A tensile ring drives tissue flows to shape the gastrulating amniote embryo

Abstract Tissue morphogenesis is driven by local cellular deformations, themselves powered by contractile actomyosin networks. While it is well demonstrated that cell-generated forces at the microscopic scale underlie a variety of local morphogenetic processes (e.g. lengthening/ narrowing 1–4 , bending 5–8 , or folding 9,10 ), how such local forces are transmitted across tissues to shape them at a mesoscopic scale remains largely unknown. Here, by performing a quantitative analysis of gastrulation in entire avian embryos, we show that the formation of the primitive streak and the associated large-scale rotational tissue flows (i.e. ‘polonaise’ movements 11,12 ) are integral parts of a global process that is captured by the laws of fluid mechanics. We identify a large-scale supracellular actomyosin ring (2 mm in diameter and 250 μm thick) that shapes the embryo by exerting a graded tension along the margin between the embryonic and extra-embryonic territories. Tissue-wide flows arise from the transmission of these localized forces across the embryonic disk and are quantitatively recapitulated by a fluid-mechanical model based on the Stokes equations for viscous flow. We further show that cell division, the main driver of cell rearrangements at this stage 13 , is required for fluid-like behavior and for the progress of gastrulation movements. Our results demonstrate the power of a hydrodynamic approach to tissue-wide morphogenetic processes 14–16 and provide a simple, unified mechanical picture of amniote gastrulation. A tensile embryo margin, in addition to directing tissue motion, could act as an interface between mechanical and molecular cues, and play a central role in embryonic self-organization.