QTL analysis of sex pheromone blend differences between two closely related moths: Insights into divergence in biosynthetic pathways

Insect Biochemistry and Molecular Biology

Volumn 39, Issue 8, 2009, Pages 568-577

  Groot, Astrid T ^a   Estock, Marie L ^a   Horovitz, Joy L ^a   Hamilton, Jennifer ^a   Santangelo, Richard G ^a   Schal, Coby ^a   Gould, Fred ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Biosynthetic pathway; Candidate genes; Heliothis subflexa; Heliothis virescens; Noctuidae; Sex pheromone production

Indexed keywords

HELIOTHIS SUBFLEXA; HELIOTHIS VIRESCENS; LEPIDOPTERA; NOCTUIDAE;

EID: 67650639004     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2009.05.002     Document Type: Article

References (72)

1. Baker T.C., Quero C., Ochieng S.A., and Vickers N.J. Inheritance of olfactory preferences. II. Olfactory receptor neuron responses from Heliothis subflexa × Heliothis virescens hybrid male moths. Brain Behav. Evol. 68 (2006) 75-89
2. Beavis W.D. The power and deceit of QTL experiments: lessons from comparative QTL studies. In: Johnston I.A. (Ed). Proceedings of the 49th Annual Corn and Sorghum Research Conference (1994), ASTA, Washington, DC 250
3. Beavis W.D. QTL analyses: power, precision and accuracy. In: Paterson A.H. (Ed). Molecular Dissection of Complex Traits (1998), CRC Press, NY 145-162
4. Belknap J.K., Mitchell S.R., O'Toole L.A., Helms M.L., and Crabbe J.C. Type I and type II error rates for quantitative trait loci (QTL) mapping studies using recombinant inbred mouse strains. Behav. Genet. 26 (1996) 149-160
5. Bennett B., and Carosone-Link P. Replication of small effect quantitative trait loci for behavioral traits facilitated by estimation of effect size from independent cohorts. Genes Brain Behav. 5 (2006) 404-412
6. Bürger R.K., Schneider A., and Willensdorfer M. The conditions for speciation through intraspecific competition. Evolution 60 (2006) 2185-2206
7. Butlin R. Genetic variation in mating signals and responses. In: Lambert D.M., and Spencer H.G. (Eds). Speciation and the Recognition Concept: Theory and Application (1995), Johns Hopkins Univ. Press, Baltimore, MD 327-366
8. Butlin R., and Trickett A.J. Can population genetic simulations help to interpret pheromone evolution?. In: Cardé R.T., and Minks A.K. (Eds). Insect Pheromone Research: New Directions (1997), Chapman and Hall, New York 548-562
9. Choi M.-Y., Groot A.T., and Jurenka R.A. Pheromone biosynthetic pathways in the moths Heliothis subflexa and Heliothis virescens. Arch. Insect Biochem. Physiol. 59 (2005) 53-58
10. Cossé A.A., Campbell M., Glover T.J., Linn Jr. C.E., Todd J.L., Baker T.C., and Roelofs W.L. Pheromone behavioral responses in unusual male European corn borer hybrid progeny not correlated to electrophysiological phenotypes of their pheromone-specific antennal neurons. Experientia 51 (1995) 809-816
11. Coyne J.A., Barton N.H., and Turelli M. Perspective: a critique of Sewall Wright's shifting balance theory of evolution. Evolution 51 (1997) 643-671
12. Coyne J.A., and Orr H.A. Speciation (2004), Sinauer, Sunderland, MA
13. Dieckmann U., and Doebeli M. On the origin of species by sympatric speciation. Nature 400 (1999) 354-357
14. Dopman E.B., Bogdanowicz S.M., and Harrison R.G. Genetic mapping of sexual isolation between E and Z pheromone strains of the European corn borer (Ostrinia nubilalis). Genetics 167 (2004) 301-309
15. Gerhard H.C. Female mate choice in treefrogs: static and dynamic acoustic criteria. Anim. Behav. 42 (1991) 615-635
16. Gleason J.M., and Ritchie M.G. Do quantitative trait loci (QTL) for a courtship song difference between Drosophila simulans and D. sechellia coincide with candidate genes and intraspecific QTL?. Genetics 166 (2004) 1303-1311
