Patterned invagination prevents mechanical instability during gastrulation

Abstract

Mechanical forces are crucial for driving and shaping tissue morphogenesis during embryonic development^1,2,3. However, their relevance for the evolution of development remains poorly understood⁴. Here we show that an evolutionary novelty of fly embryos—the patterned embryonic invagination known as the cephalic furrow^5,6,7—has a mechanical role during Drosophila gastrulation. By integrating in vivo experiments and in silico simulations, we demonstrate that the head–trunk boundary of the embryo is under increased compressive stress due to the concurrent formation of mitotic domains and germ band extension and that the cephalic furrow counteracts these stresses, preventing mechanical instabilities during gastrulation. Then, by comparing the genetic patterning of species with and without the cephalic furrow, we find evidence that changes in the expression of the transcription factor buttonhead are associated with the evolution of the cephalic furrow. These results suggest that the cephalic furrow may have evolved through the genetic stabilization of morphogenesis in response to the mechanical challenges of dipteran gastrulation. Together, our findings uncover empirical evidence for how mechanical forces can influence the evolution of morphogenetic innovations in early development.