Expansion of apical extracellular matrix underlies the morphogenesis of a recently evolved structure

One of the fundamental gaps in our knowledge of the evolution of novel structures is understanding how the morphogenetic processes that form these structures arise. Here, we traced the cellular development of a morphological novelty, the posterior lobe of D. melanogaster . We found that this genital outgrowth forms through an extreme increase in cell height. By examining the apical extracellular matrix (aECM), we uncovered a vast network associated with the developing genitalia of lobed and non-lobed species. We observed that cells which will form the posterior lobe show expanded expression of the aECM protein Dumpy which connects them to the ancestral aECM network. Further analysis demonstrated a required role for Dumpy in cell height increase during development. We propose that the aECM presents a rich reservoir for generating morphological novelty, in addition to highlighting a yet unseen role for aECM in regulating extreme cell height.