TY - JOUR
T1 - Genomic regions influencing aggressive behavior in honey bees are defined by colony allele frequencies
AU - Avalos, Arián
AU - Fang, Miaoquan
AU - Pan, Hailin
AU - Ramirez Lluch, Aixa
AU - Lipka, Alexander E.
AU - Zhao, Sihai Dave
AU - Giray, Tugrul
AU - Robinson, Gene E.
AU - Zhang, Guojie
AU - Hudson, Matthew E.
N1 - Funding Information:
ACKNOWLEDGMENTS. We thank G. Diaz and F. Noel for assistance during sample collection and trait measurements; C.J. Fields, G. Rendon, and the rest of the High Performance Computing for Biology team for technical assistance; and B. Harpur for providing archival QTL marker data. This work was supported by National Science Foundation (NSF) Grants 15-501 1547830 (to A.A.), HRD 1736019 (to A.R.L. and T.G.), Puerto Rico Science, Technology and Research Trust 2020-00139 (to A.R.L. and T.G.), and NSF Division of Environmental Biology 1826729 (to A.R.L. and T.G.) and National Institutes of Health Grant R01GM117467 (to G.E.R. and N. Goldenfeld). This project was also supported, in part, by Strategic Priority Research Program of the Chinese Academy of Science Grant XDB13000000; Lundbeckfonden Grant R190-2014-2827 (to G.Z.); and funding from the Carl R. Woese Institute for Genomic Biology at the University of Illinois (to M.E.H.).
PY - 2020/7/21
Y1 - 2020/7/21
N2 - For social animals, the genotypes of group members affect the 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.
AB - For social animals, the genotypes of group members affect the 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.
KW - Aggression
KW - Behavioral genetics
KW - GWAS
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U2 - 10.1073/pnas.1922927117
DO - 10.1073/pnas.1922927117
M3 - Article
C2 - 32631983
SN - 0027-8424
VL - 117
SP - 17135
EP - 17141
JO - Proceedings of the National Academy of Sciences
JF - Proceedings of the National Academy of Sciences
IS - 29
ER -