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

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.

Polymorphism and division of labour in a socially complex ant: neuromodulation of aggression in the Australian weaver ant,Oecophylla smaragdina

“…In the completely dimorphic ant Pheidole pallidula, changes in foraging or defence in major workers are correlated with the expression of the PPFOR protein in a small number of cells; this does not occur in minors [60]. Downstream neurobiological effects contributing to division of labour between subcastes and the higher defensive aggression shown by major workers have not been determined in P. pallidula or other ants; however, studies on honeybees suggest the nature of the mechanisms involved [61].…”

Diverse societies are more productive: a lesson from ants

“…The latter could have not only increased mean colony aggression but also its variation. Presumably, aggression in ants is generated through a combination of inherited, age-related or environmental factors similar to the honeybees [19].…”

What can whole genome expression data tell us about the ecology and evolution of personality?

“…Comparing expression differences between such lines could potentially tell us the identity of those genes that differ between them. The same principle also applies to natural populations that differ in personality traits, such as more bold versus less bold populations of sticklebacks, or more aggressive versus less aggressive populations as in the Africanized and European honeybees (Alaux et al 2009). …”

“…In general, Africanized honeybees are more aggressive than European honeybees. Alaux et al (2009) compared brain gene expression in these two subspecies, and also compared the molecular response to an alarm pheromone, which triggers aggression, in the European honeybees. They found that some of the genes that were involved in the behavioural response to alarm pheromone were also differentially expressed between the two subspecies, in the absence of alarm pheromone.…”

“…One can look for common motifs upstream of the candidate genes to look for transcription factor binding sites (Alaux et al 2009). If common motifs and their transcription factors are identified, those transcription factors are interesting candidate master switches that might regulate a suite of gene expression changes.…”