Skip to main content
SpringerLink
Log in

A comparison of responses from olfactory receptor neurons of Heliothis subflexa and Heliothis virescens to components of their sex pheromone

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Single-cell electrophysiological recordings were obtained from olfactory receptor neurons in sensilla trichodea on male antennae of the heliothine species Heliothis subflexa and the closely related congener H. virescens. A large percentage of sensilla (72% and 81%, respectively, of all sensilla sampled) contained a single odor-responsive receptor neuron tuned to the major pheromone component of both species, Z-11-hexadecenal. A second population of sensilla on H. subflexa antennae (18%) housed receptor neurons that were tuned to Z-9-hexadecenal but also responded with less sensitivity to Z-9-tetradecenal. A similar population of sensilla (4%) on H. virescens male antennae housed receptor neurons that were shown to be tuned specifically only to Z-9-tetradecenal, with no response to even high dosages of Z-9-hexadecenal. A third population of sensilla (comprising 8% and 16% of the sensilla sampled in H. subflexa and H. virescens, respectively) housed two olfactory receptor neurons, one of which was tuned to Z-11-hexadecenyl acetate and the other tuned to Z-11-hexadecenol. In H. subflexa the Z-11-hexadecenyl acetate-tuned neuron also responded to Z-9-tetradecenal with nearly equivalent sensitivity. The behavioral requirements of males of these two species for distinct pheromonal blends was, therefore, reflected by the subtle differences in the tuning properties of antennal olfactory receptor neurons.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2A–C
Fig. 3
Fig. 4. A
Fig. 5
Fig. 6. A
Fig. 7
Fig. 8. A
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

MGC:

macroglomerular complex

ORN:

olfactory receptor neuron

Z9–14:Ald:

(Z)-9-tetradecenal

Z9–16:Ald:

(Z)-9-hexadecenal

Z11–16:Ac:

(Z)-11-hexadecenyl acetate

Z11–16:Ald:

(Z)-11-hexadecenal

Z11–16:OH:

(Z)-11-hexadecenol

References

  • Almaas TJ, Christensen TA, Mustaparta H (1991) Chemical communication in heliothine moths I. Antennal receptor neurons encode several features of intra- and interspecific odorants in the corn earworm moth Helicoverpa zea. J Comp Physiol A 169:249–258

    Google Scholar 

  • Baker TC, Fadamiro HY, Cossé AA (1998) Moth uses fine tuning for odour resolution. Nature 393:530

    Article  CAS  Google Scholar 

  • Berg BG, Tumlinson J, Mustaparta H (1995) Chemical communication in heliothine moths. IV. Receptor neuron responses to pheromone compounds and formate analogues in the male tobacco budworm moth Heliothis virescens. J Comp Physiol A 177:527–534

    CAS  Google Scholar 

  • Berg BG, Almaas TJ, Bjaalie JG, 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 BG, Galizia CG, Brandt R, Mustaparta H (2002) Digital atlases of the antennal lobe in two species of tobacco budworm moths, the oriental Helicoverpa assulta (male) and the American Heliothis virescens (male and female). J Comp Neurol 446:123–134

    Article  PubMed  Google Scholar 

  • Christensen TA (1997) Anatomical and physiological diversity in the central processing of sex-pheromone information in different moth species. In: Cardé RT, Minks AK (eds) Insect pheromone research: new directions. Chapman and Hall, New York, pp 184–193

  • Christensen TA, Mustaparta H, Hildebrand JG (1991) Chemical communication in heliothine moths. II. Central processing of intra- and interspecific olfactory messages in the corn earworm moth Helicoverpa zea. J Comp Physiol A 169:259–274

    Google Scholar 

  • Christensen TA, Mustaparta H, Hildebrand JG (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

    CAS  Google Scholar 

  • Cossé AA, Todd JL, Baker TC (1998) Neurons discovered in male Helicoverpa zea antennae that correlate with pheromone-mediated attraction and interspecific antagonism. J Comp Physiol A 182:585–594

    Article  Google Scholar 

  • Fadamiro HY, Cossé AA, Baker TC (1999) Fine-scale resolution of closely spaced pheromone and antagonist filaments by flying male Helicoverpa zea. J Comp Physiol A 185:131–141

    Google Scholar 

  • Grant AJ, Mayer MS, Mankin RW (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

