Skip to main content
Log in

The Dynamics of Pheromone Gland Synthesis and Release: a Paradigm Shift for Understanding Sex Pheromone Quantity in Female Moths

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

Abstract

Moths are exemplars of chemical communication, especially with regard to specificity and the minute amounts they use. Yet, little is known about how females manage synthesis and storage of pheromone to maintain release rates attractive to conspecific males and why such small amounts are used. We developed, for the first time, a quantitative model, based on an extensive empirical data set, describing the dynamical relationship among synthesis, storage (titer) and release of pheromone over time in a moth (Heliothis virescens). The model is compartmental, with one major state variable (titer), one time-varying (synthesis), and two constant (catabolism and release) rates. The model was a good fit, suggesting it accounted for the major processes. Overall, we found the relatively small amounts of pheromone stored and released were largely a function of high catabolism rather than a low rate of synthesis. A paradigm shift may be necessary to understand the low amounts released by female moths, away from the small quantities synthesized to the (relatively) large amounts catabolized. Future research on pheromone quantity should focus on structural and physicochemical processes that limit storage and release rate quantities. To our knowledge, this is the first time that pheromone gland function has been modeled for any animal.

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

Fig. 1: Model for the pheromone gland of Heliothis virescens and parameter estimations for associated physiological processes through the scotophase (0–480 min)
Fig. 2: Model testing
Fig. 3: Model exploration
Fig. 4: Calling frequency of females of different age

Similar content being viewed by others

References

  • Allison JD, Cardé RT (eds) (2016a) Pheromone communication in moths: evolution, behavior and application. University of Caifornia Press, Oakland, California

    Google Scholar 

  • Allison JD, Cardé RT (2016b) Variation in moth pheromone: causes and consequences. In: Allison JD, Cardé RT (eds) Pheromone communication in moths: evolution, behavior and application. University of California Press, Oakland, pp 25–41

    Google Scholar 

  • Baker TC, Roelofs WL (1981) Initiation and termination of oriental fruit moth male response to pheromone concentrations in the field. Environ Entomol 10:211–218

    Article  Google Scholar 

  • Cardé RT (2016) Moth navigation along pheromone plumes. In: Allison JD, Cardé RT (eds) Pheromone communication in moths: evolution, behavior and application. University of California Press, Berkeley, California, pp 173–189

    Google Scholar 

  • Cardé RT, Baker TC (1984) Sexual communication with pheromones. In: Bell WJ, Cardé RT (eds) Chemical ecology of insects. Chapman and Hall Ltd, London, pp 355–383

  • Christensen TA, Lashbrook JM, Hildebrand JG (1994) Neural activation of the sex-pheromone gland in the moth Manduca sexta: real-time measurement of pheromone release. Physiol Entomol 19:265–270

    Article  CAS  Google Scholar 

  • Crawley MJ (2007) The R book. John Wiley & Sons, Chichester, UK

    Book  Google Scholar 

  • Ding Y-S, Prestwich G (1986) Metabolic transformation of tritium-labeled pheromone by tissues of Heliothis virescens moths. J Chem Ecol 12:411–429. https://doi.org/10.1007/BF01020564

    Article  PubMed  CAS  Google Scholar 

  • DiStefano J III (2013) Dynamic systems biology modeling and simulation ist edn. Academic Press, Cambridge, MA

    Google Scholar 

  • Fang NB, Teal PEA, Tumlinson JH (1995) Characterization of oxidase(s) associated with the sex pheromone gland in Manduca sexta (L) females. Arch Insect Biochem Physiol 29:243–257

    Article  CAS  Google Scholar 

  • Foster S, Anderson K (2011) The use of mass isotopomer distribution analysis to quantify synthetic rates of sex pheromone in the moth Heliothis virescens. J Chem Ecol 37:1208–1210

    Article  PubMed  CAS  Google Scholar 

  • Foster S, Johnson C (2011) Signal honesty through differential quantity in the female-produced sex pheromone of the moth Heliothis virescens. J Chem Ecol 37:717–723

    Article  PubMed  CAS  Google Scholar 

  • Foster SP (2000) The periodicity of sex pheromone biosynthesis, release and degradation in the lightbrown apple moth, Epiphyas postvittana (Walker). Arch Insect Biochem Physiol 43:125–136

