Phenotypic heterogeneity in lag reflects an evolutionarily stable bet-hedging strategy

Area of Science:

• Microbiology
• Evolutionary Biology
• Systems Biology

Background:

• Single-cell yeast experiments reveal two heritable phenotypes: 'arresters' (non-growing) and 'recoverers' (delayed growth) under adverse conditions.
• The coexistence of these phenotypes is a robust phenomenon, but its evolutionary stability and fitness implications were unclear.

Purpose of the Study:

• To determine if a mixed strategy of arresters and recoverers represents an evolutionarily stable strategy in yeast.
• To identify the optimal distribution of phenotypes that maximizes long-term population fitness in fluctuating environments.
• To elucidate the physiological basis for the growth-lag trade-off favoring phenotypic heterogeneity.

Main Methods:

• A dynamic programming framework was used to model fitness-maximizing phenotype distributions in stochastically switching environments.
• A minimal model integrating metabolism, growth, and enzyme allocation was developed to explain the physiological origins of the growth-lag trade-off.

Main Results:

• A heterogeneous strategy combining both arrester and recoverer phenotypes maximizes long-term population fitness across various growth-lag trade-offs.
• The study identified a power-law growth-lag trade-off that favors phenotypic heterogeneity.
• A predicted relationship between the fraction of recoverers and their lag time was observed in wild yeast strains and evolved isolates.

Conclusions:

• Phenotypic heterogeneity, comprising both arresters and recoverers, is an evolutionarily advantageous strategy for yeast in changing environments.
• The findings suggest an evolutionary 'rheostat' mechanism enabling rapid adaptation to environmental shifts.