Dynamic morphoskeletons in development

Abstract

Morphogenetic flows in developmental biology are characterized by the coordinated motion of thousands of cells that organize into tissues, naturally raising the question of how this collective organization arises. Using only the kinematics of tissue deformation, which naturally integrates local and global mechanisms along cell paths, we identify the dynamic morphoskeletons behind morphogenesis, i.e., the evolving centerpieces of multicellular trajectory patterns. These features are model- and parameter-free, frame-invariant, and robust to measurement errors and can be computed from unfiltered cell-velocity data. We reveal the spatial attractors and repellers of the embryo by quantifying its Lagrangian deformation, information that is inaccessible to simple trajectory inspection or Eulerian methods that are local and typically frame-dependent. Computing these dynamic morphoskeletons in wild-type and mutant chick and fly embryos, we find that they capture the early footprint of known morphogenetic features, reveal new ones, and quantitatively distinguish between different phenotypes. Significance Coordinated cell migration is a hallmark of tissue morphogenesis during development and emerges from the combination of local cell behaviors and distributed chemo-mechanical interactions integrated across many spatial and temporal scales. A challenge in the field is to predict developmental outcomes of tissue morphogenesis using cellular trajectories. We provide a rigorous kinematic framework to analyze cell motion and identify robust multicellular attractors and repellers in space and time. Our results yield a scheme for comparing different morphogenetic phenotypes and help bridge the gap between bottom-up and top-down modeling approaches to morphogenesis.