Pulling Through: A Biomechanical Analysis of Normal and Aberrant Embryogenesis in Drosophila

Abstract

Biomechanical analysis of the developing Drosophila embryo has historically focused on the role of individual cells. Cells translate genetic information into protein machinery that is capable of generating forces. With this perspective, the field has tried to identify which cells are responsible for the morphological changes that occur during embryogenesis. Taking a different perspective, this work considers the cumulative effect of all cells in a coherent epithelium. This reveals a mechanical trade-off between cell-type dependent tensions and embryo-imposed constraints on cells. To investigate this further, a 2.5-D cellular finite element model is built and used to analyze the mechanics of one stage of development, germband retraction. This analysis finds that germband retraction is robust to cell-type dependent tensions, but contingent on the initial cell geometry. Experiments then test the embryo’s mechanical robustness to environmental perturbation. A non-specific heat shock stress to the embryo results in delayed development and the formation of holes in the epithelium. These holes disrupt the mechanical integrity of the tissue preventing development beyond germband retraction. The model is expanded to explain how germband retraction fails, thus providing a mechanical explanation for failure due to holes in heat-shocked embryos. This dissertation finds that embryogenesis is a mechanically robust process that is not dependent on any single group of differentiated cells, but rather is contingent on coherent and contiguous epithelial tissues that maintain developmental information through cell morphology.