title: Honey bee aggression supports a link between gene regulation and behavioral evolution.
abstract: A prominent theory states that animal phenotypes arise by evolutionary changes in gene regulation, but the extent to which this theory holds true for behavioral evolution is not known. Because "nature and nurture" are now understood to involve hereditary and environmental influences on gene expression, we studied whether environmental influences on a behavioral phenotype, i.e., aggression, could have evolved into inherited differences via changes in gene expression. Here, with microarray analysis of honey bees, we show that aggression-related genes with inherited patterns of brain expression are also environmentally regulated. There were expression differences in the brain for hundreds of genes between the highly aggressive Africanized honey bee compared with European honey bee (EHB) subspecies. Similar results were obtained for EHB in response to exposure to alarm pheromone (which provokes aggression) and when comparing old and young bees (aggressive tendencies increase with age). There was significant overlap of the gene lists generated from these three microarray experiments. Moreover, there was statistical enrichment of several of the same cis regulatory motifs in promoters of genes on all three gene lists. Aggression shows a remarkably robust brain molecular signature regardless of whether it occurs because of inherited, age-related, or environmental (social) factors. It appears that one element in the evolution of different degrees of aggressive behavior in honey bees involved changes in regulation of genes that mediate the response to alarm pheromone.
authors.affiliation: Department of Entomology, University of Illinois, Urbana, IL 61801, USA.
authors.forename: Cédric
authors.initials: C
authors.lastname: Alaux
authors.forename: Saurabh
authors.initials: S
authors.lastname: Sinha
authors.forename: Linda
authors.initials: L
authors.lastname: Hasadsri
authors.forename: Greg J
authors.initials: GJ
authors.lastname: Hunt
authors.forename: Ernesto
authors.initials: E
authors.lastname: Guzmán-Novoa
authors.forename: Gloria
authors.initials: G
authors.lastname: DeGrandi-Hoffman
authors.forename: José Luis
authors.initials: JL
authors.lastname: Uribe-Rubio
authors.forename: Bruce R
authors.initials: BR
authors.lastname: Southey
authors.forename: Sandra
authors.initials: S
authors.lastname: Rodriguez-Zas
authors.forename: Gene E
authors.initials: GE
authors.lastname: Robinson
mesh_terms: D000374:Aggression; D000818:Animals; D001516:Bees / Q000502:physiology*; D001522:Behavior, Animal / Q000502:physiology*; D005075:Biological Evolution; D001921:Brain / Q000378:metabolism; D004798:Enzymes / Q000378:metabolism; D005786:Gene Expression Regulation; D008800:Mexico; D024101:Mitochondrial Proteins / Q000378:metabolism; D020411:Oligonucleotide Array Sequence Analysis; D025341:Principal Component Analysis; D050436:Regulatory Elements, Transcriptional / Q000235:genetics; D013045:Species Specificity
chemical_list: D004798:Enzymes; D024101:Mitochondrial Proteins
references.citation: Proc Natl Acad Sci U S A. 2008 Mar 18;105(11):4226-31
references.pmid: 18337502
references.citation: Eur J Neurosci. 1998 Oct;10(10):3035-43
references.pmid: 9786198
references.citation: Annu Rev Entomol. 2004;49:271-98
references.pmid: 14651465
references.citation: Science. 2008 Nov 7;322(5903):896-900
references.pmid: 18988841
references.citation: J Chem Ecol. 2007 Jul;33(7):1346-50
references.pmid: 17505874
references.citation: J Hum Genet. 2005;50(4):210-216
references.pmid: 15838597
references.citation: Nat Neurosci. 2006 Apr;9(4):569-77
references.pmid: 16547508
references.citation: Proc Natl Acad Sci U S A. 2008 Apr 29;105(17):6409-14
references.pmid: 18443293
references.citation: Proc Natl Acad Sci U S A. 2006 Oct 31;103(44):16352-7
references.pmid: 17065326
references.citation: Genes Brain Behav. 2009 Apr;8(3):309-19
references.pmid: 19220482
references.citation: Front Neuroendocrinol. 2008 Oct;29(4):476-89
references.pmid: 18280561
references.citation: Proc Natl Acad Sci U S A. 2005 May 3;102 Suppl 1:6543-9
references.pmid: 15851679
references.citation: PLoS Biol. 2005 Jul;3(7):e204
references.pmid: 15934786
references.citation: Genome Biol. 2004;5(12):R101
references.pmid: 15575967
references.citation: Behav Neurosci. 2003 Jun;117(3):540-7
references.pmid: 12802882
references.citation: J Comp Physiol A. 1999 May;184(5):481-8
references.pmid: 10377981
references.citation: J Insect Physiol. 2007 May;53(5):399-410
references.pmid: 17379239
references.citation: Nature. 2006 Oct 26;443(7114):931-49
references.pmid: 17073008
references.citation: Science. 2001 Sep 14;293(5537):2087-92
references.pmid: 11557892
references.citation: Genes Brain Behav. 2002 Nov;1(4):197-203
references.pmid: 12882364
references.citation: Annu Rev Entomol. 2004;49:351-76
references.pmid: 14651468
references.citation: Behav Genet. 2003 May;33(3):357-64
references.pmid: 12837024
references.citation: Evolution. 2000 Aug;54(4):1079-91
references.pmid: 11005278
references.citation: Neuroscience. 2007 Mar 16;145(2):403-12
references.pmid: 17222984
references.citation: PLoS Genet. 2008 Jul 18;4(7):e1000127
references.pmid: 18636101
references.citation: Trends Neurosci. 2001 Dec;24(12):713-9
references.pmid: 11718876
references.citation: Nat Genet. 2007 May;39(5):678-82
references.pmid: 17450142
references.citation: Naturwissenschaften. 2007 Apr;94(4):247-67
references.pmid: 17171388
references.citation: Proc Biol Sci. 2004 Nov 7;271(1554):2267-73
references.pmid: 15539352
references.citation: Brain Res Brain Res Rev. 2005 Feb;48(1):1-15
references.pmid: 15708625
references.citation: Nature. 2005 Mar 17;434(7031):338-45
references.pmid: 15735639
references.citation: J Neurosci. 2006 Feb 8;26(6):1864-71
references.pmid: 16467535
references.citation: Pharmacol Biochem Behav. 2007 Jun-Jul;87(2):241-9
references.pmid: 17537494
references.citation: BMC Genomics. 2008 May 19;9:232
references.pmid: 18489784
references.citation: PLoS Biol. 2005 Jul;3(7):e245
references.pmid: 16000021
references.citation: Cell Tissue Res. 2005 Sep;321(3):443-58
references.pmid: 16034628
references.citation: Proc Natl Acad Sci U S A. 2008 Apr 15;105(15):5657-63
references.pmid: 18408154
references.citation: Cell. 2008 Jul 11;134(1):25-36
references.pmid: 18614008
references.citation: Brain Res Bull. 2006 Apr 14;69(3):259-65
references.pmid: 16564420