    Google Scholar 

  • Hansson BS (1995) Olfaction in Lepidoptera. Experientia 51:1003–1027

    CAS  Google Scholar 

  • Hansson BS, Christensen TA (1998) Functional characteristics of the antennal lobe. In: Hansson BS (ed) Insect olfaction. Springer, Berlin Heidelberg New York, pp 125–161

  • Hansson BS, Löfstedt C, Roelofs WL (1987) Inheritance of olfactory response to sex pheromone components in Ostrinia nubilalis. Naturwissenschaften 74:497–499

    CAS  Google Scholar 

  • Hansson BS, Almaas TJ, Anton S (1995) Chemical communication in heliothine moths. V. Antennal lobe projection patterns of pheromone-detecting olfactory receptor neurons in the male Heliothis virescens (Lepidoptera: Noctuidae). J Comp Physiol A 177:535–543

    CAS  Google Scholar 

  • Hartstack AW Jr, Lopez JD, Klun JA, Witz JA, Shaver TN, Plimmer JR (1980) New trap designs and pheromone bait formulation for Heliothis. Proc Beltwide Cotton Prod Res Conf, pp 132–135

  • Heath RR, Mitchell ER, Cibrian-TovarJ (1990) 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 16:1259–1268

    CAS  Google Scholar 

  • Hildebrand JG (1995) Analysis of chemical signals by nervous system. Proc Natl Acad Sci USA 92:67–74

    CAS  PubMed  Google Scholar 

  • Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595–631

    CAS  PubMed  Google Scholar 

  • Kaissling K-E (1974) Sensory transduction in insect olfactory receptors. In: Jaenicke L (ed) Biochemistry of sensory functions. Springer, Berlin Heidelberg New York, pp 243–273

  • Klun JA, Plimmer JR, Bierl-Leonhardt BA, Sparks AN, Chapman OL (1979) Trace chemicals: the essence of sexual communication systems in Heliothis species. Science 204:1328–1330

    CAS  Google Scholar 

  • Klun JA, Plimmer JR, Bierl-Leonhardt BA, Sparks AN, Primiani M, Chapman OL, Lee GH, Lepone G (1980a) Sex pheromone chemistry of female corn earworm moth, Heliothis zea. J Chem Ecol 6:165–175

    CAS  Google Scholar 

  • Klun JA, Plimmer JR, Bierl-Leonhardt BA, Sparks AN, Primiani M, Chapman OL, Lepone G, Lee GH (1980b) Sex pheromone chemistry of female tobacco budworm moth, Heliothis virescens. J Chem Ecol 6:177–183

    CAS  Google Scholar 

  • Klun JA, Leonhardt BA, Lopez JD Jr, Lachance LE (1982) Female Heliothis subflexa (Lepidoptera: Noctuidae) sex pheromone: chemistry and congeneric comparisons. Environ Entomol 11:1084–1090

    Google Scholar 

  • Laster ML (1972) Interspecific hybridization of Heliothis virescens and Heliothis subflexa. Environ Entomol 1:682–687

    Google Scholar 

  • Pope MM, Gaston LK, Baker TC (1984) Composition, quantification, and periodicity of sex pheromone volatiles from individual Heliothis zea females. J Insect Physiol 30:943–945

    CAS  Google Scholar 

  • Proshold FI, Martin DF, Laster ML, Raulston JR, Sparks AN (1983) Release of backcross insects on St. Croix to suppress the tobacco budworm (Lepidoptera: Noctuidae): methodology and dispersal of insects. J Econ Entomol 76:885–891

    Google Scholar 

  • Quero C, Baker TC (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 

  • Quero C., Fadamiro HY, Baker TC (2001) Responses of male Helicoverpa zea to single pulses of sex pheromone and behavioural antagonist. Physiol Entomol 26:106–115

    Article  Google Scholar 

  • Ramaswamy SB, Randle SA, Ma WK (1985) Field evaluation of the sex pheromone components of Heliothis virescens (Lepidoptera: Noctuidae) in cone traps. Environ Entomol 14:293–296

    CAS  Google Scholar 

  • Roelofs WL, Hill AS, Cardé RT, Baker TC (1974) Two sex pheromone components of the tobacco budworm moth, Heliothis virescens. Life Sci 14:1555–1562

