A Morphoelastic Shell Theory of Biological Invagination in Embryos

The embryo of Volvox globator, a monolayer spheroidal cell sheet, undergoes an inversion to release its flagella during the late stage of its development. This inversion, known as the type-B inversion, initiates from the equator. Other types of inversions also exist, such as the inversion from the anterior pole of Volvox carteri and the bowl-shaped inversion of Pleodorina. These inversions can be regarded as axisymmetric processes, during which complex fold patterns are generated. The invagination of the cell sheet plays a crucial role in embryonic development, and our aim is to understand this process from an interdisciplinary point of view, with a particular focus on the mechanical aspects. In this work, we first develop a morphoelastic shell theory for general deformations of biological shells, incorporating both active and passive biomechanical effects, as well as membrane and bending effects. By means of asymptotic analysis, we establish an analytical framework to study axisymmetric deformations of morphoelastic shells focusing mainly on the membrane effects. For illustrative purposes, we apply this framework to investigate the invagination of Volvox globator embryo. The underlying active stretches driving this process are derived analytically by inverse analysis of experimental data through the morphoelastic shell model. We highlight a two-order remodeling strategy that generates the observed invagination pattern: the Gaussian morphing of the cell sheet creates the first fundamental form of the stress-free folded patterns, while a secondary remodeling generates the membrane tension necessary to balance the external pressure and the second fundamental form of the invaginated pattern. This remodeling strategy unveils the complex interplay between geometry, mechanics, and biological processes during Volvox globator embryogenesis.