlling active tissue fracture to achieve tissue-level organization.