    CAS  PubMed  Google Scholar 

  • Sparks AN, Raulston JR, Lingren PD, Carpenter JE, Klun JA, Mullinix BG (1979) Field response of male Heliothis virescens to pheromone stimuli and traps. ESA Bull 2:268–274

    Google Scholar 

  • Teal PEA, Tumlinson JH (1997) Effects of interspecific hybridization between Heliothis virescens and Heliothis subflexa (Lepidoptera: Noctuidae) on the sex pheromone communication system. In Cardé RT, Minks AK (eds) Insect pheromone research: new directions. Chapman and Hall, New York, pp 535–547

  • Teal PEA, Heath RR, Tumlinson JH, McLaughlin JR (1981) Identification of a sex pheromone of Heliothis subflexa (GN.) (Lepidoptera: Noctuidae) and field trapping studies using different blends. J Chem Ecol 7:1011–1022

    Google Scholar 

  • Teal PEA, Tumlinson JH, Heath RR (1986) Chemical and behavioral analyses of volatile sex pheromone components released by calling Heliothis virescens (F.) females (Lepidoptera: Noctuidae). J Chem Ecol 12:107–125

    Google Scholar 

  • Tumlinson, JH, Hendricks PE, Mitchell ER, Doolittle RE, Brennan MM (1975) Isolation, identification and synthesis of the sex pheromone of the tobacco budworm. J Chem Ecol 1:203–214

    Google Scholar 

  • Van der Pers JNC, Den Otter CJ (1978) Single cell responses from olfactory receptors of small ermine moths to sex-attractants. J Insect Physiol 24:337–343

    Article  Google Scholar 

  • Vetter RS, Baker TC (1983) Behavioral responses of male Heliothis virescens in a sustained-flight tunnel to combinations of seven compounds identified from female glands. J Chem Ecol 9:747–759

    CAS  Google Scholar 

  • Vetter RS, Baker TC (1984) Behavioral responses of male Heliothis zea moths in sustained flight-tunnel to combinations of four compounds identified from female sex pheromone gland. J Chem Ecol 10:193–202

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Vickers NJ, Baker TC (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 A 180:523–536

    Article  CAS  Google Scholar 

  • Vickers NJ, Christensen TA (2003) Functional divergence of spatially conserved olfactory glomeruli in two related moth species. Chem Senses 28:325–338

    Article  PubMed  Google Scholar 

  • Vickers NJ, Christensen TA, Mustaparta H, Baker TC (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

    Google Scholar 

  • Vickers NJ, Christensen TA, Hildebrand JG (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  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was funded by a collaborative NSF grant between T.C.B. (IBN-9910783) and N.J.V. (IBN-9905683). We thank Jennifer Harris for rearing many of the H. virescens moths used in this study. David Kelly, Alan Pack, Matt Pond and Keri Swearingen assisted in maintaining the H. subflexa colony. Many thanks to Dr. Fred Gould and co-workers for providing the animals used to establish this colony and suggestions for its maintenance.

Author information

Authors and Affiliations

  1. Department of Entomology, Pesticide Research Laboratory, Penn State University, University Park, PA, 16802, USA

    T. C. Baker, S. G. Lee & J. L. Todd

  2. Department of Entomology, 123 West Walters Hall, Kansas State University, Manhattan, KS, 66506, USA

    S. A. Ochieng’

  3. USDA/ARS, National Center for Agricultural Utilization Research, Peoria, IL, 61604, USA

    A. A. Cossé

  4. Department of Biological Organic Chemistry, IIQAB (CSIC), Jordi Girona 18, 08034, Barcelona, Spain

    C. Quero

  5. Department of Biology, University of Utah, Salt Lake City, UT, 84112, USA

    N. J. Vickers

Authors
  1. T. C. Baker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. A. Ochieng’
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. A. Cossé
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. G. Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. L. Todd
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Quero
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. N. J. Vickers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. C. Baker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baker, T.C., Ochieng’, S.A., Cossé, A.A. et al. A comparison of responses from olfactory receptor neurons of Heliothis subflexa and Heliothis virescens to components of their sex pheromone. J Comp Physiol A 190, 155–165 (2004). https://doi.org/10.1007/s00359-003-0483-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-003-0483-2

Keywords

Search

Navigation