Active Cell Divisions Generate Four-Fold Orientational Order in Living Tissue

Morphogenetic programs in living systems reliably transform initially disordered tissues into highly ordered states, despite unfolding far from thermal equilibrium. The active physical mechanisms that generate and maintain order as part of these programs remain pooly understood. We uncover a four-fold orientationally ordered phase in the crustacean Parhyale hawaiensis and provide a quantitative profile of the tissue dynamics through which this order emerges. Light-sheet microscopy and tissue cartography reveal that actively orchestrated spatiotemporal profiles of cell division convert a disordered epithelial tissue into a robust tetratic phase with quasi-long range four-fold order. Waves of anisotropic cell proliferation propagate across the embryo with precise choreography so that defects introduced into the nascent lattice are healed by subsequent divisions. Using an active hydrodynamic model, we show that the tissue velocities leading to this ordered phase are incompressible and almost completely determined by the cell divisions. Strict control of cell proliferation rates and orientations enable cell divisions, which would otherwise fluidize the embryo, to serve as an active mechanism for generating four-fold order in a non-equilibrium system.