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Title:   Author  item
                                            ALAUX, CEDRIC - UNIV. ILLINOIS, URBANAitem
                                            SINHA, SAURABH - UNIV. ILLINOIS, URBANAitem
                                            HASADSRI, LINDA - UNIV. ILLINOIS, URBANAitem
                                            HUNT, GREG - PURDUE UNIV.item
                                            GUZMAN-NOVOA, ERNESTO - UNIV. GUELPH, CANADAitem
                                            DeGrandi-Hoffman, Gloriaitem
                                            URIBE-RUBIO, JOSE LUIS - CENIDFA-INIFAP, MEXICOitem
                                            RODRIGUEZ-ZAS, SANDRA - UNIV. ILLINOIS, URBANAitem
                                            ROBINSON, GENE - UNIV. ILLINOIS, URBANA
  Submitted to: Proceedings of the National Academy of Sciences (PNAS)
                                    Publication Type: Proceedings
                                    Publication Acceptance Date: 9/14/2009
                                    Publication  Date: 9/8/2009
                                    Citation: Alaux, C., Sinha, S., Hasadsri, L., Hunt, G.J., Guzman-Novoa, E., Hoffman, G.D., Uribe-Rubio, J., Rodriguez-Zas, S., Robinson, G.E. 2009. Honey bee aggression supports a link between gene regulation and behavioral evolution. Proceedings of the National Academy of Sciences, 106(36): 15400-15405. doi:10.1073pnas.0907043106.Interpretive Summary: A well known difference between Africanized and European honey bees is that Africanized bees have a greater expression of nest defense behavior.  Underlying the differences in the expression of defensive behavior might be differences in the temporal and spatial patterns of gene expression.  We found differences in brain gene expression that are related to the evolution of nest defense behavior.  Our study using microarray analysis revealed differences between European and Africanized bees in the expression of hundreds of genes associated with defensive behavior.  To relate these differences to behavioral evolution, we determined whether some of these genes also are associated with stinging behavior within European bees in real time.  One experiment studied the effects of exposure to alarm pheromone, which provokes defensive behavior, and a second experiment compared old and young bees, because defensive behaviors increase with age in honeybees.  There was significant overlap of the gene lists generated from the three microarray experiments.  Increased defensive behavior was associated with a downregulation of brain metabolism genes.  Our results suggest that one factor in the evolution of nest defense behavior in honey bees is the regulation of genes that mediate the response to alarm pheromone.
                                Technical Abstract: A prominent theory holds that animal phenotypes arise by evolutionary changes in the regulation of gene expression.  Emerging from studies of animal development, evidence for this theory consists largely of differences in temporal or spatial patterns of gene expression that are related to morphological evolution.  With only a few cases studied to date, the extent to which this theory holds for behavioral evolution is not known.  Here we report differences in brain gene expression that are related to the evolution of aggressive behaviour in the honeybee Apis mellifera.  Microarray analysis revealed expression differences for hundreds of genes between the highly aggressive Africanized honeybee compared to European subspecies.  To relate these differences to behavioral evolution, we determined whether some of these genes also are associated with aggressive behaviour within European bees in real time.  One experiment studied the effects of exposure to alarm pheromone, which provokes aggressive behaviour, and a second experiment compared old and young bees, because aggressive tendencies increase with age in honeybees.  There was significant overlap of the gene lists generated from the three microarray experiments.  Moreover, there was statistical enrichment of several of the same cis regulatory motifs across the three gene lists.  In all three cases increased aggression was associated with a downregulation of brain metabolism genes; decreased brain metabolism was confirmed by enzyme assay.  Common genetic regulatory architecture over three timescales - evolutionary, organismal, and physiological - suggest that one factor in the evolution of aggressive behaviour in honeybees involved changes in regulation of genes that mediate the response to alarm pheromone.


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