Beyond conflict: kinship theory of intragenomic conflict predicts individual variation in altruistic behavior

Studies of the genetic basis of behavioral variation have emphasized gene cooperation within networks, often overlooking gene conflicts. The Kinship Theory of Intragenomic Conflict (KTIC) proposes that conflicts can occur within genes when parent-specific alleles have different strategies for maximizing reproductive fitness. Here, we test a prediction of the KTIC – that selection should favor alleles which promote “altruistic” behaviors that support the reproductive fitness of kin. In honey bee (Apis mellifera) colonies, workers act altruistically when tending to the queen by performing a “retinue” behavior, distributing the queen’s mandibular pheromone (QMP) throughout the hive. Workers exposed to QMP do not activate their ovaries, ensuring they care for the queen’s brood instead of competing to lay unfertilized eggs. Thus, the KTIC predicts that response to QMP should be favored by the maternal genome. Using a reciprocal cross design, we tested for parent-of-origin effects on the workers’ 1) responsiveness to QMP, 2) ovary activation, and 3) brain transcriptome. We hypothesized that QMP-responsive workers have smaller and less active ovaries, influenced by the workers’ parent-of-origin. With an allele-specific transcriptomic analysis, we tested whether QMP-responsive workers show enriched maternal allele-biased gene expression compared to QMP-unresponsive workers. Finally, we explored how parent-of-origin gene expression patterns are associated with overall gene expression patterns and regulatory networks. We report evidence in support of the KTIC for the retinue behavior and associated conflicts within gene networks. Our study provides new insights into the genetic basis of behavior and the potential for behavioral variation influenced by intragenomic conflict.