Beyond the (Geometric) Mean: Stochastic Models Undermine Deterministic Predictions of Bet Hedger Evolution

Abstract

AbstractBet hedging is a ubiquitous strategy for risk reduction in environments that change unpredictably, where a lineage lowers its variance in fitness across environments at the expense of also lowering its arithmetic mean fitness. Classically, the benefit of bet hedging has been quantified using geometric mean fitness (GMF); bet hedging is expected to evolve if and only if it has a higher GMF than the wild type. We build on previous research on the effect of incorporating stochasticity in phenotypic distribution, environment, and reproduction to investigate the extent to which these sources of stochasticity impact the evolution of real-world bet-hedging traits. We demonstrate that modeling stochasticity can alter the sign of selection for bet hedging compared with deterministic predictions. Bet hedging can be deleterious at small population sizes and beneficial at larger population sizes. This phenomenon occurs across parameter space for conservative and diversified bet hedgers. We apply our model to published data to show that incorporating stochasticity is necessary to explain the evolution of real-world bet-hedging traits, including Papaver dubium variable germination phenology, Salmonella typhimurium antibiotic persistence, and seed banking in Clarkia xantiana. Our results suggest that GMF is not enough to predict when bet hedging is adaptive in a wide range of scenarios.

Keywords: bacterial persistence; bet hedging; fluctuating environment; germination phenology; population genetics; stochastic modeling.