Direction and Constraint in Phenotypic Evolution: Dimension Reduction and Global Proportionality in Phenotype Fluctuation and Responses

TL;DR

This paper develops a macroscopic theory linking cellular phenotypic states, their robustness, and evolution, demonstrating that phenotypic changes are constrained within a low-dimensional manifold and showing proportional responses to genetic and environmental changes.

Contribution

The study introduces a macroscopic framework connecting phenotypic robustness, evolution, and fluctuation, highlighting the role of slow modes in high-dimensional phenotypes.

Findings

Phenotypes during steady-growth are confined to a low-dimensional slow manifold.

Proportionality exists between phenotypic responses to genetic and environmental changes.

Robustness to noise and mutation is linked through developmental dynamics.

Abstract

A macroscopic theory for describing cellular states during steady-growth is presented, which is based on the consistency between cellular growth and molecular replication, as well as the robustness of phenotypes against perturbations. Adaptive changes in high-dimensional phenotypes were shown to be restricted within a low-dimensional slow manifold, from which a macroscopic law for cellular states was derived, which was confirmed by adaptation experiments on bacteria under stress. Next, the theory was extended to phenotypic evolution, leading to proportionality between phenotypic responses against genetic evolution and environmental adaptation. The link between robustness to noise and mutation, as a result of robustness in developmental dynamics to perturbations, showed proportionality between phenotypic plasticity by genetic changes and by environmental noise. Accordingly, directionality and constraint in phenotypic evolution was quantitatively formulated in terms of phenotypic fluctuation and the response against environmental change. The evolutionary relevance of slow modes in controlling high-dimensional phenotypes is discussed.