The inheritance of process: a dynamical systems approach

A central unresolved problem of evolutionary biology concerns the way in which evolution at the genotypic level relates to the evolution of phenotypes. This genotype-phenotype map involves developmental and physiological processes, which are complex and not well understood. These processes co-determine the rate and direction of adaptive change by shaping the distribution of phenotypic variability on which selection can act. In this study, we argue-expanding on earlier ideas by Goodwin, Oster, and Alberch-that an explicit treatment of this map in terms of dynamical systems theory can provide an integrated understanding of evolution and development. We describe a conceptual framework, which demonstrates how development determines the probability of possible phenotypic transitions-and hence the evolvability of a biological system. We use a simple conceptual model to illustrate how the regulatory dynamics of the genotype-phenotype map can be passed on from generation to generation, and how heredity itself can be treated as a dynamic process. Our model yields explanations for punctuated evolutionary dynamics, the difference between micro- and macroevolution, and for the role of the environment in major phenotypic transitions. We propose a quantitative research program in evolutionary developmental systems biology-combining experimental methods with mathematical modeling-which aims at elaborating our conceptual framework by applying it to a wide range of evolving developmental systems. This requires a large and sustained effort, which we believe is justified by the significant potential benefits of an extended evolutionary theory that uses dynamic molecular genetic data to reintegrate development and evolution.