17. Groot A.T., Ward C., Wang J., Pokrzywa A., O'Brien J., Bennett J., Kelly J., Santangelo R.G., Schal C., and Gould F. Introgressing pheromone QTL between species: towards and evolutionary understanding of differentiation in sexual communication. J. Chem. Ecol. 30 (2004) 2495-2514
18. Groot A.T., Fan Y., Brownie C., Jurenka R.A., Gould F., and Schal C. Effect of PBAN on pheromone production in mated Heliothis virescens and Heliothis subflexa females. J. Chem. Ecol. 31 (2005) 15-28
19. Groot A.T., Horovitz J.L., Hamilton J., Santangelo R.G., Schal C., and Gould F. Experimental evidence for interspecific directional selection on moth pheromone communication. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 5858-5863
20. Groot A.T., Santangelo R.G., Ricci E., Brownie C., Gould F., and Schal C. Differential attraction of Heliothis subflexa males to synthetic pheromone lures in Eastern US and Western Mexico. J. Chem. Ecol. 33 (2007) 353-368
21. Groot, A.T., Inglis, O., Bowdridge, S., Santangelo, R.G., Blanco, C., López Jr., J.D., Téran Vargas, A., Gould, F., Schal, C. Geographic and temporal variation in moth chemical communication. Evolution, early online: doi:10.1111/j.1558-5646.2009.00702.x.
22. Haynes K.F. Genetics of pheromone communication in the cabbage looper moth, Trichoplusia ni. In: Cardé R.T., and Minks A.K. (Eds). Insect Pheromone Research: New Directions (1997), Chapman and Hall, New York 525-534
23. Heath R.R., Mitchell E.R., and Cibrian-Tovar J. Effect of release rate and ratio of (Z)-11-hexadecen-1-ol from synthetic pheromone blends on trap capture of Heliothis subflexa (Lepidoptera: Noctuidae). J. Chem. Ecol. 16 (1990) 1259-1268
24. Heckel D.G. Comparative genetic linkage mapping in insects. Annu. Rev. Entomol. 38 (1993) 381-408
25. Heckel D.G., Gahan L.J., Daly J.D., and Trowell S. A genomic approach to understanding Heliothis and Helicoverpa resistance to chemical and biological insecticides. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353 (1998) 1713-1722
26. Jeong S.E., Rosenfield C.-L., Marsella-Herrick P., You K.M., and Knipple D.C. Multiple acyl-CoA desaturase-encoding transcripts in pheromone glands of Helicoverpa assulta, the oriental tobacco budworm. Insect Biochem. Mol. Biol. 3 (2003) 609-622
27. Jurenka R.A. Biochemistry of female moth sex pheromones. In: Blomquist G.J., and Vogt R. (Eds). Insect Pheromones - Biochemistry and Molecular Biology (2003), Academic Press, New York 53-80
28. Jurenka R.A. Insect pheromone biosynthesis. Top. Curr. Chem. 239 (2004) 97-132
29. Klun J.A., Plimmer J.R., and Bierl-Leonhardt B.A. Trace chemicals: essence of sexual communication systems in Heliothis species. Science 204 (1979) 1328-1330
30. Klun J.A., Bierl-Leonhardt B.A., Plimmer J.R., Sparks A.N., Primiani M., Chapman O.L., Lepone G., and Lee G.H. Sex pheromone chemistry of the female tobacco budworm moth Heliothis virescens. J. Chem. Ecol. 6 (1980) 177-183
31. Klun J.A., Leonardt B.A., Lopez J.D., and LaChance L.E. Female Heliothis subflexa (Lepidoptera, Noctuidae) sex pheromone - chemistry and congeneric comparisons. Environ. Entomol. 11 (1982) 1084-1090
32. Knipple D.C., Rosenfield C.-L., Nielsen R., You K.M., and Jeong S.E. Evolution of the integral membrane desaturase gene family in moths and flies. Genetics 162 (2002) 1737-1752
33. Kondrashov A.S., and Kondrashov F.A. Interactions among quantitative traits in the course of sympatric speciation. Nature 400 (1999) 351-354
34. LaForest S., Wu W.Q., and Löfstedt C. A genetic analysis of population differences in pheromone production and response between two populations of the turnip moth, Agrotis segetum. J. Chem. Ecol. 23 (1997) 1487-1503
