Balancing selection shapes density-dependent foraging behavior

The optimal foraging strategy in a given environment depends on the number of competing individuals and their behavioral strategies. Little is known about the genes and neural circuits that integrate social information into foraging decisions. Here we show that ascaroside pheromones that signal population density suppress exploratory foraging in Caenorhabditis elegans, and that heritable variation in this behavior generates alternative foraging strategies. Natural C. elegans isolates differ in their sensitivity to the potent ascaroside icas#9 (IC-asc-C5). A quantitative trait locus (QTL) for icas#9 sensitivity includes srx-43, a G protein-coupled icas#9 receptor; srx-43 acts in ASI sensory neurons to suppress exploration. Two ancient haplotypes associated with this QTL confer competitive growth advantages that depend on ascaroside secretion, its detection by srx-43, and the distribution of food. These results suggest that balancing selection at the srx-43 locus generates alternative density-dependent behaviors, fulfilling a prediction of foraging game theory.