Gene expression tied to social behavior in honey bees

Genes and behavior go together in honey bees so strongly that an individual bee’s occupation can be predicted by knowing a profile of its gene expression in the brain, say researchers at the University of Illinois at Urbana-Champaign.

This strong relationship surfaced in a complex molecular study of 6,878 different genes replicated with 72 cDNA microarrays that captured the essence of brain gene activity within the natural world of the honey bee (Apis mellifera). Even though most of the differences in gene expression were small, the changes were observable in 40 percent of the genes studied, the scientists report in the Oct. 10 issue of the journal Science.

“We have discovered a clear molecular signature in the bee brain that is robustly associated with behavior,” said principal researcher Gene E. Robinson, a professor of entomology and director of the Neuroscience Program at Illinois. “This provides a striking picture of the genome as a dynamic entity, more actively involved in modulating behavior in the adult brain than we previously thought.”

Microarrays let researchers get a broad view of gene activity by generating simultaneous measurements of messenger RNA, which reflect levels of protein activity. The mRNA binds to specific sites on the array, allowing for the measurement of expression from thousands of genes.

Robinson, who also holds the G. William Arends Professorship in Integrative Biology at Illinois, and colleagues generated mRNA profiles from 60 different bees who were working either as nurses (taking care of the brood within the hive) or foragers (gathering food outside). A computer program was able to use the profiles to determine correctly, for 57 of 60 the bees, which individual belonged to what group.

Behavioral differences between nurses and foragers are part of an age-related, socially regulated division of bee labor. Nurses perform care-giving duties for their first two to three weeks of life, then shift to foraging for nectar and pollen. As the behavioral transition occurs the bees experience changes in brain structure, brain chemistry, and, as this new study shows, many changes in gene expression.

Robinson, whose research is part of a federally funded project to sequence the honey bee genome, has long been interested in the mechanisms involved in honey bee division of labor as a model to understand the relationships between genes, brain and behavior.

After an initial analysis showed differences between nurses and foragers, the researchers faced the problem of relating these differences to either age or behavior, because foragers are both behaviorally different and older than nurses. So Robinson and colleagues created colonies consisting entirely of same-aged bees. In the absence of older bees, some individuals in a hive will begin foraging up to two weeks earlier than usual while others will grow up normally and act as nurses, making for age-matched young nurses and foragers. Age-matched old foragers and old nurses also were obtained from these colonies.

A dominant pattern of gene expression emerged, and it “was clearly associated with behavior,” the researchers wrote. Since precocious foraging is a response to the shortage of foragers, this finding indicates that the genome is responding dynamically to changes in the bee’s social environment, Robinson said.

The study was unique, he said, because it focused on individual profiles. Previous studies of gene expression and behavior in mice and flies, for instance, have focused on group tendencies, looking at pools of individuals.

Robinson’s colleagues on the paper were Charles W. Whitfield, a postdoctoral researcher in the department of entomology, and undergraduate Anne-Marie Cziko.

The research was funded by a National Science Foundation Postdoctoral Fellowship in Bioinformatics to Whitfield and by grants from the University of Illinois Critical Research Initiatives Program and Burroughs Wellcome Trust.

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