35. Linn Jr. C.E., and Roelofs W.L. Pheromone communication in moths and its role in the speciation process. In: Lambert D.M., and Spencer H.G. (Eds). Speciation and the Recognition Concept: Theory and Application (1995), Johns Hopkins Univ. Press, Baltimore 263-300
36. Liu W., Ma P.W.K., Marsella-Herrick P., Rosenfield C.-L., Knipple D.C., and Roelofs W. Cloning and functional expression of a cDNA encoding a metabolic acyl-CoA Δ9-desaturase of the cabbage looper moth, Trichoplusia ni. Insect Biochem. Mol. Biol. 29 (1999) 435-443
37. Löfstedt C. Moth pheromone genetics and evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 340 (1993) 161-177
38. Moehring A.J., Li J., Schug M.D., Smith S.G., deAngelis M., Mackay T.F.C., and Coyne J.A. Quantitative trait loci for sexual isolation between Drosophila simulans and D. mauritiana. Genetics 167 (2004) 1265-1274
39. Orr H.A. Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data. Genetics 149 (1998) 2099-2104
40. Park H.Y., Kim M.S., Paek A., Jeong S.E., and Knipple D.C. An abundant acyl-CoA (Δ9) desaturase transcript in pheromone glands of the cabbage moth, Mamestra brassicae, encodes a catalytically inactive protein. Insect Biochem. Mol. Biol. 38 (2008) 581-595
41. Phelan P.L. Genetic and phylogenetics in the evolution of sex pheromones. In: Cardé R.T., and Minks A.K. (Eds). Insect Pheromone Research: New Directions (1997), Chapman and Hall, New York 563-579
42. Pope M.M., Gaston L.K., and Baker T.C. Composition, quantification, and periodicity of sex pheromone gland volatiles from individual Heliothis virescens females. J. Chem. Ecol. 8 (1982) 1043-1055
43. Rafaeli A. Neuroendocrine control of pheromone biosynthesis in moths. Int. Rev. Cytol. 213 (2002) 49-92
44. Raffa K.F., and Dahlsten D.L. Differential responses among natural enemies and prey to bark beetle pheromones. Oecologia 102 (1995) 17-23
45. Raina A.K., Jaffe H., Kempe T.G., Blacher R.W., Fales H.M., Riley C.T., Klun J.A., Ridgway R., and Hayes D.K. Identification of a neuropeptide hormone that regulates pheromone production in female moths. Science 244 (1989) 796-798
46. Raina A.K., Kempe T.G., and Jaffe H. Pheromone biosynthesis activating neuropeptide - regulation of pheromone production in moths. ACS Symp. Ser. 453 (1991) 100-109
47. Ramaswamy S.B., Randle S.A., and Ma W.K. Field evaluation of the sex-pheromone components of Heliothis virescens (Lepidoptera, Noctuidae) in cone traps. Environ. Entomol. 14 (1985) 293-296
48. Roelofs W.L., Hill A.S., Cardé R.T., and Baker T.C. Two sex pheromone components of the tobacco budworm moth, Heliothis virescens. Life Sci. 14 (1974) 1555-1562
49. Roelofs W.L., and Rooney A.P. Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 9179-9184
50. Roelofs W.L., Liu W., Hao G., Jiao H., Rooney A.P., and Linn Jr. C.E. Evolution of moth sex pheromones via ancestral genes. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 13621-13626
51. Rosenfield C.-L., You K.M., Marsella-Herrick P., Roelofs W.L., and Knipple D.C. Structural and functional conservation and divergence among acyl-CoA desaturase-encoding genes of two Noctuid species, the corn earworm, Helicoverpa zea, and the cabbage looper moth, Trichoplusia ni. Insect. Biochem. Mol. Biol. 31 (2001) 949-964
52. Schon C.C., Utz H.F., Groh S., Truberg B., Openshaw S., and Melchinger A.E. Quantitative trait locus mapping based on resampling in a vast maize testcross experiment and its relevance to quantitative genetics for complex traits. Genetics 167 (2004) 485-498
53. Shaw K.L., and Parsons Y.M. Divergence of mate recognition behavior and its consequences for genetic architectures of speciation. Am. Nat. 159 (2002) S61-S75
54. Sheck A.L., and Gould F. The genetic basis of host range in Heliothis virescens. Larval survival and growth. Entomol. Exp. Appl. 69 (1993) 157-172
