Abstract

The fruit fly wing develops from an epithelium called the imaginal disc, which grows continuously during fly larval development. At the start of the pupal development phase it everts and forms a double layered pupal wing. Large scale tissue flows reshape the pupal wing over ~16 hours of pupal morphogenesis. How do cellular processes and mechanical stresses lead to the proper reshaping of the wing and how does a shape defect arise in a dumpy mutant wing? We observe the dorsal wing layer during pupal morphogenesis in vivo. Imaging the tissue at cellular resolution allows us to track individual cells in time and space and to identify different cellular processes: cell division, cell extrusion and T1 transitions. We calculate the contributions of these cellular processes to the overall tissue shape changes using the Triangle Method. Furthermore, we develop a hydrodynamic theory to relate tissue stresses to tissue deformations and cell shape changes [Etournay et al. eLife e07090; Etournay et al. eLife e14334; Merkel et al., arXiv:1607.00357; Popovic et al., https://arxiv.org/abs/1607.03304]. We find that at the early times of pupal morphogenesis blade cells elongate more than the blade tissue itself due to active T1 transitions acting to increase the cell elongation. In the context of the hydrodynamic theory we describe the shear flow contribution from the T1 transitions as a linear function of cell elongation with an exponential memory kernel. These memory effects produce a tissue rheology that differs from the standard Maxwell viscoelastic material by an effective inertial element and can lead to damped oscillations in the tissue. Finally, we construct a simple model of the pupal wing morphogenesis and we find that the misshaped dumpy mutant wing can be understood as the wild type wing tissue with compromised boundary attachments to the surrounding cuticle.