    Article  PubMed  CAS  Google Scholar 

  • Foster SP (2005) Lipid analysis of the sex pheromone gland of the moth Heliothis virescens. Arch Insect Biochem Physiol 59:80–90. https://doi.org/10.1002/arch.20058

    Article  PubMed  CAS  Google Scholar 

  • Foster SP (2009) Sugar feeding via trehalose haemolymph concentration affects sex pheromone production in mated Heliothis virescens moths. J Exp Biol 212:2789–2794. https://doi.org/10.1242/jeb.030676

    Article  PubMed  CAS  Google Scholar 

  • Foster SP (2016) Toward a quantitative paradigm for sex pheromone production in moths. In: Allison JD, Cardé RT (eds) Pheromone communication in moths: evolution, behavior and application. University of California Press, Oakland, pp 113–126

    Google Scholar 

  • Foster SP, Anderson KG, Casas J (2017) Sex pheromone in the moth Heliothis virescens is produced as a mixture of two pools: de novo and via precursor storage in glycerolipids. Insect Biochem Mol Biol 87:26–34. https://doi.org/10.1016/j.ibmb.2017.06.004

    Article  PubMed  CAS  Google Scholar 

  • Foster SP, Johnson CP (2010) Feeding and hemolymph trehalose concentration influence sex pheromone production in virgin Heliothis virescens moths J Insect Physiol 56:1617–1623 https://doi.org/10.1016/j.jinsphys.2010.06.002

  • Goodman WG, Cusson M (2012) The juvenile hormones. In: Gilbert LI (ed) Insect endocrinology. Academic Press, San Diego, pp 305–394. https://doi.org/10.1016/B978-0-12-384749-2.10008-1

    Chapter  Google Scholar 

  • Goriely A (2018) Applied mathematics: a very short introduction. Oxford University Press, Oxford, U.K.

    Book  Google Scholar 

  • Greenfield MD (1981) Moth sex pheromones: an evolutionary perspective. Florida Entomol 64:4–17

    Article  Google Scholar 

  • Groot AT (2014) Circadian rhythms of sexual activities in moths: a review. Front Ecol Evol 2. https://doi.org/10.3389/fevo.2014.00043

  • Haefner JW (2005) Modeling biological systems: principles and applications. Springer Science & Business Media, Dordrecht, The Netherlands

    Google Scholar 

  • Harari AR, Steinitz H (2013) The evolution of female sex pheromones. Curr Zoology 59:569–578

    Article  Google Scholar 

  • Harari AR, Zahavi T, Thiéry D (2011) Fitness cost of pheromone production in signaling female moths. Evolution 65:1572–1582. https://doi.org/10.1111/j.1558-5646.2011.01252.x

    Article  PubMed  Google Scholar 

  • Heath RR, McLaughlin JR, Proshold F, Teal PEA (1991) Periodicity of female sex pheromone titer and release in Heliothis subflexa and H. virescens (Lepidoptera: Noctuidae). Ann Entomol Soc Am 84:182–189

    Article  CAS  Google Scholar 

  • Hellerstein MK, Neese RA (1992) Mass isotopomer distribution analysis: a technique for measuring biosynthesis and turnover of polymers. Am J Physiol Endocrinol Metab 263:E988–E1001

  • Johansson B, Jones T (2007) The role of chemical communication in mate choice. Biol Rev Camb Philos Soc 82:265–289. https://doi.org/10.1111/j.1469-185X.2007.00009.x

    Article  PubMed  Google Scholar 

  • Jurenka R (2017) Regulation of pheromone biosynthesis in moths. Curr Opin Insect Sci 24:29–35. https://doi.org/10.1016/j.cois.2017.09.002

    Article  PubMed  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Assoc. Inc., Sunderland, MA

    Google Scholar 

  • Ma PWK, Ramaswamy SB (2003) Biology and ultrastructure of sex pheromone-producing tissue. In: Blomquist GJ, Vogt RC (eds) Insect pheromone biochemsitry and molecular biology. Elsevier Academic Press, London, pp 19–51

