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Developmental Biology - Genetic Behavior

What Influences Bee Aggression?

Group dynamics - NOT genes - drive aggression in honey bees...

Researchers often study the genomes of individual organisms to try to tease out the relationship between genes and behavior. A new study of Africanized honey bees reveals, however, that the genetic inheritance of individual bees has little influence on their propensity for aggression. Instead, the genomic traits of the hive as a whole are strongly associated with how fiercely its soldiers attack.

The findings are reported in the journal of the Proceedings of the National Academy of Sciences, PNAS.
"We've always thought the most significant aspects of an organism's behavior are driven, at least in part, by its own genetic endowment and not the genomics of its society. This is a signal that there may be more to the genetics of behavior as a whole than we've been thinking about."

Matthew Hudson PhD, University of Illinois at Urbana-Champaign, Professor, Bioinformatics, Department of Crop Sciences.

Dr.Hudson led the research with Gene Robinson, an entomology professor and director of the Carl R. Woese Institute for Genomic Biology at the University of Illinois at Urbana-Champaign (U of I). Researchers focused on a unique population of gentle Africanized honey bees in Puerto Rico, which evolved to become more docile than Africanized bees anywhere else in the world.

"We wanted to know which parts of the genome are responsible for gentle behavior versus aggressive behavior," Hudson explains. "And because there's quite a bit of variation in aggression among these bees, they are an ideal population to study."

Africanized bees are hardier and more resistant to disease than their European predecessors on the island, so scientists are eager to learn more about the genetic underpinnings of the Puerto Rican bees' gentle nature.
When a honey bee hive is disturbed, guard bees emit a chemical signal that spurs soldier bees into action. The response depends on the nature of the threat and the aggressiveness of the hive. Whether the soldiers sting their target is another measure of aggression, as soldiers that sting will die as a result.

In general, foragers do little to defend the hive.

Researchers compared the genomes of soldier and forager bees from each of nine honey bee colonies in Puerto Rico, and tested how aggressively soldier bees responded to an assault on their hive.
To their surprise, the scientists found no genome-sequence differences between soldiers and foragers that would consistently explain their different responses.

But when researchers conducted a genomewide association study comparing the most and least aggressive hives, they saw a strong correlation between hive genomics and aggression.

"There was one chunk of DNA where the frequency of that chunk in the hive seems to dictate how gentle that hive is going to be to a large extent," Hudson explained. "What that tells us is that the individual genetic makeup of the bee doesn't have a strong influence on how aggressive it is. But the genetic makeup of the society that the bees live in - the colony - has a very strong impact on how aggressive bees in that colony are."

"Many behavioral traits in animals and humans are known to be strongly affected by inherited differences in genome sequence, but for many behaviors, how an individual acts also is influenced by how others around it are acting - nature and nurture, respectively," explainsRobinson. "We now see that in the beehive, nurture can also have a strong genomic signature."
Such behavioral genomic influence may be particularly pronounced in honey bees, which live in an extraordinarily cooperative society where each individual has a defined social and functional role.

Honey bee colony defense is an emergent trait composed of individual aggressive responses. Here, we investigated the relationship between individual genotype, colony allele frequency, and aggression in individual bees. Our findings show that the colony-level defense response strongly correlates with colony-level allele frequency in a way that can be used to identify causative genomic regions. Importantly, we were able to validate a key associated region as also being under selection. As very similar allele frequency correlations are observed in both soldier and forager bees, we conclude that group genetics is more important than individual genetics in this case, giving further insight into the relationships between “nature,” “nurture,” and behavioral evolution.

For social animals, the genotypes of group members affect their 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.

Arián Avalos, Miaoquan Fang,Hailin Pan, Aixa Ramirez Lluch, Alexander E. Lipka, Sihai Dave Zhao, Tugrul Giray, Gene E. Robinson, Guojie Zhang and Matthew E. Hudson

The National Science Foundation, National Institutes of Health, Chinese Academy of Sciences, Lundbeck Foundation and IGB supported this research.

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Jul 8 2020   Fetal Timeline   Maternal Timeline   News

Researchers studied a unique population of gentle Africanized honey bees in Puerto Rico.
CREDIT Photo by Manuel A. Giannoni-Guzman.

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