Balanced Olfactory Antagonism as a Concept for Understanding Evolutionary Shifts in Moth Sex Pheromone Blends



In the sex pheromone communication systems of moths, both heterospecific sex pheromone components and individual conspecific pheromone components may act as behavioral antagonists when they are emitted at excessive rates and ratios. In such cases, the resulting blend composition does not comprise the sex pheromone of a given species. That is, unless these compounds are emitted at optimal rates and ratios with other compounds, they act as behavioral antagonists. Thus, the array of blend compositions that are attractive to males is centered around the characterized female-produced sex pheromone blend of a species. I suggest here that the resulting optimal attraction of males to a sex pheromone is the result of olfactory antagonistic balance, compared to the would-be olfactory antagonistic imbalance imparted by behaviorally active compounds when they are emitted individually or in other off-ratio blends. Such balanced olfactory antagonism might be produced in any number of ways in olfactory pathways, one of which would be mutual, gamma-aminobutyric-acid-related disinhibition by local interneurons in neighboring glomeruli that receive excitatory inputs from pheromone-stimulated olfactory receptor neurons. Such mutual disinhibition would facilitate greater excitatory transmission to higher centers by projection interneurons arborizing in those glomeruli. I propose that in studies of moth sex pheromone olfaction, we should no longer artificially compartmentalize the olfactory effects of heterospecific behavioral antagonists into a special category distinct from olfaction involving conspecific sex pheromone components. Indeed, continuing to impose such a delineation among these compounds may retard advances in understanding how moth olfactory systems can evolve to allow males to exhibit correct behavioral responses (that is, attraction) to novel sex-pheromone-related compositions emitted by females.


Sex pheromone Moths Lepidoptera Attractant Behavioral antagonist Olfaction Evolution Asymmetric tracking Speciation Reproductive character displacement 


  1. Anton, S., and Homberg, U. 1999. Antennal lobe structure, pp. 97–124, in B. S. Hansson (ed.). Insect OlfactionSpringer, Berlin.Google Scholar
  2. Baker, T. C. 2002. Mechanism for saltational shifts in pheromone communication systems. Proc. Nat. Acad. Sci. USA 99:13368–13370.PubMedCrossRefGoogle Scholar
  3. Baker, T. C., and Heath, J. J. 2004. Pheromones—function and use in insect control, pp. 407–460, in L. I. Gilbert, K. Iatro, and S. S. Gill (eds.). Molecular Insect Science, vol. 6. Elsevier, The Netherlands.Google Scholar
  4. Baker, T. C., Hansson, B. S., Löfstedt, C., and Löfqvist, J. 1989. Adaptation of male moth antennal neurons in a pheromone plume is associated with cessation of pheromone-mediated flight. Chem. Senses 14:439–448.CrossRefGoogle Scholar
  5. Baker, T. C., Fadamiro, H. Y., and Cossé, A. A. 1998. Moth uses fine tuning for odour resolution. Nature (London) 393:530.CrossRefGoogle Scholar
  6. Baker, T. C., Quero, C., Ochieng, S. A., and Vickers, N. J. 2006. Inheritance of olfactory preferences. II. Olfactory receptor neuron responses from Heliothis subflexa x Heliothis virescens hybrid moths. Brain Behav. Evol. 68:75–89.PubMedCrossRefGoogle Scholar
