Skip to main content
Log in

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

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Anton, S., and Homberg, U. 1999. Antennal lobe structure, pp. 97–124, in B. S. Hansson (ed.). Insect OlfactionSpringer, Berlin.

    Google Scholar 

  • Baker, T. C. 2002. Mechanism for saltational shifts in pheromone communication systems. Proc. Nat. Acad. Sci. USA 99:13368–13370.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • Baker, T. C., Fadamiro, H. Y., and Cossé, A. A. 1998. Moth uses fine tuning for odour resolution. Nature (London) 393:530.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • De Belle, S., and Kanzaki, R. 1999. Protocerebral olfactory processing, pp. 97–124, in B. S. Hansson (ed.). Insect OlfactionSpringer, Berlin.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • De bruyne, M., Foster, K., and Carlson, J. R. 2001. Odor coding in the Drosophila antenna. Neuron 30:537–552.

    Article  PubMed  Google Scholar 

  • Dethier, V. G. 1971. A surfeit of stimuli, a paucity of receptors. Am. Sci. 59:706–715.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Du, G., and Prestwich, G. D. 1995. Protein structure encodes the ligand binding specificity in pheromone binding proteins. Biochemistry 34:8726–8732.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hallem, E. A., and Carlson, J. R. 2006. Coding of odors by a receptor repertoire. Cell 125:143–160.

    Article  PubMed  CAS  Google Scholar 

  • Hallem, E. A., Ho, M., and Carlson, J. R. 2004. The molecular basis of odor coding in the Drosophila antenna. Cell 117:965–979.

    Article  PubMed  CAS  Google Scholar 

  • Hansson, B. S., and Baker, T. C. 1991. Differential adaptation rates in a male moth’s sex pheromone receptor neurons. Naturwissenschaften 78:517–520.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

  • 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 

  • Hildebrand, J. G., and Shepard, G. 1997. Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20:595–631.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Löfstedt, C. 1990. Population variation and genetic control of pheromone communication systems in moths. Entomol. Exp. Appl. 54:199–218.

    Article  Google Scholar 

  • Löfstedt, C. 1993. Moth pheromone genetics and evolution. Phil. Trans. Roy. Soc. B 340:167–177.

    Article  Google Scholar 

  • Löfstedt, C., Herrebout, W. M., and Du, J.-W. 1986. Evolution of the ermine moth pheromone tetradecyl acetate. Nature 323:621–623.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Roelofs, W. L., and Brown, R. L. 1982. Pheromones and evolutionary relationships of Tortricidae. Ann. Rev. Ecolog. Syst. 13:395–422.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Vickers, N. J. 2002. Defining a synthetic pheromone blend attractive to male Heliothis subflexa under wind tunnel conditions. J. Chem. Ecol. 28:1255–1267.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I am indebted to Wendell Roelofs, Charles Linn, Jr., and Ken Haynes for many comments and heart-felt constructive criticisms of this paper during its formative stages. I also thank the two anonymous reviewers and Jocelyn Millar of UC Riverside for helping hone this contribution to its present state. The end result does not imply an agreement on their part about the conclusions. Nevertheless, they helped shape the discussion of these issues, which I offer to our semiochemical community through the Journal of Chemical Ecology for inspection, introspection, and perhaps a new way of looking at things. I think I echo my colleagues in saying that I am indebted to the late Professors Robert M. (Milt) Silverstein and John Simeone for their inspiration in leading the founding of the International Society of Chemical Ecology and the Journal of Chemical Ecology.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas C. Baker.

Additional information

Invited Paper, Silverstein/Simeone Lecture, ISCE Meeting Hamburg, Germany

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baker, T.C. Balanced Olfactory Antagonism as a Concept for Understanding Evolutionary Shifts in Moth Sex Pheromone Blends. J Chem Ecol 34, 971–981 (2008). https://doi.org/10.1007/s10886-008-9468-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-008-9468-5

Keywords

Navigation