Gene expression noise can promote the fixation of beneficial mutations in fluctuating environments

Abstract

Nongenetic phenotypic variation can either speed up or slow down adaptive evolution. We show that it can speed up evolution in environments in which available carbon and energy sources change over time. To this end, we use an experimentally validated model of Escherichia coli growth on two alternative carbon sources, glucose and acetate. On the superior carbon source (glucose), all cells achieve high growth rates, while on the inferior carbon source (acetate) only a small fraction of the population manages to initiate growth. Consequently, populations experience a bottleneck when the environment changes from the superior to the inferior carbon source. Growth on the inferior carbon source depends on a circuit under the control of a transcription factor that is repressed in the presence of the superior carbon source. We show that noise in the expression of this transcription factor can increase the probability that cells start growing on the inferior carbon source. In doing so, it can decrease the severity of the bottleneck and increase mean population fitness whenever this fitness is low. A modest amount of noise can also enhance the fitness effects of a beneficial allele. It can accelerate the spreading of such an allele, increase its likelihood of going to fixation, and reduce its fixation time. Central to the adaptation-enhancing principle we identify is the ability of noise to mitigate population bottlenecks. Because such bottlenecks are frequent in fluctuating environments, and because fluctuating environments themselves are ubiquitous, this principle may apply to a broad range of environments and organisms. Author summaryIndividuals that grow in the same environment and share the same genes may still differ in their behaviour and their traits. These differences between individuals arise from uncertainty inherent in all biological processes, and they are found in all domains of life. Although this random individual variability is itself short-lived, it still has the potential to shape evolution in the long term. For example, if a population encounters a harsh environment, random (nongenetic) differences between individuals can cause some individuals to cope better with the new environment than others. These rare individuals may give a population an advantage compared to populations with fewer such differences between individuals. Furthermore, if some of these rare individuals carry a beneficial gene variant, the beneficial effect of this gene variant may become amplified, and consequently spread faster in a population with more random variation. Using a realistic model of cell growth, we show that this mechanism not only works in unfavourable environments that are stable, but also in environments that switch back and forth between a favourable and an unfavourable state. Because many natural environments undergo such periodic changes, and because random differences between individuals are ubiquitous, the mechanism we have identified may be widespread in nature.