Genomic regions influencing aggressive behavior in honey bees are defined by colony allele frequencies

Authors: Avalos, Arian; FANG, MIAOQUAN - CHINESE ACADEMY OF SCIENCES; PAN, HAILIN - CHINESE ACADEMY OF SCIENCES; RAMIREZ LLUCH, AIXA - UNIVERSITY OF PUERTO RICO; LIPKA, ALEXANDER - UNIVERSITY OF ILLINOIS; ZHAO, SIHAI - UNIVERSITY OF ILLINOIS; GIRAY, TUGRUL - UNIVERSITY OF PUERTO RICO; ROBINSON, GENE - UNIVERSITY OF ILLINOIS; ZHANG, GUOJIE - CHINESE ACADEMY OF SCIENCES; HUDSON, MATTHEW - UNIVERSITY OF ILLINOIS

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/18/2020
Publication Date: 7/6/2020
Citation: Avalos, A., Fang, M., Pan, H., Ramirez Lluch, A., Lipka, A., Zhao, S., Giray, T., Robinson, G., Zhang, G., Hudson, M. 2020. Genomic regions influencing aggressive behavior in honey bees are defined by colony allele frequencies. Proceedings of the National Academy of Sciences. 1-7.
DOI: https://doi.org/10.1073/pnas.1922927117

Interpretive Summary: Evolution and genetics of behaviors are difficult to study in social insects because behaviors are influenced by group environment which can confound results. We used a unique population of gentle Africanized bees and whole genome sequencing to examine the genetic underpinning of aggression. Our analyses found no correlations between behavior and genetic structure at the individual level but did find strong correlations when we conducted our analysis at the group level. In addition, many of the genomic regions we identify here were also regions under selection towards gentle behavior in an independent study of the same population. This approach to examine signals of correlation between genomic regions and behaviors at the group level serves as a novel approach to identify cryptic genetic associations in complex phenotypes. Ultimately, this can serve as a novel tool in the study of honey bee behavioral traits.

Technical Abstract: The genetics and evolution of behavioral traits are difficult to elucidate via association, possibly because many behavioral phenotypes are influenced by group environments. Such effects confound discovery of correlates using individual genotype-phenotype data. Sequencing whole genomes, we found no significant correlations between individual aggression and genotype in a well-characterized population of Africanized honey bees. By contrast, we found strong correlations between colony aggression and the frequency of specific haplotypes within colonies. Furthermore, many of these haplotypes were found to have positive signatures of selection during the evolution of gentleness in an independent study. Association of group phenotype with population genetics can therefore identify cryptic genetic correlates for complex traits. These results add a new dimension to our understanding of genotype to phenotype matching.