Drift in Individual Behavioral Phenotype as a Strategy for Unpredictable Worlds

Abstract

Individuals, even with matched genetics and environment, show substantial phenotypic variability. This variability may be part of a bet-hedging strategy, where populations express a range of phenotypes to ensure survival in unpredictable environments. In addition to phenotypic variability between individuals ("bet-hedging"), individuals also show variability in their behavioral phenotype across time, even absent obvious external cues. There are few evolutionary theories that explain random shifts in phenotype across an animals life, which we term phenotypic drift. We use individuality in locomotor handedness in Drosophila melanogaster to characterize both bet-hedging and drift. We use a continuous circling assay to show that handedness spontaneously changes over timescales ranging from seconds to the lifespan of a fly. We compare the amount of behavioral drift and bet-hedging across a number of different fly strains and show independent strain-specific differences in bet-hedging and behavioral drift. We show manipulation of serotonin changes the rate of behavioral drift, indicating a potential circuit substrate controlling behavioral drift. We then develop a theoretical framework for assessing the adaptive value of phenotypic drift, demonstrating that drift may be adaptive for populations subject to selection pressures that fluctuate on timescales similar to the lifespan of an animal. We apply our model to real-world environmental signals and find patterns of fluctuations that favor random drift in behavioral phenotype, suggesting that drift may be adaptive under some real-world conditions. These results demonstrate that behavioral drift plays a role in driving variability in a population and may serve an adaptive role distinct from population level bet-hedging. Significance StatementWhy do individuals animals spontaneously change their preferences over time? While stable idiosyncratic behavioral preferences have been proposed to help species survive unpredictable environments as part of a bet-hedging strategy, the role of intraindividual shifts in preferences is unclear. Using Drosophila melanogaster, we show the stability of individual preferences is influenced by genetic background and neuromodulation, and is therefore a regulated phenomenon. We use theoretical modeling to show that shifts in preferences may be adaptive to environments that change within an individuals lifespan, including many real-world patterns of environmental fluctuations. Together, this work suggests that the stability of individual preferences may affect the survival of species in unpredictable worlds -- understanding that may be increasingly important in the face of anthropogenic change.