Genomic regions influencing aggressive behavior in honey bees are defined by colony allele frequencies

For social animals, the genotypes of group members affect the social
environment, and thus individual behavior, often indirectly. We used
genome-wide association studies (GWAS) to determine the influence of
individual vs. group genotypes on aggression in honey bees. Aggression in
honey bees arises from the coordinated actions of colony members,
primarily nonreproductive “soldier” bees, and thus, experiences
evolutionary selection at the colony level. Here, we show that individual
behavior is influenced by colony environment, which in turn, is shaped by
allele frequency within colonies. Using a population with a range of
aggression, we sequenced individual whole genomes and looked for
genotype–behavior associations within colonies in a common environment.
There were no significant correlations between individual aggression and
specific alleles. By contrast, we found strong correlations between colony
aggression and the frequencies of specific alleles within colonies,
despite a small number of colonies. Associations at the colony level were
highly significant and were very similar among both soldiers and foragers,
but they covaried with one another. One strongly significant association
peak, containing an ortholog of the Drosophila sensory gene dpr4 on
linkage group (chromosome) 7, showed strong signals of both selection and
admixture during the evolution of gentleness in a honey bee population. We
thus found links between colony genetics and group behavior and also,
molecular evidence for group-level selection, acting at the colony level.
We conclude that group genetics dominates individual genetics in
determining the fatal decision of honey bees to sting.