Abstract

Understanding, predicting, and controlling the phenotypic consequences of genetic and environmental change is essential to many areas of fundamental and applied biology. In evolutionary biology, the generative process of development is a major source of organismal evolvability that constrains or facilitates adaptive change by shaping the distribution of phenotypic variation that selection can act upon. While the complex interactions between genetic and environmental factors during development may appear to make it impossible to infer the consequences of perturbations, the persistent observation that many perturbations result in similar phenotypes indicates that there is a logic to what variation is generated. Here, we show that a general representation of development as a dynamical system can reveal this logic. We build a framework that allows predicting the phenotypic effects of perturbations, and conditions for when the effects of perturbations of different origins are concordant. We find that this concordance is explained by two generic features of development, namely the dynamical dependence of the phenotype on itself and the fact that all perturbations must affect the developmental process to have an effect on the phenotype. We apply our theoretical framework to classical models of development and show that it can be used to predict the evolutionary response to selection using information of plasticity and to accelerate evolution in a desired direction. The framework we introduce provides a way to quantitatively interchange perturbations, opening an avenue of perturbation design to control the generation of variation.

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