Cell differentiation can underpin the reproducibility of morphogenesis

Abstract

Morphogenesis of complex body shapes is reproducible despite the noise inherent in the underlying morphogenetic processes. However, how these morphogenetic processes work together to achieve this reproducibility remains unclear. Here, we ask how morphogenetic reproducibility is realised by developing a computational model that evolves complex morphologies. We find that evolved, complex morphologies are reproducible in a sizeable fraction of simulations, despite no direct selection for reproducibility. We show that high reproducibility is caused by segregating moving cells that "shape" morphologies from stationary cells that "maintain" morphologies during morphogenesis. Strikingly, most highly reproducible morphologies also evolved cell differentiation, where proliferative, moving stem cells (i.e., progenitor cells) irreversibly differentiate into non-dividing, stationary differentiated cells. These results suggest that cell differentiation observed in natural development plays a fundamental role in morphogenesis in addition to the production of specialised cell types. This previously-unrecognised role of cell differentiation has major implications for our understanding of how morphologies are generated and regenerated.