Periodic Reporting for period 3 - EVOMORPHYS (Identifying how Evolution exploits physical properties of tissues to generate the complexity and diversity of Life)
Reporting period: 2022-08-01 to 2024-01-31
The present project focuses on one of the most important questions in biology: what are the fundamental drivers of morphological complexity and diversity of Life? I will identify the fundamental principles that rule how Evolution manipulates and exploits the physical properties of living matter to generate the complexity and diversity of Life. Using a combination of mathematical models, numerical simulations, as well as physical and biological experiments, I will investigate how the evolutionary process explores the phase space of possible interactions between physical and biological mechanisms, and produces functional phenotypes. The core of my project consists in testing / quantifying the power and limitations of natural selection and stochastic evolutionary principles in generating shapes and forms under the fundamental constraints of physics. Evolution is the creative engine, but we need to decipher how physical processes take part in this creativity.
We have developed a computer model for numerical simulations in 3D on realistic lizard skin geometries. This has allowed us to demonstrate that (i) skin thickness variation on its own is sufficient to cause scale-by-scale coloration and cellular automata (CA) dynamics, (ii) this phenomenon is robust to variations of the model, and (iii) animal growth affects the scale-colour flipping dynamics by causing a substantial decrease of the relative length scale of the labyrinthine colour pattern of the lizard skin. These results have been published in 2021 (Reaction-diffusion in a growing 3D domain of skin scales generates a discrete cellular automaton - Fofonjka & Milinkovitch - Nature Communications 12 : 2433 (2021)). We also developed a new mathematical model of scale-by-scale colour change based on the Lenz-Ising model. We recently published this work in Physical Review Letters, i.e. the world’s premier physics letter journal. This article (Lizard Skin Patterns and the Ising Model - Zakany, Smirnov and Milinkovitch - Phys. Rev. Lett. 128, 048102 (2022)) has been highlighted by the American Physical Society and the media.
Despite the elegance of Alan Turing’s reaction-diffusion (RD) model, its relevance for the precise description of morphogenesis in real organisms is largely disputed. We will investigate if subtle color sub-clustering predicted by the theoretical model are detectable in real lizards using hyperspectral imaging and extensive histological analyses. If these predictions are confirmed, these data will show that subtle mesoscopic properties of biological dynamical systems, as well as some of the underlying microscopic features, are captured by simple RD models without integrating the unmanageable profusion of variables at lower scales. In addition, we will investigate if the various stochastic (CA and Lenz-Ising) and RD models of patterning can be generalized to five species, belonging to five divergent lineages, exhibiting largely different adult patterns, and all exhibiting dynamics of post-hatching scale-by-scale color change. Taking advantage of their constitutive or effective spatial discretization, we will compare the respective efficiencies of Lenz-Ising, sCA, 2D-dRD, 2D-cRD, and 3D-cRD mathematical models to predict both actual patterns and their statistical attributes. Furthermore, we will develop a mechanical model to predict folding patterns in the developing skin of crocodiles and combine it with RD to produce an extensive model integrating signaling and mechanics. This biophysical model will constitute a powerful tool for predicting how evolution produces functional phenotypes.