In vertebrates, skin colour patterns emerge from nonlinear dynamical microscopic systems of cell interactions. Here we show that in ocellated lizards a quasi-hexagonal lattice of skin scales, rather than individual chromatophore cells, establishes a green and black labyrinthine pattern of skin colour. We analysed time series of lizard scale colour dynamics over four years of their development and demonstrate that this pattern is produced by a cellular automaton (a grid of elements whose states are iterated according to a set of rules based on the states of neighbouring elements) that dynamically computes the colour states of individual mesoscopic skin scales to produce the corresponding macroscopic colour pattern. Using numerical simulations and mathematical derivation, we identify how a discrete von Neumann cellular automaton emerges from a continuous Turing reaction-diffusion system. Skin thickness variation generated by three-dimensional morphogenesis of skin scales causes the underlying reaction-diffusion dynamics to separate into microscopic and mesoscopic spatial scales, the latter generating a cellular automaton. Our study indicates that cellular automata are not merely abstract computational systems, but can directly correspond to processes generated by biological evolution.
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We previously showed that the adult ocellated lizard skin colour pattern is effectively generated by a stochastic cellular automaton (CA) of skin scales. We additionally suggested that the canonical continuous 2D reaction-diffusion (RD) process of colour pattern development is transformed into this discrete CA by reduced diffusion coefficients at the borders of scales (justified by the corresponding thinning of the skin). Here, we use RD numerical simulations in 3D on realistic lizard skin geometries and demonstrate that skin thickness variation on its own is sufficient to cause scale-by-scale coloration and CA dynamics during RD patterning. In addition, we show that this phenomenon is robust to RD model variation. Finally, using dimensionality-reduction approaches on large networks of skin scales, we show that 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.
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