Emergence and robustness of 3D complex tissue architectures from simple physical forces

Although at central stake in biology and biological engineering, our understanding of how biological tissues acquire their architectures during morphogenesis and which mechanisms have been selected through evolution remain limited. Using adipose tissue as a biological model, we build a 3D mathematical model with simple mechanical rules between cells and fibers, and show that the model reproduces, in-silico, not only the emergence of complex and heterogeneous 3D architectures, but also the intra and inter-individual heterogeneities of shapes as observed in vivo. The model reveals that specific rules for cell differentiation are not necessary for tissue structuring, but could have been selected through evolution for robustness and efficiency. This study therefore suggests a paradigm shift where tissue architecture is an emerging process surprisingly more driven by mechanical processes than by complex predetermined molecular or genetic programs.