The evolutionary origins of gene regulation

Abstract

One way that organisms cope with constantly changing physical and biological conditions is by regulating the expression of genes and thereby altering protein production. Clearly, altering the protein production to match the environmental demands can be adaptive, but there may be evolutionary barriers to the transition from constitutive expression to regulated expression. In particular, down-regulating a gene when it is not needed means that there will necessarily be a delay in protein production when the protein is up-regulated in the future. We develop a model of simple gene regulation in response to randomly changing environmental conditions. We calculate the long-term behavior of gene expression and determine the fitness consequences of changes in the gene regulation. We then embed this model into a population genetic framework in order to determine the conditions that allow populations to evolve environment-specific transcription rates. The population genetic model follows the evolutionary transition from constitutive expression to regulated expression. There are three distinct possible evolutionary outcomes. The gene may be stuck in the always on position, the gene may first evolve to an intermediate constitutive expression level and then evolve regulation, or regulation can evolve directly from the ancestral state in a smooth fashion. Regulation is most likely to evolve when the costs of mis-expression are low and the transcript decay rate is high. This suggests that genes that have less severe reductions in fitness when mis-expressed are more likely to initially evolve regulation.