  7. Berg, B. G., Tumlinson, J. H., and Mustaparta, H. 1995. Chemical communication in heliothine moths IV. Receptor neuron responses to pheromone compounds and formate analogs in the male tobacco budworm moth Heliothis virescens. J. Comp. Physiol. A 177:527–534.Google Scholar
  8. Berg, B. G., Almaas, T. J., Bjaalie, J. G., and Mustaparta, H. 1998. The macroglomerular complex of the antennal lobe in the tobacco budworm Heliothis virescens: specified subdivision in four compartments according to information about biologically significant compounds. J. Comp. Physiol. A 183:669–682.CrossRefGoogle Scholar
  9. Berg, B. G., Almaas, T. J., Bjaalie, J. G., and Mustaparta, H. 2005. Projections of male-specific receptor neurons in the antennal lobe of the oriental tobacco budworm moth, Helicoverpa assulta: a unique glomerular organization among related species. J. Comp. Neurol. 486:209–220.PubMedCrossRefGoogle Scholar
  10. Butlin, R. K., and Ritchie, M. G. 1989. Genetic coupling in mate recognition systems: what is the evidence? Biol. J. Linn. Soc. 37:237–246.CrossRefGoogle Scholar
  11. Butlin, R. K., and Trickett, A. J. 1997. Can population genetics simulations help to interpret pheromone evolution?, pp. 548–562, in R. T. Cardé, and A. K. Minks (eds.). Insect Pheromone Research: New DirectionsChapman & Hall, New York.Google Scholar
  12. Cardé, R. T., Cardé, A. M., Hill, A. S., and Roelofs, W. L. 1977. Sex pheromone specificity as a reproductive isolating mechanism among the sibling species Archips argyrospilus and A. mortuanus and other sympatric tortricine moths (Lepidoptera: Tortricidae). J. Chem. Ecol. 3:71–84.CrossRefGoogle Scholar
  13. Christensen, T. A., Waldrop, B. R., Harrow, L. D., and Hildebrand, J. G. 1993. Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J. Comp. Physiol. A 173:385–399.PubMedCrossRefGoogle Scholar
  14. Christensen, T. A., Mustaparta, H., and Hildebrand, J. G. 1995. Chemical communication in heliothine moths. VI. Parallel pathways for information processing in the macroglomerular complex of the tobacco budworm moth Heliothis virescens. J. Comp. Physiol. A 177:545–557.CrossRefGoogle Scholar
  15. Christensen, T. A., Pawlowski, V. M., Lei, H., and Hildbrand, J. G. 2000. Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles. Nat. Neurosci. 3:927–931.PubMedCrossRefGoogle Scholar
  16. Clyne, P., Certel, S., De Bruyne, M., Zaslavsky, L., Johnson, W., and Carlson, J. 1999. The odor specificities of a subset of olfactory receptor neurons are governed by Acj6, a POU-domain transcription factory. Neuron 22:339–347.PubMedCrossRefGoogle Scholar
  17. Cossé, A. A., Campbell, M. G., Glover, T. J., Linn, C. E. Jr., Todd, J. L., Baker, T. C., and Roelofs, W. L. 1995. Pheromone behavioral responses in unusual male European corn borer hybrid progeny not correlated to electrophysiological phenotypes of their pheromone-specific antennal neurons. Experientia 51:809–816.CrossRefGoogle Scholar
  18. De Belle, S., and Kanzaki, R. 1999. Protocerebral olfactory processing, pp. 97–124, in B. S. Hansson (ed.). Insect OlfactionSpringer, Berlin.Google Scholar
  19. De Bruyne, M., Clyne, P. J., and Carlson, J. R. 1999. Odor coding in a model olfactory organ: the Drosophila maxillary palp. J. Neurosci. 19:4520–4532.PubMedGoogle Scholar
  20. De bruyne, M., Foster, K., and Carlson, J. R. 2001. Odor coding in the Drosophila antenna. Neuron 30:537–552.PubMedCrossRefGoogle Scholar
  21. Dethier, V. G. 1971. A surfeit of stimuli, a paucity of receptors. Am. Sci. 59:706–715.Google Scholar
