Journal of Chemical Ecology

, Volume 35, Issue 4, pp 405–415 | Cite as

Altered Olfactory Receptor Neuron Responsiveness Is Correlated with a Shift in Behavioral Response in an Evolved Colony of the Cabbage Looper Moth, Trichoplusia ni

  • Michael J. Domingue
  • Kenneth F. Haynes
  • Julie L. Todd
  • Thomas C. Baker
Article

Abstract

There is little understanding of how sex pheromone blends might change during speciation events. For the cabbage looper, Trichoplusia ni, there is a mutant laboratory strain that has exhibited characteristics of a shift to a new pheromone blend. Mutant females produce a blend that is significantly different from wild-type females in having a much higher proportion of a minor pheromone component and lower quantity of the major component. Males in this colony have changed over the years to become more broadly tuned and fly upwind equally well to both the wild-type and mutant female pheromone blends. They also exhibit reduced overall sensitivity to pheromone, flying upwind to either blend at a lower success rate than is typical when wild-type males respond to the wild-type blend. Using single-cell recordings, we examined the olfactory receptor neurons (ORNs) of males from evolved and wild-type colonies for evidence of changes in response characteristics that might explain the above-described behavioral evolution. We found that in evolved-colony males the ORNs tuned to the major sex pheromone component exhibited a somewhat lower responsiveness to that compound than the ORNs of wild-type males. In addition, the minor pheromone component, emitted at excessively high rates by mutant females, elicited a drastically reduced ORN responsiveness in evolved-colony males compared to wild-type males. This alteration in ORN responsiveness may be responsible for allowing evolved males to tolerate the excessive amounts of the minor pheromone component in the mutant female blend, which would normally antagonize the upwind flight of unevolved males. Thus, peripheral olfactory alterations have occurred in T. ni males that are correlated with the evolution of the more broadly tuned, but less sensitive, behavioral response profile.

Keywords

Lepidoptera Electrophysiology Pheromone Evolution Behavior Olfaction Antenna 

Notes

Acknowledgments

Andy Myrick of Penn State University assisted in the statistical calculations. Bonnie Chastain and Shelby Stamper of the University of Kentucky maintained insect colonies.

