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Expression Study Links Gene Regulation and Evolution of Aggression in Bees

NEW YORK (GenomeWeb News) – Short-term aggressive behavior in European honey bees involves many of the same gene expression patterns found in the inherently more aggressive Africanized bees, according to research scheduled to appear online this week in the Proceedings of the National Academy of Sciences.

Researchers from the US, Canada, and Mexico used microarrays to compare gene expression in the brains of various European and Africanized bees under different environmental conditions. Their results indicate that the types of short-term gene expression changes in alarmed European honey bee brains resembled the baseline expression pattern in the brains of more aggressive older bees or Africanized bees.

"Based on brain gene expression profiles, Africanized bees look like they've been exposed to an alarm pheromone," senior author Gene Robinson, a genomics, entomology, and neuroscience researcher at the University of Illinois at Urbana-Champaign, told GenomeWeb Daily News.

In addition, many of the aggression-related genes in each of the bee groups tested seem to share cis-regulatory motifs in their promoters, bolstering the team's hypothesis that gene regulation and the evolution of aggression in bees are linked.

Past research has shown that honey bee aggression involves multiple genes. Bees can become aggressive in response to alarms issued by other bees — for instance, in response to perceived danger to the hive.

But some bees and some colonies are inherently more aggressive than others, the researchers explained. For example, older bees tend to get riled up more easily than younger bees. And Africanized bees, thought to have come about through the hybridization of two honey bee sub-species from Africa and Europe, are generally much more aggressive than European bees.

For the latest study, done through the National Science Foundation funded BeeSpace project, Robinson and his colleagues designed a set of experiments intended to look at gene expression related to bee behavior over different time scales — comparing alarmed bees with control bees, old bees with young bees, and European bees with Africanized bees.

Under each set of conditions, the team gauged gene expression in bee brains using custom spotted 70-mer microarrays designed from honey bee genome sequence. The arrays are a publicly available resource for sale at cost from the University of Illinois' Keck Center for Comparative and Functional Genomics, Robinson noted.

The team reported that brain gene expression varied depending on a bee's role in the colony. For example, there were more gene expression differences in the brains of Africanized and European guard bees and soldier bees than between the Africanized and European forager bees from each group.

By raising Africanized bees in European bee colonies and vice versa, the researchers were able to begin teasing apart the influence of genotype and environment on brain gene expression. Their results suggest that some 30 percent of the variation in gene expression is due to a bee's genotype while another 25 percent was due to the genotype of the colony.

They also found that exposing the European bees to an alarm pheromone for a minute led to changes in the expression of hundreds of genes in the bee brain. As it turned out, the expression pattern in these alarmed bees was actually quite similar to that found in the brains of Africanized bees under normal conditions. Older, more aggressive European bees also had a similar expression profile.

The genes that were up-regulated in each group of bees during arousal or aggression tended to share the same cis-regulatory motifs in their promoter region, the authors noted, suggesting that "hereditary and environmental influences on aggression share a common molecular basis."

When the researchers explored the function of the genes whose expression changed with aggression using the Gene Ontology, they turned up genes involved alertness, sight, smell, and other processes known to get switched on during aggressive behavior.

Unexpectedly, though, the expression of metabolic genes actually decreased in the brains of aggressive bees. Though the team proposed several possible explanations for this pattern, they said more research is needed to get to the bottom of this metabolism-aggression link.

So far, Robinson said, it's unclear whether the ongoing expression of aggression-related genes in African bees is an ancestral condition that was lost from European bees, which now show this pattern when alarmed or older or whether the increased expression of these genes came about through selection in the African bees.

"Aggression shows a remarkably robust brain molecular signature regardless of whether it occurs because of inherited, age-related, or environmental (social) factors," the authors explained. "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."

In the future, the team plans to use some new methods such as transcript sequencing to explore gene expression patterns coinciding with aggression and arousal in the bee brain, Robinson said. He noted that co-author Saurabh Sinha, also at the University of Illinois, is also looking into some of the cis-regulation patterns found in the current study.

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