Network architecture determines vein fate during spontaneous reorganization, with a time delay

Vascular networks continuously reorganize their morphology by growing new or shrinking existing veins to optimize function. Flow shear stress on vein walls has been set forth as the local driver for this continuous adaptation. Yet, shear feedback alone cannot account for the observed diversity of network dynamics -- a puzzle made harder by scarce spatio-temporal data. Here, we resolve network-wide vein dynamics and shear during spontaneous reorganization in the prototypical vascular networks of Physarum polycephalum. Our experiments reveal a plethora of vein dynamics (stable, growing, shrinking) that are not directly proportional to local shear. We observe (a) that shear rate sensing on vein walls occurs with a time delay of 1 to 3 min and (b) that network architecture dependent parameters -- such as relative pressure or relative vein resistance -- are key to determine vein fate. We derive a model for vascular adaptation, based on force balance at the vein walls. Together with the time delay, our model reproduces the diversity of experimentally observed vein dynamics, and confirms the role of network architecture. Finally, we observe avalanches of network reorganization events which cause entire clusters of veins to vanish. Such avalanches are consistent with architectural feedback as the vein connections perpetually change with reorganization. As these network architecture dependent parameters are intrinsically connected with the laminar fluid flow in the veins, we expect our findings to play a role across flow-based vascular networks.