Abstract
Substantial progress has been made toward understanding the neuroendocrine regulation of sex-pheromone glands in Lepidoptera, but several recent studies have revealed that direct contact of the pheromone gland with blood-borne factors is not necessary to induce pheromone biosynthesis and release in some species. The nervous system provides an alternate route of activation. Evidence from several species indicates that the pheromone gland is innervated and regulated by neural activity. Electrical stimulation of efferent axons arising from the terminal abdominal ganglion results in a significant increase in pheromone production, and neural stimulation furthermore evokes the rapid release of pheromone into the surrounding air. In some heliothine moths, the biogenic monoamine octopamine stimulates pheromone production, and octopamine has also been isolated from pheromone gland tissue. Moreover, the critical period for maximal octopamine action mirrors the time when peak levels of octopamine are present in the gland. These findings suggest that octopamine is involved in the regulation of pheromone biosynthesis and/or release, but its actions depend on additional factors associated with age and photoperiod. The combined evidence using anatomical, electrophysiological, and biochemical methods indicates that the pheromone gland is innervated and regulated by neurons that arise in the terminal abdominal ganglion. Indirect evidence suggests that at least some of this innervation is octopaminergic. In these respects, the pheromone gland in Lepidoptera exhibits characteristics of other neuroeffector systems in insects.
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Abernathy, R. L., Nachman, R. J., Teal P. E. A., Yamashita, O. and Tumlinson, J H. (1995) Pheromonotropic activity of naturally occurring pyrokinin insect neuropeptides (FXPRLamides) inHelicoverpa zea. Peptides,16, 215–219.
Altstein, M., Gazit, Y. and Dunkelblum, E. (1993) Neuroendocrine control of sex pheromone biosynthesis inHeliothis peltigera. Arch. Insect Biochem. Physiol,22, 153–168.
Christensen, T. A., Itagaki, H., Teal, P. E. A., Jasensky, R. D., Tumlinson, J. H. and Hildebrand, J. G. (1991) Innervation and neural regulation of the sex pheromone gland in femaleHeliothis moths.Proc. Natl. Acad. Sci. USA,88, 4971–4975.
Christensen, T. A., Lehman, H. K., Teal, P. E. A., Itagaki, H., Tumlinson, J. H. and Hildebrand, J. G. (1992) Diel changes in the presence and physiological actions of octopamine in the female sex-pheromone glands of heliothine moths.Insect Biochem. Molec. Biol.,22, 841–849.
Christensen, T. A., Lashbrook, J. M. and Hildebrand, J. G. (1994) Neural activation of the sex-pheromone gland in the mothManduca sexta: real-time measurement of pheromone release.Physiol. Entomol.,19, 265–270.
Davis, N. T., Homberg, U., Teal, P. E. A., Altstein, M. and Hildebrand, J. G. (1995) Neuroanatomy and immunocytochemistry of the median neurosecretory cells of the subesophageal ganglion of the tobacco hawkmoth,Manduca sexta: immunoreactivity to PBAN and other neuropeptides.Microsc. Res. Tech. (in press).
Fonagy, A., Matsumoto, S., Schoofs, L., DeLoof, A. and Mitsui, T. (1992a)In vivo andin vitro pheromonotropic activity of two locustatachykinin peptides inBombyx mori.Biosci. Biotech. Biochem.,56, 1692–1693.
Fonagy, A., Schoofs, L., Matsumoto, S., DeLoof, A. and Mitsui, T. (1992b) Functional cross-reactivities of some locustamyotropins andBombyx pheromone biosynthesis activating neuropeptide.J. Insect Physiol.,38, 651–657.
Hewes, R. S. and Truman, J. W. (1991) The roles of central and peripheral eclosion hormone release in the control of ecdysis behavior inManduca sexta.J. Comp. Physiol. A,168, 697–707.
Hollander, A. L. and Yin, C.-M. (1982) Neurological influences on pheromone release and calling behavior in the gypsy mothLymantria dispar.Physiol. Entomol.,7, 163–166.
Hollander, A. L. and Yin, C.-M. (1985) Lack of humoral control in calling and pheromone release by brain, corpora cardiaca, corpora allata and ovaries of the female gypsy moth,Lymantria dispar.J. Insect Physiol,31, 159–163.
Homberg, U. (1994)Distribution of Neurotransmitters in the Insect Brain. Stuttgart: Gustav Fischer.
