Patterned embryonic invagination evolved in response to mechanical instability

Mechanical forces are crucial for driving and shaping tissue morphogenesis during embryonic development, but their relevance for the evolution of development remains poorly understood. Here, we show that a morphogenetic innovation present in fly embryos--a deep epithelial fold known as the cephalic furrow--plays a mechanical role during Drosophila gastrulation. By integrating in vivo experiments and in silico simulations, we find that the formation of the cephalic furrow prevents mechanical instabilities at the head-trunk epithelium by absorbing the compressive stresses generated by concurrent morphogenetic movements of gastrulation, the expansion of mitotic domains and the germ band extension. Furthermore, by comparing the expression of known and novel genes involved in cephalic furrow formation between fly species, we find that the presence of the cephalic furrow is linked to changes in the expression of buttonhead transcription factor at the head-trunk boundary. These data suggest that the genetic control of cephalic furrow formation was established through the integration of a new player into the ancestral head-trunk patterning system, and that mechanical instability may have been the selective pressure associated with the evolution of the cephalic furrow. Our findings uncover empirical evidence for how mechanical forces can influence the evolution of morphogenetic innovations in early development.