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

Abstract

<jats:p>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 <jats:italic>Drosophila</jats:italic> sensory gene <jats:italic>dpr4</jats:italic> 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.</jats:p>

Honey bee colony aggression and indirect genetic effects

“…The highly significant finding for the colony-level GWAS was surprising, given the n = 9 sample size. This is addressed in Avalos et al (7).…”

“…Avalos et al (7) use the IGE framework as a guide toward finding genes that affect colony-level aggression. Honey bee colonies were collected from Puerto Rican sites and transferred to the University of Puerto Rico field station for acclimation before experiments.…”

“…How can we validate and functionally investigate the role of genetic variants in a group setting? In PNAS, Avalos et al (7) use genome-wide association studies (GWAS) in the eusocial honey bee to uncover genomic regions defined by colony allele frequencies that influence colony aggressive behavior.…”

“…Social experiences can affect different levels of biological organization (e.g., neural transmission, gene expression, and development) acting on different timescales (10). IGEs are found in many species of insects including beetles (11) and the fruit fly (12,13), fire ant (7), and honey bee (6,14); however, a link to group allele frequencies has not been established, and mechanistic studies of IGEs are lacking.…”

The honey bee genome-- what has it been good for?

“…The dance language remains a special challenge for honey bee genomicists; nonetheless; honey bee behavioural genomics has had its share of successes. Numerous honey bee behaviours that can be more readily phenotyped have been studied in detail on a genomic level including pollen foraging (Page Jr et al, 2012, Rueppell 2014, age polyethism (Zayed and Robinson 2012), learning and memory (Müller, 2012) and defensive behaviour (Avalos et al 2020, Harpur et al 2020). These bodies of work have resulted in profound leaps forward in our understanding of the molecular underpinnings of other aspects of honey bee behaviour.…”