Honey bee aggression supports a link between gene regulation and behavioral evolution.
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.
Alaux
Cédric
C
Department of Entomology, University of Illinois, Urbana, IL 61801, USA.
Sinha
Saurabh
S
Hasadsri
Linda
L
Hunt
Greg J
GJ
Guzmán-Novoa
Ernesto
E
DeGrandi-Hoffman
Gloria
G
Uribe-Rubio
José Luis
JL
Southey
Bruce R
BR
Rodriguez-Zas
Sandra
S
Robinson
Gene E
GE
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
D004798:Enzymes; D024101:Mitochondrial Proteins
Proc Natl Acad Sci U S A. 2008 Mar 18;105(11):4226-31
18337502
Eur J Neurosci. 1998 Oct;10(10):3035-43
9786198
Annu Rev Entomol. 2004;49:271-98
14651465
Science. 2008 Nov 7;322(5903):896-900
18988841
J Chem Ecol. 2007 Jul;33(7):1346-50
17505874
J Hum Genet. 2005;50(4):210-216
15838597
Nat Neurosci. 2006 Apr;9(4):569-77
16547508
Proc Natl Acad Sci U S A. 2008 Apr 29;105(17):6409-14
18443293
Proc Natl Acad Sci U S A. 2006 Oct 31;103(44):16352-7
17065326
Genes Brain Behav. 2009 Apr;8(3):309-19
19220482
Front Neuroendocrinol. 2008 Oct;29(4):476-89
18280561
Proc Natl Acad Sci U S A. 2005 May 3;102 Suppl 1:6543-9
15851679
PLoS Biol. 2005 Jul;3(7):e204
15934786
Genome Biol. 2004;5(12):R101
15575967
Behav Neurosci. 2003 Jun;117(3):540-7
12802882
J Comp Physiol A. 1999 May;184(5):481-8
10377981
J Insect Physiol. 2007 May;53(5):399-410
17379239
Nature. 2006 Oct 26;443(7114):931-49
17073008
Science. 2001 Sep 14;293(5537):2087-92
11557892
Genes Brain Behav. 2002 Nov;1(4):197-203
12882364
Annu Rev Entomol. 2004;49:351-76
14651468
Behav Genet. 2003 May;33(3):357-64
12837024
Evolution. 2000 Aug;54(4):1079-91
11005278
Neuroscience. 2007 Mar 16;145(2):403-12
17222984
PLoS Genet. 2008 Jul 18;4(7):e1000127
18636101
Trends Neurosci. 2001 Dec;24(12):713-9
11718876
Nat Genet. 2007 May;39(5):678-82
17450142
Naturwissenschaften. 2007 Apr;94(4):247-67
17171388
Proc Biol Sci. 2004 Nov 7;271(1554):2267-73
15539352
Brain Res Brain Res Rev. 2005 Feb;48(1):1-15
15708625
Nature. 2005 Mar 17;434(7031):338-45
15735639
J Neurosci. 2006 Feb 8;26(6):1864-71
16467535
Pharmacol Biochem Behav. 2007 Jun-Jul;87(2):241-9
17537494
BMC Genomics. 2008 May 19;9:232
18489784
PLoS Biol. 2005 Jul;3(7):e245
16000021
Cell Tissue Res. 2005 Sep;321(3):443-58
16034628
Proc Natl Acad Sci U S A. 2008 Apr 15;105(15):5657-63
18408154
Cell. 2008 Jul 11;134(1):25-36
18614008
Brain Res Bull. 2006 Apr 14;69(3):259-65
16564420