Individual Variation in Pheromone Response Correlates with Reproductive Traits and Brain Gene Expression in Worker Honey Bees

BACKGROUND: Variation in individual behavior within social groups can affect the fitness of the group as well as the individual, and can be caused by a combination of genetic and environmental factors. However, the molecular factors associated with individual variation in social behavior remain relatively unexplored. We used honey bees (Apis mellifera) as a model to examine differences in socially-regulated behavior among individual workers, and used transcriptional profiling to determine if specific gene expression patterns are associated with these individual differences. In honey bees, the reproductive queen produces a pheromonal signal that regulates many aspects of worker behavior and physiology and maintains colony organization. METHODOLOGY/PRINCIPAL FINDINGS: Here, we demonstrate that there is substantial natural variation in individual worker attraction to queen pheromone (QMP). Furthermore, worker attraction is negatively correlated with ovariole number—a trait associated with reproductive potential in workers. We identified transcriptional differences in the adult brain associated with individual worker attraction to QMP, and identified hundreds of transcripts that are organized into statistically-correlated gene networks and associated with this response. CONCLUSIONS/SIGNIFICANCE: Our studies demonstrate that there is substantial variation in worker attraction to QMP among individuals, and that this variation is linked with specific differences in physiology and brain gene expression patterns. This variation in individual response thresholds may reveal underlying variation in queen-worker reproductive conflict, and may mediate colony function and productivity by creating variation in individual task performance.