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.




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References
Allison JD, Cardé RT (eds) (2016a) Pheromone communication in moths: evolution, behavior and application. University of Caifornia Press, Oakland, California
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
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
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
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
Crawley MJ (2007) The R book. John Wiley & Sons, Chichester, UK
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
DiStefano J III (2013) Dynamic systems biology modeling and simulation ist edn. Academic Press, Cambridge, MA
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
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
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
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
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
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
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
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
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
Goriely A (2018) Applied mathematics: a very short introduction. Oxford University Press, Oxford, U.K.
Greenfield MD (1981) Moth sex pheromones: an evolutionary perspective. Florida Entomol 64:4–17
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
Harari AR, Steinitz H (2013) The evolution of female sex pheromones. Curr Zoology 59:569–578
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
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
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
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
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Assoc. Inc., Sunderland, MA
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
Molina PE (2013) Endocrine physiology. 4th edn. McGraw-Hill, New York, NY
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
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
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
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
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
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
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
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
Teal PEA, Tumlinson JH (1988) Properties of cuticular oxidases used for sex pheromone biosynthesis by Heliothis zea. J Chem Ecol 14:2131–2145
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
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
Weisberg M (2013) Simulation and similarity: using models to understand the world. Oxford University Press, Oxford, U.K.
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
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.
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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
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DOI: https://doi.org/10.1007/s10886-018-0963-z