  22. Dobritsa, A. A., Van der goes van naters, W., Warr, C. G., Steinbrecht, R. A., and Carlson, J. R. 2003. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37:827–841.PubMedCrossRefGoogle Scholar
  23. Domingue, M. J., Musto, C. J., Linn, C. E. Jr., Roelofs, W. L., and Baker, T. C. 2007. Evidence of olfactory antagonistic imposition as a facilitator of evolutionary shifts in pheromone blend usage in Ostrinia spp. (Lepidoptera: Crambidae). J. Insect Physiol. 53:488–496.PubMedCrossRefGoogle Scholar
  24. Du, G., and Prestwich, G. D. 1995. Protein structure encodes the ligand binding specificity in pheromone binding proteins. Biochemistry 34:8726–8732.PubMedCrossRefGoogle Scholar
  25. Endo, K., Aoki, T., Yoda, Y., Kimura, K.-I., and Hama, C. 2007. Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages. Nat. Neurosci. 10:153–160.PubMedCrossRefGoogle Scholar
  26. Goldman, A., Van der goes van naters, W., Lessing, D., Warr, C., and Carlson, J. R. 2005. Coexpression of two functional odor receptors in one neuron. Neuron 45:661–666.PubMedCrossRefGoogle Scholar
  27. Grant, A. J., Mayer, M. S., and Mankin, R. W. 1989. Responses from sensilla on the antennae of male Heliothis zea to its major pheromone component and two analogs. J. Chem. Ecol. 15:2625–2634.CrossRefGoogle Scholar
  28. Hallem, E. A., and Carlson, J. R. 2006. Coding of odors by a receptor repertoire. Cell 125:143–160.PubMedCrossRefGoogle Scholar
  29. Hallem, E. A., Ho, M., and Carlson, J. R. 2004. The molecular basis of odor coding in the Drosophila antenna. Cell 117:965–979.PubMedCrossRefGoogle Scholar
  30. Hansson, B. S., and Baker, T. C. 1991. Differential adaptation rates in a male moth’s sex pheromone receptor neurons. Naturwissenschaften 78:517–520.CrossRefGoogle Scholar
  31. Hansson, B. S., and Christensen, T. A. 1999. Functional characteristics of the antennal lobe, pp. 125–161, in B. S. Hansson (ed.). Insect OlfactionSpringer, Berlin.Google Scholar
  32. Hansson, B. S., Tóth, M., Löfstedt, C., Szöcs, G., Subchev, M., and Löfqvist, J. 1990. Pheromone variation among eastern European and a western Asian population of the turnip moth Agrotis segetum. J. Chem. Ecol. 16:1611–1622.CrossRefGoogle Scholar
  33. Hansson, B. S., Dekker, T., and Kárpáti, Z. 2007. Strain-specific pheromone processing in the European corn borer antennal lobe. Abstract, 23rd ISCE Annual Meeting. Jena, Germany, July 2007. pp. 43.Google Scholar
  34. Haynes, K. F. 1997. Genetics of pheromone communication in the cabbage looper, pp. 525–534, in R. T. Cardé, and A. K. Minks (eds.). Pheromone Research: New DirectionsChapman & Hall, New York.Google Scholar
  35. Hildebrand, J. G., and Shepard, G. 1997. Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20:595–631.PubMedCrossRefGoogle Scholar
  36. Ishikawa, Y., Takanashi, T., Kim, C.-G., Hoshizaki, S., Tatsuki, S., and Huang, Y. 1999. Ostrinia spp. in Japan: their host plants and sex pheromones. Entomol. Exp. Appl. 91:237–244.CrossRefGoogle Scholar
  37. Leal, W. S., Chen, A. M., Ishida, Y., Chiang, V. P., Erickson, M. L., Morgan, T. L., and Tsuruda, J. M. 2005. Kinetics and molecular properties of pheromone binding and release. Proc. Natl. Acad. Sci. USA 102:5386–5391.PubMedCrossRefGoogle Scholar
  38. Lee, S.-G., Carlsson, M. A., Hansson, B. S., Todd, J. L., and Baker, T. C. 2006a. Antennal lobe projection destinations of Helicoverpa zea. Male olfactory receptor neurons responsive to heliothine sex pheromone components. J. Comp. Physiol. A. 192:351–363.CrossRefGoogle Scholar