55. Sheck A.L., and Gould F. A genetic analysis of oviposition behavior of Heliothis virescens and Heliothis subflexa (Lepidoptera: Noctuidae). Environ. Entomol. 24 (1995) 341-347
56. Sheck A.L., Groot A.T., Ward C., Gemeno C., Wang J., Schal C., and Gould F. Genetics of pheromone blend differences between Heliothis virescens and Heliothis subflexa: a chromosome mapping approach. J. Evol. Biol. 19 (2006) 600-617
57. Tabata F., and Ishikawa Y. Genetic basis to divergence of sex pheromones in two closely related moths, Ostrinia scapulalis and O. zealis. J. Chem. Ecol. 31 (2005) 1111-1124
58. Taylor M., Zawadski J., Black B., and Kreitman M. Genome size and endopolyploidy in pyrethroid-resistant and susceptible strains of Heliothis virescens. J. Econ. Entomol. 86 (1993) 1030-1034
59. Teal P.E.A., and Oostendorp A. Effect of interspecific hybridization between Heliothis virescens and H. subflexa (Lepidoptera: Noctuidae) on sex pheromone production by females. J. Insect Physiol. 41 (1995) 519-525
60. Teal P.E.A., and Tumlinson J.H. Effects of interspecific hybridization between Heliothis virescens and Heliothis subflexa on the sex pheromone communication system. In: Cardé R.T., and Minks A.K. (Eds). Insect Pheromone Research: New Directions (1997), Chapman and Hall, New York 535-547
61. Teal P.E.A., Heath R.R., Tumlinson J.H., and McLaughlin J.R. Identification of sex pheromone of Heliothis subflexa (G.) (Lepidoptera: Noctuidae) and field trapping studies using different blends of components. J. Chem. Ecol. 7 (1981) 1011-1022
62. Teal P.E.A., Tumlinson J.H., and Heath R.R. Chemical and behavioral analyses of volatile sex pheromone components released by calling Heliothis virescens (F.) females (Lepidoptera: Noctuidae). J. Chem. Ecol. 12 (1986) 107-126
63. Ting C.-T., Takahashi A., and Wu C.I. Incipient speciation by sexual isolation in Drosophila: concurrent evolution at multiple loci. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 6709-6713
64. Tumlinson J.H., Hendricks P.E., Mitchell E.R., Doolittle R.E., and Brennan M.M. Isolation, identification and synthesis of the sex pheromone of the tobacco budworm. J. Chem. Ecol. 1 (1975) 203-214
65. Tumlinson J.H., Heath R.R., and Teal P.E.A. Analysis of chemical communication systems of Lepidoptera. In: Leonhardt B.A., and Beroza M. (Eds). Insect Pheromone Technology - Chemistry and Applications (1982), Am. Chem. Soc., Washington, DC 1-25
66. Vetter R.S., and Baker T.C. Behavioral responses of male Heliothis virescens in a sustained flight-tunnel to combinations of seven compounds identified from female glands. J. Chem. Ecol. 9 (1983) 747-759
67. Vickers N.J. Defining a synthetic blend attractive to male Heliothis subflexa under wind tunnel conditions. J. Chem. Ecol. 28 (2002) 1255-1267
68. Vickers N.J. Inheritance of olfactory preferences. I. Pheromone-mediated behavioral responses of Heliothis subflexa × Heliothis virescens hybrid male moths. Brain Behav. Evol. 68 (2006) 63-74
69. Vickers N.J. Inheritance of olfactory preferences. III. Processing of pheromonal signals in the antennal lobe of Heliothis subflexa × Heliothis virescens hybrid male moths. Brain Behav. Evol. 68 (2006) 90-108
70. Vickers N.J., and Baker T.C. Chemical communication in heliothine moths. VII. Correlation between diminished responses to point-source plumes and single filaments similarly tainted with a behavioral antagonist. J. Comp. Physiol. A 180 (1997) 523-536
71. Wade M.J., and Goodnight C.J. Perspective: the theories of Fisher and Wright in the context of metapopulations: when nature does many small experiments. Evolution 52 (1998) 1537-1553
72. Whitlock M.C., and Phillips P.C. The exquisite corpse: a shifting view of the shifting balance. TREE 15 (2000) 347-348