Honey bee aggression supports a link between gene regulation and behavioral evolution

TLDR

Animal phenotypes are thought to arise from evolutionary changes in gene regulation, but it is unclear whether this applies to behavioral evolution. We investigated whether environmental influences on honey bee aggression could become inherited through changes in gene expression. Microarray analysis revealed that aggression‑associated genes with inherited brain expression patterns are also environmentally regulated, with hundreds of genes differing between Africanized and European bees, similar responses to alarm pheromone and age, overlapping gene lists enriched for shared cis‑regulatory motifs, indicating a robust molecular signature of aggression driven by regulatory changes.

Abstract

A prominent theory states that animal phenotypes arise by evolutionary changes in gene regulation, but the extent to which this theory holds true for behavioral evolution is not known. Because “nature and nurture” are now understood to involve hereditary and environmental influences on gene expression, we studied whether environmental influences on a behavioral phenotype, i.e., aggression, could have evolved into inherited differences via changes in gene expression. Here, with microarray analysis of honey bees, we show that aggression-related genes with inherited patterns of brain expression are also environmentally regulated. There were expression differences in the brain for hundreds of genes between the highly aggressive Africanized honey bee compared with European honey bee (EHB) subspecies. Similar results were obtained for EHB in response to exposure to alarm pheromone (which provokes aggression) and when comparing old and young bees (aggressive tendencies increase with age). There was significant overlap of the gene lists generated from these three microarray experiments. Moreover, there was statistical enrichment of several of the same cis regulatory motifs in promoters of genes on all three gene lists. Aggression shows a remarkably robust brain molecular signature regardless of whether it occurs because of inherited, age-related, or environmental (social) factors. It appears that one element in the evolution of different degrees of aggressive behavior in honey bees involved changes in regulation of genes that mediate the response to alarm pheromone.