  39. Lee, S.-G., Vickers, N. J., and Baker, T. C. 2006b. Glomerular targets of Helicoverpa subflexa male olfactory receptor neurons housed within long trichoid sensilla. Chem. Senses 9:821–834.CrossRefGoogle Scholar
  40. Linn, C. E. Jr., and Roelofs, W. L. 1981. Modification of sex pheromone blend discrimination in male Oriental fruit moths by pre-exposure to (E)-8-dodecenyl acetate. Physiol. Entomol. 6:421–429.CrossRefGoogle Scholar
  41. Linn, C. E. Jr., Campbell, M. G., and Roelofs, W. L. 1986. Male moth sensitivity to multicomponent pheromones: the critical role of the female released blend in determining the functional role of components and the active space of the pheromone. J. Chem. Ecol. 12:659–668.CrossRefGoogle Scholar
  42. Linn, C. E. Jr., Campbell, M. G., and Roelofs, W. l. 1987. Pheromone components and active spaces: What do male moths smell and where do they smell it? Science 237:650–652.PubMedCrossRefGoogle Scholar
  43. Linn, C. Jr., O’connor, M., and Roelofs, W. L. 2003. Silent genes and rare males: a fresh look at pheromone response specificity in the European corn borer moth, Ostrinia nubilalis. J. Insect Sci. 3:151–6.Google Scholar
  44. Linn, C. Jr., Nojima, S., and Roelofs, W. L. 2005. Antagonist effects of non-host fruit volatiles on discrimination of host fruit by Rhagoletis pomonella flies infesting apple (Malus pumila), hawthorn (Crataegus spp.), and flowering dogwood (Cornus florida). Entomol. Exp. Appl. 114:97–105.CrossRefGoogle Scholar
  45. Linn, C. E. Jr., Domingue, M. J., Musto, C., Baker, T. C., and Roelofs, W. L. 2007a. Support for (Z)-11-hexadecanal as a pheromone antagonist in Ostrinia nubilalis: flight tunnel and single sensillum studies with a New York population. J. Chem. Ecol. 33:909–921.PubMedCrossRefGoogle Scholar
  46. Linn, C. E. Jr., Musto, C. J., and Roelofs, W. L. 2007b. More rare males in Ostrinia: response of Asian corn borer moths to the sex pheromone of the European corn borer. J. Chem. Ecol. 33:199–212.PubMedCrossRefGoogle Scholar
  47. Liu, Y.-B., and Haynes, K. F. 1994. Evolution of behavioral responses to sex pheromone in mutant laboratory colonies of Trichoplusia ni. J. Chem. Ecol. 20:231–238.CrossRefGoogle Scholar
  48. Löfstedt, C. 1990. Population variation and genetic control of pheromone communication systems in moths. Entomol. Exp. Appl. 54:199–218.CrossRefGoogle Scholar
  49. Löfstedt, C. 1993. Moth pheromone genetics and evolution. Phil. Trans. Roy. Soc. B 340:167–177.CrossRefGoogle Scholar
  50. Löfstedt, C., Herrebout, W. M., and Du, J.-W. 1986. Evolution of the ermine moth pheromone tetradecyl acetate. Nature 323:621–623.CrossRefGoogle Scholar
  51. Löfstedt, C., Hansson, B. S., Dijkerman, H. J., and Herrebout, W. M. 1990. Behavioral and electrophysiological activity of unsaturated analogues of the pheromone tetradecenyl acetate in the small ermine moth Yponomeuta rorellus. Physiol. Entomol. 15:47–54.CrossRefGoogle Scholar
  52. Löfstedt, C., Herrebout, W. M., and Menken, J. 1991. Sex pheromones and their potential role in the evolution of reproductive isolation in small ermine moths (Yponomeutidae). Chemoecology 2:20–28.CrossRefGoogle Scholar
  53. Olsson, S. B., Linn, C. E. Jr., and Roelofs, W. L. 2006a. The chemosensory basis for behavioral divergence involved in sympatric host shifts. I. Characterizing olfactory receptor neuron classes responding to key host volatiles. J. Comp. Physiol. A. Neuroethol. Sens. Neural Behav. Physiol. 192:279–288.PubMedCrossRefGoogle Scholar
