Integrating cell and tissue motion patterns during early embryogenesis: How much “Cell Migration” really occurs?

The assembly of a hornet's nest is an example of an emergent biological pattern. Construction of a nest is not directly encoded in genetic or cell regulatory pathways. The architecture arises from thousands of hornets following simple instinctive rules; and cannot be reduced to the study of an individual hornet or its constituent parts. Our recent studies show that amniotes rely on emergent patterns to a much greater extent compared to other vertebrates. For example, time‐lapse imaging data provide mounting evidence that early bird embryos engage in significantly less autonomous cellular motion compared to fish or frog embryos. In fact, we find a preponderance of collective cell/tissue behavior in birds. Our data suggest that during evolution, amniotes selected morphogenetic mechanisms in which the embryo is shaped by collectively engineering a new micromechanical state of the tissue — which generates physical displacements and folding of entire tissues and organ primordia. One of the emergent processes we study is the de novo formation of primary vascular networks, a system in which there is little or no evidence for the presence of a genetically encoded pre‐pattern. Emergent morphogenetic behavior is also required for formation of a midline heart. In amniotes the primitive heart forms out of coherent planar sheets of tissue. Our data show that heart precursors do not “migrate” from lateral positions towards the future site of the midline heart. Instead, cells of the mesodermal and endodermal layers appear to generate traction forces, and the resulting stresses, together with controlled relaxation, drives large‐scale tissue movements.