During embryogenesis, multicellular animals are shaped via cell proliferation, cell rearrangement, and apoptosis. At the end of development, tissue architecture is then maintained through balanced rates of cell proliferation and loss. Here, we take an in silico approach to look for generic systems features of morphogenesis in multicellular animals that arise as a consequence of the evolution of development. Using artificial evolution, we evolved cellular automata-based digital organisms that have distinct embryonic and homeostatic phases of development. Although these evolved organisms use a variety of strategies to maintain their form over time, organisms of different types were all found to rapidly recover from environmental damage in the form of wounds. This regenerative response was most robust in an organism with a stratified tissue-like architecture. An evolutionary analysis revealed that evolution itself contributed to the ability of this organism to maintain its form in the face of genetic and environmental perturbation, confirming the results of previous studies. In addition, the exceptional robustness of this organism to surface injury was found to result from an upward flux of cells, driven in part by cell divisions with a stable niche at the tissue base. Given the general nature of the model, our results lead us to suggest that many of the robust systems properties observed in real organisms, including scar-free wound-healing in well-protected embryos and the layered tissue architecture of regenerating epithelial tissues, may be by-products of the evolution of morphogenesis, rather than the direct result of selection.
During development, multicellular animals are shaped by cell proliferation, cell rearrangement, and cell death to generate an adult whose form is maintained over time. Disruption of this finely balanced state can have devastating consequences, including aging, psoriasis, and cancer. Typically, however, development is robust, so that animals achieve the same final form even when challenged by environmental damage such as wounding. To see how morphogenetic robustness arises, we have taken an in silico approach to evolve digital organisms that exhibit distinct phases of growth and homeostasis. During the homeostasis period, organisms were found to use a variety of strategies to maintain their form. Remarkably, however, all recovered from severe wounds, despite having evolved in the absence of selection pressure to do so. This ability to regenerate was most striking in an organism with a tissue-like architecture, where it was enhanced by a directional flux of cells that drives tissue turnover. This identifies a stratified architecture, like that seen in human skin and gut, as an evolutionarily accessible and robust form of tissue organisation, and suggests that wound-healing may be a general feature of evolved morphogenetic systems. Both may therefore contribute to homeostasis, wound-healing, and regeneration in real animals.