The evolutionary emergence of stochastic phenotype switching in bacteria

Abstract

Stochastic phenotype switching - or bet hedging - is a pervasive feature of living systems and common in bacteria that experience fluctuating (unpredictable) environmental conditions. Under such conditions, the capacity to generate variable offspring spreads the risk of being maladapted in the present environment, against offspring likely to have some chance of survival in the future. While a rich subject for theoretical studies, little is known about the selective causes responsible for the evolutionary emergence of stochastic phenotype switching. Here we review recent work - both theoretical and experimental - that sheds light on ecological factors that favour switching types over non-switching types. Of particular relevance is an experiment that provided evidence for an adaptive origin of stochastic phenotype switching by subjecting bacterial populations to a selective regime that mimicked essential features of the host immune response. Central to the emergence of switching types was frequent imposition of 'exclusion rules' and 'population bottlenecks' - two complementary faces of frequency dependent selection. While features of the immune response, exclusion rules and bottlenecks are likely to operate in many natural environments. Together these factors define a set of selective conditions relevant to the evolution of stochastic switching, including antigenic variation and bacterial persistence.

Figure 1

Schematic representation of the dynamics experienced by a population evolving in the face of fluctuating selection wrought by the host immune response. A.) The population is founded by a single (blue) genotype. During the course of growth, rare mutant types arise. B.) At some future moment the environment changes (e.g., the population is detected by the immune system) and common types are eliminated. C.) A single new (red) type avoids detection and proceeds to re-establish the population. A.-C.) The population experiences an ‘exclusion rule’ and passes through a bottleneck. The process is repeated: the red type becomes common, but is eventually detected and eliminated (D.). E.) The population once again passes through a single-cell bottleneck before being re-established from the rare (purple) type. In the face of such selective conditions a type that evolves the capacity to stochastically switch, at high frequency, between phenotypic states, has a clear selective advantage compared to a type that relies on spontaneous mutation to effect the change.