    Chapter  Google Scholar 

  • Molina PE (2013) Endocrine physiology. 4th edn. McGraw-Hill, New York, NY

    Google Scholar 

  • Nielsen F, Olsen E, Fredenslund A (1995) Prediction of isothermal evaporation rates of pure volatile organic compounds in occupational environments—a theoretical approach based on laminar boundary layer theory. Ann Occup Hyg 39:497–511. https://doi.org/10.1016/0003-4878(95)00032-A

    Article  CAS  Google Scholar 

  • Nijhout HF, Reed MC (2008) A mathematical model for the regulation of juvenile hormone titers. J Insect Physiol 54:255–264. https://doi.org/10.1016/j.jinsphys.2007.09.008

    Article  PubMed  CAS  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Raina AK, Klun JA, Stadelbacher EA (1986) Diel periodicity and effect of age and mating on female sex pheromone titer in Heliothis zea (Lepidoptera: Noctuidae). Ann Entomol Soc Am 79:128–131

    Article  CAS  Google Scholar 

  • Raina AK, Wergin WP, Murphy CA, Erbe EF (2000) Structural organization of the sex pheromone gland in Helicoverpa zea in relation to pheromone production and release. Arthropod Struct Develop 29:343–353

    Article  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. https://doi.org/10.1016/0024-3205(74)90166-0

    Article  PubMed  CAS  Google Scholar 

  • Soetaert K, Cash J, Mazzia F (2012) Solving differential equations in R. Springer Verlag, Berlin

  • Solari P, Crnjar R, Spiga S, Sollai G, Loy F, Masala C, Liscia A (2007) Release mechanism of sex pheromone in the female gypsy moth Lymantria dispar: a morpho-functional approach. J Comp Physiol A 193:775–785. https://doi.org/10.1007/s00359-007-0232-z

    Article  CAS  Google Scholar 

  • Symonds MRE, Johnson TL, Elgar MA (2012) Pheromone production, male abundance, body size, and the evolution of elaborate antennae in moths. Ecol Evolut 2:227–246. https://doi.org/10.1002/ece3.81

    Article  Google Scholar 

  • Teal PEA, Tumlinson JH (1988) Properties of cuticular oxidases used for sex pheromone biosynthesis by Heliothis zea. J Chem Ecol 14:2131–2145

    Article  PubMed  CAS  Google Scholar 

  • Umbers KDL, Symonds MRE, Kokko H (2015) The Mothematics of female pheromone signaling: strategies for aging virgins. Am Nat 185:417–432. https://doi.org/10.1086/679614

    Article  PubMed  Google Scholar 

  • Webster RP, Cardé RT (1982) Relationship among pheromone titre, calling and age in the omnivorous leafroller moth (Platynota stultana). J Insect Physiol 28:925–933

    Article  CAS  Google Scholar 

  • Weisberg M (2013) Simulation and similarity: using models to understand the world. Oxford University Press, Oxford, U.K.

    Book  Google Scholar 

  • Wolfe RR, Chinkes DL (2005) Isotope tracers in metabolic research, Second Edition. John Wiley & Sons, Inc.

  • Wyatt TD (2014) Pheromones and animal behaviour: chemical signals and signatures. 2nd edn. Cambridge University Press

Download references

Acknowledgements

This work was funded in part by a United States Department of Agriculture Hatch Project ND02388 (to SPF). The purchase of the GC/MS system was funded in part by a United States Department of Agriculture–National Institute of Food and Agriculture Instrument Grant, 2015-07238 (to SPF). We thank Le Studium Loire Valley Institute for Advanced Studies and Dr. D. Giron for supporting the visit of SPF to Tours, where this collaboration was initiated. We also thank Dr. T. Zemb (ICSM, Site de Marcoule) and the INOV group at IRBI for discussions and comments on the work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephen P. Foster.

Electronic supplementary material

ESM 1

(PDF 149 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Foster, S.P., Anderson, K.G. & Casas, J. The Dynamics of Pheromone Gland Synthesis and Release: a Paradigm Shift for Understanding Sex Pheromone Quantity in Female Moths. J Chem Ecol 44, 525–533 (2018). https://doi.org/10.1007/s10886-018-0963-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-018-0963-z

Keywords