The Evolution of Robust Development and Homeostasis in Artificial Organisms

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.

[1]  A. Wagner Robustness, evolvability, and neutrality , 2005, FEBS letters.

[2]  Ronald A. DePinho,et al.  How stem cells age and why this makes us grow old , 2007, Nature Reviews Molecular Cell Biology.

[3]  Andreas Deutsch,et al.  Cellular Automaton Models of Tumor Development: a Critical Review , 2002, Adv. Complex Syst..

[4]  Rustem F. Ismagilov,et al.  Dynamics of Drosophila embryonic patterning network perturbed in space and time using microfluidics , 2005, Nature.

[5]  Andreas Wagner,et al.  Robustness Can Evolve Gradually in Complex Regulatory Gene Networks with Varying Topology , 2007, PLoS Comput. Biol..

[6]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[7]  S. Leibler,et al.  Establishment of developmental precision and proportions in the early Drosophila embryo , 2002, Nature.

[8]  F. Watt Stem cell fate and patterning in mammalian epidermis. , 2001, Current opinion in genetics & development.

[9]  S. Torquato,et al.  Lineal-path function for random heterogeneous materials. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[10]  G. Zant,et al.  Stem cells, aging, and cancer: inevitabilities and outcomes , 2004, Oncogene.

[11]  S. Leibler,et al.  Precise domain specification in the developing Drosophila embryo. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[12]  Brian Stramer,et al.  Wound healing and inflammation: embryos reveal the way to perfect repair. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[13]  M. Longaker,et al.  Scar formation: the spectral nature of fetal and adult wound repair. , 1996, Plastic and reconstructive surgery.

[14]  A. Spradling,et al.  The Mother of All Stem Cells? , 2007, Science.

[15]  G B Ermentrout,et al.  Cellular automata approaches to biological modeling. , 1993, Journal of theoretical biology.

[16]  S Torquato,et al.  Cellular automaton of idealized brain tumor growth dynamics. , 2000, Bio Systems.

[17]  Michael P. Murphy,et al.  What is life? : the next fifty years : speculations on the future of biology , 1995 .

[18]  C. Nüsslein-Volhard,et al.  Mutations affecting segment number and polarity in Drosophila , 1980, Nature.

[19]  Rintoul,et al.  Reconstruction of the Structure of Dispersions , 1997, Journal of colloid and interface science.

[20]  S. O'Kane,et al.  Scar-free healing: from embryonic mechanisms to adult therapeutic intervention. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[21]  J. Timmer,et al.  Design principles of a bacterial signalling network , 2005, Nature.

[22]  Heng Liu,et al.  A Biological Development Model for the Design of Robust Multiplier , 2005, EvoWorkshops.

[23]  P. Hogeweg Shapes in the Shadow: Evolutionary Dynamics of Morphogenesis , 1999, Artificial Life.

[24]  Andreas Wagner,et al.  Genetic redundancy caused by gene duplications and its evolution in networks of transcriptional regulators , 1996, Biological Cybernetics.

[25]  Paul Martin,et al.  Wound healing recapitulates morphogenesis in Drosophila embryos , 2002, Nature Cell Biology.

[26]  T. A. Mason,et al.  Use of microstructural statistics in predicting polycrystalline material properties , 1999 .

[27]  P. Bentley,et al.  Investigating the evolvability of biologically inspired CA. , 2004 .

[28]  Salvatore Torquato,et al.  Generating random media from limited microstructural information via stochastic optimization , 1999 .

[29]  J. Miller,et al.  Guidelines: From artificial evolution to computational evolution: a research agenda , 2006, Nature Reviews Genetics.

[30]  Christopher S Potten,et al.  The intestinal epithelial stem cell. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[31]  Paul Martin,et al.  Cell Biology: Master Regulators of Sealing and Healing , 2005, Current Biology.

[32]  Takuji Nishimura,et al.  Mersenne twister: a 623-dimensionally equidistributed uniform pseudo-random number generator , 1998, TOMC.

[33]  L. Rowe,et al.  Natural Selection in a Bottle , 2002, The American Naturalist.

[34]  A. Spradling,et al.  The stem cell niche: theme and variations. , 2004, Current opinion in cell biology.

[35]  Lewis Wolpert,et al.  Principles of Development , 1997 .

[36]  J. Miller,et al.  15 – Evolving the program for a cell: from French flags to Boolean circuits , 2003 .

[37]  Paul Martin,et al.  Parallels between tissue repair and embryo morphogenesis , 2004, Development.

[38]  M. Ferguson,et al.  Ontogeny of the skin and the transition from scar-free to scarring phenotype during wound healing in the pouch young of a marsupial, Monodelphis domestica. , 1995, Developmental biology.

[39]  Diego Federici,et al.  Evolution and Development of a Multicellular Organism: Scalability, Resilience, and Neutral Complexification , 2006, Artificial Life.

[40]  Peter J. Bentley,et al.  Evolving and growing microstructures of using biologically inspired CA , 2004, Proceedings. 2004 NASA/DoD Conference on Evolvable Hardware, 2004..

[41]  P. Bentley,et al.  Using genetic algorithms to evolve three-dimensional microstructures from two-dimensional micrographs , 2005 .