Abstract
A long-standing goal of evolutionary developmental biology is to identify the rules by which processes governing individual cells scale up to organism-level patterning. The viscoelastic properties of embryonic tissues imply collective cell behaviours, leading to the expectation that gene regulatory networks should capitalize on the material properties of tissues. Here, we show that large-scale variation in morphogenesis can be traced to cell-level dynamic. In avian beak primordia, we find that fields of mesenchymal cells undergo cycles of local jamming that predictably change coordination of cell shapes and movements. These cycles, in turn, alter the spatial reach of regulatory proteins, shaping their gradients in relation to tissue mechanical state. Long-range gradients of proteins most sensitive to local jamming differ the most across populations and, through their priming of tissue compartmentalization, can facilitate evolutionary divergence in beak morphology. Jamming transitions might thus allow these tissues to reconcile seemingly contradictory needs: robust maintenance, facilitated by jamming phase that resets or synchronizes cells, and adaptive flexibility, promoted by unjamming phase, that allow rearrangements, explorations or expansions. These transitions can also integrate stochastic physical processes and biological regulation allowing local rules governing cell behaviours to propagate to tissue-level patterning, ultimately promoting diversification and plasticity while preserving robustness.