References

  1. Baker, T. C. 2002. Mechanism for saltational shifts in pheromone communication systems. Proc. National Acad. Sci. U. S. A. 99:13368–13370.PubMedCrossRefGoogle Scholar
  2. Baker, T. C. 2008. Balanced olfactory antagonism as a concept for understanding evolutionary shifts in moth sex pheromone blends. J. Chem. Ecol. 34:971–981.PubMedCrossRefGoogle Scholar
  3. Bjostad, L. B., Linn, C. E., Du, J. -W., and Roelofs, W. L. 1984. Identification of new sex pheromone components in Trichoplusia ni, predicted from biosynthetic precursors. J. Chem. Ecol. 10:1309-1323.CrossRefGoogle Scholar
  4. Cossé, A. A., Todd, J. L., and Baker, T. C. 1998. Neurons discovered on male Helicoverpa zea antennae that correlate with pheromone-mediated attraction and interspecific antagonism. J. Comp. Physiol. A 182:585–594.CrossRefGoogle Scholar
  5. Domingue, M. J., Musto, C. J., Linn Jr., C. E., Roelofs, W. L., and Baker, T. C. 2007a. 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
  6. Domingue, M. J., Musto, C. J., Linn Jr., C. E., Roelofs, W. L., and Baker, T. C.. 2007b. Altered olfactory receptor neuron responsiveness in rare Ostrinia nubilalis males attracted to the O. furnacalis pheromone blend. J. Insect Physiol. 53: 1063–1071.PubMedCrossRefGoogle Scholar
  7. Grant, A. J., Riendeau, C. J., and O’Connell, R. J. 1998. Spatial organization of olfactory receptor neurons on the antenna of the cabbage looper moth. J. Comp. Physiol. A 183:433–442.CrossRefGoogle Scholar
  8. Haynes, K. F. 1997. Genetics of pheromone communication in the cabbage looper moth, Trichoplusia ni, pp. 525–534, in R. T. Cardé and A. K. Minks (eds.). Insect Pheromone Research: New Directions. Chapman and Hall, New York.Google Scholar
  9. Haynes, K. F. and Hunt, R. E. 1990. A mutation in pheromonal communication system of the cabbage looper moth, Trichoplusia ni. J. Chem. Ecol. 16:1249–1257.CrossRefGoogle Scholar
  10. Hemmann, D. J., Allison, J. D., and Haynes, K. F. 2008. Trade-off between sensitivity and specificity in the cabbage looper moth response to sex pheromone. J. Chem. Ecol. 34:1476–1486.PubMedCrossRefGoogle Scholar
  11. Hunt, R. E., and Haynes, K. F. 1990. Periodicity in the quantity and blend ratios of pheromone components in glands and volatile emissions of mutant and normal cabbage looper moths, Trichoplusia ni. J. Insect Physiol. 36:769–774.CrossRefGoogle Scholar
  12. Kaissling, K. -E. 1974. Sensory transduction in insect olfactory receptors, pp. 243–273, in L. Jaenicke (ed.). Biochemistry of Sensory Functions. Springer, Berlin.Google Scholar
  13. Kárpáti, Z., Dekker, T., and Hansson, B. S. 2008. Reversed functional topology in the antennal lobe of the male European corn borer. J. Exp. Biol. 211:2841–2848.PubMedCrossRefGoogle Scholar
  14. Linn, C. E. Jr., Bjostad, L. B., Du, J. W., and Roelofs, W. L. 1984. Redundancy in a chemical signal: behavioral responses of male Trichoplusia ni to a 6-component sex pheromone blend. J. Chem. Ecol. 10:1635–1658.CrossRefGoogle Scholar
  15. Linn, C. E. 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. 3:15 www.insectscience.org/3.15/
  16. Linn, C. E. Jr., Musto, C. J., and Roelofs, W. L. 2007. 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
  17. Liu, Y. -B. and Haynes, K. F. 1994. Evolution of behavioral response to sex pheromone in mutant laboratory colonies of Trichoplusia ni. J. Chem. Ecol. 19:503–515.CrossRefGoogle Scholar
  18. Löfstedt, C. 1990. Population variation and genetic control of pheromone communication systems in moths. Entomol. Exp. Appl. 54:199–218.CrossRefGoogle Scholar
  19. 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 Ecology: An Evolutionary Approach. Chapman and Hall, New York.Google Scholar
  20. Roelofs, W. L., Liu, W. T., Hao, G. X., Jiao, H. M., Rooney, A. P., and Linn, C. E. 2002. Evolution of moth sex pheromones via ancestral genes. Proc. Natl. Acad. Sci. U. S. A. 99:13621–13626.PubMedCrossRefGoogle Scholar
  21. Shorey, H. H. and HHale, R. L. 1965. Mass-rearing of the larvae of nine noctuid species on a simple artificial medium. J. Econ. Entomol . 58:522–524.Google Scholar
  22. Symonds, M. R. E. and Elgar, M. A. 2004. The mode of pheromone evolution: evidence from bark beetles. Proc. R. Soc. Lond. Biol. 271:839–846.CrossRefGoogle Scholar
  23. Symonds, M. R. E. and Wertheim, B. 2005. The mode of evolution of aggregation pheromones in Drosophila species. J. Evol. Biol. 18:1253–1263.PubMedCrossRefGoogle Scholar
  24. Todd, J. L., Haynes K. F., and Baker, T. C. 1992. Antennal neurons specific for redundant pheromone components in normal and mutant Trichoplusia ni males. Physiol. Entomol. 17:183–192.Google Scholar
  25. Van Der Pers, J. N. C. and Den Otter, C. J. 1978. Single cell responses from olfactory receptors of small ermine moths to sex-attractants. J. Insect Physiol. 24:337–343.CrossRefGoogle Scholar
  26. Zhu, J., Chastain, B. C., Spohn, B. G., and Haynes, K. F. 1997. Assortative mating in two pheromone strains of the cabbage looper moth, Trichoplusia ni. J. Insect Behav. 10:805–808.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Michael J. Domingue
    • 1
    • 3
  • Kenneth F. Haynes
    • 2
  • Julie L. Todd
    • 1
  • Thomas C. Baker
    • 1
  1. 1.Center for Chemical Ecology, Department of EntomologyPenn State UniversityUniversity ParkUSA
  2. 2.Department of EntomologyUniversity of KentuckyLexingtonUSA
  3. 3.USDA-ARS, Plant Sciences InstituteBeltsville Area Research CenterBeltsvilleUSA

Personalised recommendations