Sexual isolation of male moths explained by a single pheromone response QTL containing four receptor genes.
Long distance sexual communication in moths has fascinated biologists because of the complex, precise female pheromone signals and the extreme sensitivity of males to specific pheromone molecules. Progress has been made in identifying some genes involved in female pheromone production and in male response. However, we have lacked information on the genetic changes involved in evolutionary diversification of these mate-finding mechanisms that is critical to understanding speciation in moths and other taxa. We used a combined quantitative trait locus (QTL) and candidate gene approach to determine the genetic architecture of sexual isolation in males of two congeneric moths, Heliothis subflexa and Heliothis virescens. We report behavioral and neurophysiological evidence that differential male responses to three female-produced chemicals (Z9-14:Ald, Z9-16:Ald, Z11-16:OAc) that maintain sexual isolation of these species are all controlled by a single QTL containing at least four odorant receptor genes. It is not surprising that pheromone receptor differences could control H. subflexa and H. virescens responses to Z9-16:Ald and Z9-14:Ald, respectively. However, central rather than peripheral level control over the positive and negative responses of H. subflexa and H. virescens to Z11-16:OAc had been expected. Tight linkage of these receptor genes indicates that mutations altering male response to complex blends could be maintained in linkage disequilibrium and could affect the speciation process. Other candidate genes such as those coding for pheromone binding proteins did not map to this QTL, but there was some genetic evidence of a QTL for response to Z11-16:OH associated with a sensory neuron membrane protein gene.
Gould
Fred
F
Department of Entomology and W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC 27695, USA. fred_gould@ncsu.edu
Estock
Marie
M
Hillier
N Kirk
NK
Powell
Bekah
B
Groot
Astrid T
AT
Ward
Catherine M
CM
Emerson
Jennifer L
JL
Schal
Coby
C
Vickers
Neil J
NJ
D000825:Animal Structures / Q000187:drug effects / Q000502:physiology; D000818:Animals; D002874:Chromosome Mapping; D002875:Chromosomes / Q000235:genetics; D003433:Crosses, Genetic; D055724:Electrophysiological Phenomena / Q000187:drug effects; D005260:Female; D017344:Genes, Insect / Q000235:genetics*; D007178:Inbreeding; D007659:Ketones / Q000494:pharmacology; D008297:Male; D009036:Moths / Q000187:drug effects* / Q000235:genetics*; D009474:Neurons / Q000187:drug effects / Q000502:physiology; D010675:Pheromones / Q000494:pharmacology*; D040641:Quantitative Trait Loci / Q000235:genetics*; D018035:Receptors, Odorant / Q000235:genetics*; D012726:Sexual Behavior, Animal / Q000187:drug effects*; D013045:Species Specificity
C480312:11-hexadecenyl trifluoromethyl ketone; D007659:Ketones; D010675:Pheromones; D018035:Receptors, Odorant
Science. 2001 Aug 3;293(5531):857-60
11486086
J Chem Ecol. 2004 Dec;30(12):2495-514
15724967
Insect Biochem Mol Biol. 2009 Aug;39(8):568-77
19477278
J Chem Ecol. 1983 Jun;9(6):747-59
24407621
Proc Natl Acad Sci U S A. 2006 Apr 11;103(15):5858-63
16585529
FEBS Lett. 1989 Oct 9;256(1-2):215-8
2806547
Evolution. 2009 May;63(5):1171-90
19154394
J Evol Biol. 2006 Mar;19(2):600-17
16599935
J Insect Sci. 2007;7:4
20334597
Chem Senses. 2009 Jul;34(6):469-77
19289532
Annu Rev Ecol Evol Syst. 2008 Dec 1;39:21-42
20419035
Top Curr Chem. 2004;239:97-132
22160232
Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):44-9
7816846
Heredity (Edinb). 2009 Jan;102(1):77-97
18685572
J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2004 Feb;190(2):155-65
14689220
Genetics. 2003 Mar;163(3):939-53
12663534
Annu Rev Physiol. 2009;71:307-32
19575682
Annu Rev Entomol. 2006;51:113-35
16332206
Trends Ecol Evol. 2008 Apr;23(4):220-8
18308422
Genetics. 1989 Nov;123(3):553-6
2599367
Insect Biochem Mol Biol. 1993 Jun;23(4):449-56
8508187
J Econ Entomol. 2005 Aug;98(4):1357-68
16156591
J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2005 Sep;191(9):777-90
16094545
Chem Senses. 2009 Jul;34(6):465-8
19458025
Mol Ecol. 2007 Jul;16(14):2893-909
17614905
Proc Natl Acad Sci U S A. 2004 Nov 23;101(47):16653-8
15545611
Proc Natl Acad Sci U S A. 2004 Aug 10;101(32):11845-50
15289611
Nature. 2008 Mar 27;452(7186):473-7
18305480
Eur J Neurosci. 2007 Apr;25(8):2364-73
17445234
Proc Natl Acad Sci U S A. 2009 Jun 16;106(24):9737-42
19487670
J Neurobiol. 2001 Oct;49(1):47-61
11536197
Insect Mol Biol. 2007 Feb;16(1):107-19
17257213
Invert Neurosci. 2006 Mar;6(1):13-21
16402239
Evolution. 2006 Nov;60(11):2185-206
17236413
Chem Senses. 2006 Nov;31(9):821-34
16984959
Brain Behav Evol. 2006;68(2):63-74
16707860
J Exp Biol. 2008 Sep;211(Pt 17):2841-8
18723543
Eur J Neurosci. 2002 Aug;16(4):619-28
12270037
Brain Behav Evol. 2006;68(2):90-108
16707862
Insect Biochem Mol Biol. 2001 Nov 1;31(12):1173-81
11583930
Proc Biol Sci. 2005 Feb 7;272(1560):303-9
15705556
Proc Natl Acad Sci U S A. 2006 Apr 25;103(17):6575-80
16611733
J Chem Ecol. 2002 Jun;28(6):1255-67
12184401
J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2006 Feb;192(2):199-219
16249880
J Insect Sci. 2009;9:18
19613461
J Neurosci Methods. 1989 Jul;29(1):77-83
2761300