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Evolutionary dimension reduction in phenotypic space

In general, cellular phenotypes, as measured by concentrations of cellular components, involve large degrees of freedom. However, recent measurement has demonstrated that phenotypic changes resulting from adaptation and evolution in response to environmental changes are effectively restricted to a low-dimensional subspace. Thus, uncovering the origin and nature of such a drastic dimension reduction is crucial to understanding the general characteristics of biological adaptation and evolution. Herein, we first formulated the dimension reduction in terms of dynamical systems theory: considering the steady growth state of cells, the reduction is represented by the separation of a few large singular values of the inverse Jacobian matrix around a fixed point. We then examined this dimension reduction by numerical evolution of cells consisting of thousands of chemicals whose concentrations determine phenotype. As a result of the evolution, phenotypic changes due to mutations and external perturbations were found to be mainly restricted to a one-dimensional subspace. One singular value of the inverse Jacobian matrix at a fixed point of concentrations was significantly larger than the others. The major phenotypic changes due to mutations and external perturbations occur along the corresponding left-singular vector, which leads to phenotypic constraint, and fitness dominantly changes in the same direction. Once such phenotypic constraint is acquired, phenotypic evolution to a novel environment takes advantage of this restricted phenotypic direction. This results in the convergence of phenotypic pathways across genetically different strains, as is experimentally observed, while accelerating further evolution.