Experimental evolution of bet hedging

Bet hedging—stochastic switching between phenotypic states1–3— is a canonical example of an evolutionary adaptation that facilitates persistence in the face of fluctuating environmental conditions. Although bet hedging is found in organisms ranging frombacteria to humans4–10, direct evidence for an adaptive origin of this behaviour is lacking11. Here we report the de novo evolution of bet hedging in experimental bacterial populations. Bacteria were subjected to an environment that continually favoured new phenotypic states. Initially, our regime drove the successive evolution of novel phenotypes by mutation and selection; however, in two (of 12) replicates this trend was broken by the evolution of bet-hedging genotypes that persisted because of rapid stochastic phenotype switching. Genome re-sequencing of one of these switching types revealed ninemutations that distinguished it fromthe ancestor. The final mutation was both necessary and sufficient for rapid phenotype switching; nonetheless, the evolution of bet hedging was contingent upon earliermutations that altered the relative fitness effect of the finalmutation. These findings capture the adaptive evolution of bet hedging in the simplest of organisms, and suggest that riskspreading strategies may have been among the earliest evolutionary solutions to life in fluctuating environments.Editor's Summary 5 November 2009 Dicing with survival: experimental evolution of bet hedging in bacteria If living organisms are to survive, they must cope with ever-changing environments. One solution is the evolution of sensing mechanisms allowing modulation of the phenotype in response to specific cues. A simpler alternative is stochastic or random phenotype switching — 'hedging your bets'. A study of Pseudomonas fluorescens bacteria exposed to a fluctuating regime with similarities to environments such as the vertebrate immune system demonstrates the evolution of bet-hedging behaviour in real time. The P. fluorescens strain evolved the capacity to switch randomly between colony types, ensuring survival in an artificial environment that constantly favoured different colonies. The presence of bet hedging in these simple organisms, and the identification of the mutations involved, show how a changing environment can reward risk-spreading behaviour. Such strategies may have been among the earliest evolutionary solutions to life in fluctuating environments