Pre-patterned epithelial invagination prevents mechanical instability during fly gastrulation

The cephalic furrow is a deep epithelial fold that demarcates the head–trunk boundary of fly embryos during gastrulation. It forms under strict genetic control using active cellular mechanisms and follows an invariant morphogenetic sequence. But unlike other embryonic invaginations, the cells that invaginate in the cephalic furrow do not give rise to any precursor tissues or larval traits. The cephalic furrow is transient and unfolds leaving no trace. For these reasons, its function during development has remained elusive. Here we show that the cephalic furrow plays a mechanical role duringDrosophilagastrulation. By live-imaging mutant embryos, we find that without the cephalic furrow, ectopic folds appear around the head–trunk interface indicating that the epithelial stability has been compromised. Usingin vivoperturbations andin silicosimulations, we demonstrate that ectopic folding in cephalic furrow mutants occurs due to the concomitant formation of mitotic domains and extension of the germ band. These events increase the tissue strain in the head–trunk interface giving rise to mechanical instabilities. Further, we show by simulations that an early pre-patterned invagination can effectively prevent the build-up of compressive stresses by retaining epithelial tissue out-of-plane before other morphogenetic movements take place. Our findings suggest the cephalic furrow absorbs compressive stresses at the head–trunk boundary during fly gastrulation, and raise the hypothesis that mechanical forces may have played a role in the evolution of the cephalic furrow.