  54. Olsson, S. B., Linn, C. E. Jr., and Roelofs, W. L. 2006b. The chemosensory basis for behavioral divergence involved in sympatric host shifts II: olfactory receptor neuron sensitivity and temporal firing pattern to individual key host volatiles. J. Comp. Physiol. A. Neuroethol. Sens. Neural Behav. Physiol. 192:289–300.PubMedCrossRefGoogle Scholar
  55. Phelan, P. L. 1992. Evolution of sex pheromones and the role of asymmetric tracking, pp. 265–314, in B. D. Roitberg, and M. B. Isman (eds.). Insect Chemical EcologyChapman & Hall, New York.Google Scholar
  56. Phelan, P. L. 1997. Genetics and phylogenetics in the evolution of sex pheromones, pp. 563–579, in R. T. Cardé, and A. K. Minks (eds.). Insect Pheromone Research, New DirectionsChapman & Hall, New York.Google Scholar
  57. Quero, C., and Baker, T. C. 1999. Antagonistic effect of (Z)-11-hexadecen-1-ol on the pheromone-mediated flight of Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae). J. Insect Behav. 12:701–709.CrossRefGoogle Scholar
  58. Ray, A., Van der goes van naters, W., Shiraiwa, T., and Carlson, J. R. 2007. Mechanisms of odor receptor gene choice in Drosophila. Neuron 53:353–369.PubMedCrossRefGoogle Scholar
  59. Roelofs, W. L., and Brown, R. L. 1982. Pheromones and evolutionary relationships of Tortricidae. Ann. Rev. Ecolog. Syst. 13:395–422.CrossRefGoogle Scholar
  60. Roelofs, W. L., Liu, W., Hao, G., Jiao, H., Rooney, A. P., and Linn, C. E. Jr. 2002. Evolution of moth sex pheromones via ancestral genes. Proc. Natl. Acad. Sci. USA 99:13621–13626.PubMedCrossRefGoogle Scholar
  61. Syed, Z., Ishida, Y., Taylor, K., Kimbrell, D. A., and Leal, W. S. 2006. Pheromone reception in fruit flies expressing a moth’s odorant receptor. Proc. Natl. Acad. Sci. USA 103:16538–16543.PubMedCrossRefGoogle Scholar
  62. Takanashi, T., Ishikawa, Y., Anderson, P., Huang, Y., Löfstedt, C., Tatsuki, S., and Hansson, B. S. 2006. Unusual response characteristics of pheromone-specific olfactory receptor neurons in the Asian corn borer moth Ostrinia furnacalis. J. Exp. Biol. 209:4946–4956.PubMedCrossRefGoogle Scholar
  63. Vickers, N. J. 2002. Defining a synthetic pheromone blend attractive to male Heliothis subflexa under wind tunnel conditions. J. Chem. Ecol. 28:1255–1267.PubMedCrossRefGoogle Scholar
  64. Vickers, N. J., and Baker, T. C. 1997. 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. 180:523–536.CrossRefGoogle Scholar
  65. Vickers, N. J., and Christensen, T. A. 2003. Functional divergence of spatially conserved olfactory glomeruli in two related moth species. Chem. Senses 28:325–338.PubMedCrossRefGoogle Scholar
  66. Vickers, N. J., Christensen, T. A., Mustaparta, H., and Baker, T. C. 1991. Chemical communication in heliothine moths III. Flight behavior of male Helicoverpa zea and Heliothis virescens in response to varying ratios of intra- and interspecific sex pheromone components. J. Comp. Physiol. A 169:275–280.CrossRefGoogle Scholar
  67. Vickers, N. J., Christensen, T. A., and Hildebrand, J. G. 1998. Combinatorial odor discrimination in the brain: attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli. J. Comp. Neurol. 400:35–56.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Center for Chemical Ecology, Department of Entomology, 105 Chemical Ecology LaboratoryPenn State UniversityUniversity ParkUSA

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