Morphospace analysis reveals divergent cellular behaviours driving tissue internalisation during insect gastrulation

Abstract

During gastrulation, embryonic epithelia undergo large-scale remodelling to internalise the mesoderm. Whether the cellular mechanisms underlying these tissue deformations are conserved across species remains unclear. Using quantitative cell-shape embedding, we compare cellular behaviours underlying gastrulation in two insects. We show that while Drosophila mesoderm cells follow a coordinated shape change sequence during gastrulation, mesoderm cells in the beetle Tribolium display heterogeneous shapes with no clear trajectory. This heterogeneity arises from two distinct internalisation modes: canonical apical constriction-driven tissue invagination, and early internalisation through out-of-plane cell divisions. Interpretable machine learning together with in vivo perturbations identify nuclear crowding as a key predictor of out-of-plane divisions and show that, in both species, proliferation slows tissue folding while promoting individual cell internalisation. Our study showcases morphospace analysis as a powerful tool for dissecting the cellular basis of tissue morphogenesis and reveals a conserved antagonistic relationship between cell divisions and tissue folding during gastrulation.