Dynamics of morphogenesis
Morphogenesis refers to the early development of shape in embryos. In the early stage an embryo consists of just a few fundamental cell types, which are orchestrated such that after some time a highly complex organism develops. Over time the initially few cell types differentiate to a large variety of cells that form together with polymers and minerals all kinds of tissues (connective, muscle, nervous and epithelial tissue). Each tissue type performs a specific biological role for the organism and none could function on its own. From a physics perspective each tissue exhibits very different mechanical and chemical properties. An example is cartilage or bone, which are significantly stiffer than epithelial or muscle tissue. In the early embryo these difference in degree of physical and chemical properties had to develop first from a mixture of just a few cell types.
Together with Prof. L. Mahadevan (Harvard University) we are interested in the question of how a soft tissue hardens during embryogenesis. As an example we consider the condensation of cartilage during the early limb bud development. In particular, we focus on the change of mechanical properties and how they relate to the shape dynamics of the limb bud.
Biological systems are distinguished by the presence of active stresses which can affect their physical properties and alter their stability. For example, active stresses give rise to collectively moving streaks and clusters, rotating ring, swirl or aster-like patterns, or the remodelling of cell-to-cell junctions in living tissues. These systems are typically described as a single phase with active stresses that drive the assembly of the constituents and the properties of the phases are typically assumed as liquid-like or even gases.
However many active material cannot be treated as fluids. Examples include cartilage, bone, tissues in early development, and superprecipitated systems such as networks of filaments connected by crosslinks and molecular motors. The presence of activity in these systems can drive the macroscopic contraction of gels, the compaction of cells during the condensation of cartilage cells, the network formation of osteoblasts during skull closure in embryos, and the formation of furrows in tissues. This requires the augmentation of previous passive biphasic descriptions, such as associated with poroelasticity to account for active stress regulation and diffusion in cells and tissues. While recent work has included activity in a poroelastic description, the material was assumed to be homogeneous and stable despite active stress generation in one of the phases. Here we question this assumption of stability of an active mixture composed of two phases with different mechanical properties, and ask under what physical conditions an active poroelastic material might contract/condense or disintegrate/fragment, a phenomenon seen in a variety of experimental systems.
In a collboration with Chris H. Rycroft we found that differential activity between the solid and fluid phases that constitute an initially homogeneneous poroelastic medium can drive a mechanical instability leading to the demixing of a homogeneous medium into condensed solid-like patches that arise due to macroscopic contraction, reminiscent of observations in superprecipitated gels and compacted cells in tissues. Depending on the rate and ability of transport of material and stress in the biphasic material, we find both uniformly growing and pulsatile instabilities leading to assembling, disassembling and drifting solid-like clusters that undergo fusion and fission (see movies below).