SUMMARY 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.

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SUMMARYInformation flow through neural circuits is continuously modified by context-dependent learning. In the nematode Caenorhabditis elegans, pairing specific odors with food deprivation results in aversion to the odor. Here we identify cell-specific mechanisms of insulin/IGF receptor signaling that integrate sensory information with food context during aversive olfactory learning. Using FLP::FRT recombination of an endogenously targeted locus, we show that aversive learning to butanone, an odor sensed only by the AWCON olfactory neuron, requires the insulin/IGF receptor DAF-2 in AWCON. Learning requires an axonally-localized DAF-2c isoform and the insulin receptor substrate (IRS) protein IST-1, and is partly independent of the FoxO transcription factor DAF-16. Food deprivation, the unconditioned stimulus for learning, increases DAF-2 expression post-transcriptionally through an insulin- and ist-1-dependent process. Aversive learning suppresses odor-regulated glutamate release from the AWCON axon in wild-type animals but not in ist-1 mutants, suggesting that insulin signaling drives presynaptic depression to generate an aversive memory.