Growth-lag tradeoff explains phenotypic heterogeneity in fluctuating environments

Microbial populations in natural environments face fluctuating conditions that challenge their survival and growth. These shifts can involve transitions from environments where cells rely on fermentation, to conditions requiring respiration. Adjusting to these changes is not immediate, leading to a lag phase where cells reorganize their proteome to adapt. At the individual cell level, there is a physiological tradeoff - faster growth in sugar-rich environments versus a shorter lag phase following sugar depletion. This tradeoff shapes the population’s growth dynamics, as individual strategies strongly influence overall performance. Experiments in yeast show that populations adopt diverse strategies: some cells grow quickly during fermentation but experience longer lags, while others grow slower but with a shorter lag phase. We have developed a theoretical framework that explains how two distinct states – “arrestors” and “recoverers” – can jointly emerge as an optimal collective strategy to maximize long-term population growth. We show that this two-strategy solution depends strongly on the physiological tradeoff between the cell growth rate and lag duration. Our framework is general and extends to other scenarios, such as populations cycling between favorable and lethal conditions.