Premier Presentation: Aggression and metabolism in hybrid honey bees is linked to allele specific expression

Hybrids of docile European bees (Apis mellifera carnica) and aggressive Africanized bees (primarily A.m. scutellata) exhibit asymmetric levels of aggression and metabolic capacity in the reciprocal hybrids; those with European maternity (EA family) are extremely aggressive and have low metabolic rates while those with Africanized maternity (AE) do not exhibit these extremes. Previous work demonstrated that low brain metabolism is causal to high aggression in bees. We set out to test whether these asymmetric hybrid effects may be tied to one another through asymmetric allele expression (maternal versus paternal) by sequencing the transcriptomes of F1 hybrid bees from both families. We found evidence for over 500 genes preferentially using one allele and over 200 of these are asymmetrically biased toward the maternal allele only in the EA family, mirroring the hybrid phenotypic asymmetry. These asymmetrically biased genes are enriched for mitochondrial localizing genes and are enriched in loci that are associated with defensive traits in these hybrids. Additionally, GO term analysis indicates that these genes are associated with behavior as well as neurogenesis, a process that may be tied to the metabolic shift in aggressive bees. This gene set contains many genes related to metabolic shifts as well genes involved in the piRNA pathway. This pathway regulates gene transcription through sequence-specific chromatin modifications and we find two large clusters in which every testable gene is highly maternally biased (~90%), potentially implicating chromatin changes in this bias. These results indicate that asymmetric allele usage may underlie the aggression in the EA family by altering metabolism through mitochondrial retrograde signaling. We propose that bees normally utilize the piRNA pathway to modulate aggression through brain metabolism shifts and that our crossing scheme resulted in a hijacking of this mechanism in the EA family due to differential selection for aggression in the parent lineages.