Jacquin, E., Jurenka, R. A., Ljungberg, H., Nagnan, P., Löfstedt, C., Descoins, C. and Roelofs, W. (1994) Control of sex pheromone biosynthesis in the mothMamestra brassicae by the pheromone biosynthesis activating neuropeptide.Insect Biochem. Molec. Biol.,24, 203–211.
Jurenka, R. A., Jacquin, E. and Roelofs, W. L. (1991) Stimulation of pheromone biosynthesis in the mothHelicoverpa zea: action of a brain hormone on pheromone glands involves Ca2+ and cAMP as second messengers.Proc. Natl. Acad. Sci. USA,88, 8621–8625.
Kelly, T. J., Masler, E. P. and Menn, J. J. (1994) Insect neuropeptides: current status and avenues for pest control. InNatural and Engineered Pest Management Agents, ed. P. A. Hedin, J. J. Menn and R. M. Hollingworth. American Chemical Society Symposium Series,551, 292–318.
Kingan, T. G., Blackburn, M. B. and Raina, A. K. (1992) The distribution of pheromone-biosynthesis-activating neuropeptide (PBAN) immunoreactivity in the central nervous system of the corn earworm moth,Helicoverpa zea.Cell Tissue Res.,270, 229–240.
Kuniyoshi, H., Nagasawa, H., Ando, T., Suzuki, A., Nachman, R. J. and Holman, G. M. (1992) Cross-activity between pheromone biosynthesis activating neuropeptide (PBAN) and myotropic pyrokinin insect peptides.Biosci. Biotech. Biochem.,56, 167–168.
Matsumoto, S., Kitamura, A., Nagasawa, H., Kataoka, H., Orikasa, C., Mitsui, T. and Suzuki, A. (1990) Functional diversity of a neurohormone produced by the suboesophageal ganglion: molecular identity of melanization and reddish colouration hormone and pheromone biosynthesis activating neuropeptide.J. Insect Physiol.,36, 427–432.
Nachman, R. J., Kuniyoshi, H., Roberts, V. A., Holman, G. M. and Suzuki, A. (1993) Active conformation of the pyrokinin/PBAN neuropeptide family for pheromone biosynthesis in the silkworm.Biochem. Biophys. Res. Commun.,193, 661–666.
Nässel, D. R. (1993) Neuropeptides in the insect brain: a review.Cell Tissue Res.,273, 1–29.
Passier, P. C. C. M., Vullings, H. G. B., Diederen, J. H. B. and Van der Horst, D. J. (1995) Modulatory effects of biogenic amines on adipokinetic hormone secretion from locust corpora cardiacain vitro.Gen. Comp. Endocrinol.,97, 231–238.
Rafaeli, A. and Gileadi, C. (1995) Modulation of the PBAN-stimulated pheromonotropic activity inHelicoverpa armigera.Insect Biochem. Molec. Bio.,25, 827–834.
Rafaeli, A., Hirsch, J., Soroker, V., Kamensky, B. and Raina, A. K. (1991) Spatial and temporal distribution of PBAN inHelicoverpa (Heliothis) armigera using RIA andin vitro bioassay.Arch. Insect Biochem. Physiol.,18, 119–129.
Rafaeli, A., Soroker, V., Hirsch, J., Kamensky, B. and Raina, A. K. (1993) Influence of photoperiod and age on the competence of pheromone glands and on the distribution of immunoreactive PBAN inHelicoverpa spp.Arch. Insect Biochem. Physiol.,22, 169–180.
Raina, A. K. (1993) Neuroendocrine control of sex pheromone biosynthesis in Lepidoptera.Ann. Rev. Entomol.,38, 329–349.
Raina, A. K. and Menn, J. J. (1993) Pheromone biosynthesis activating neuropeptide: from discovery to current status.Arch. Insect Biochem. Physiol.,22, 141–151.
Ramaswamy, S. B., Jurenka, R. A., Linn, C. E. and Roelofs, W. L. (1995) Evidence for the presence of a pheromonotropic factor in hemolymph and regulation of sex pheromone production inHelicoverpa zea.J. Insect Physiol.,41, 501–508.
Sakurai, S., Warren, J. T. and Gilbert, L. I. (1991) Ecdysteroid synthesis and molting by the tobacco hornworm,Manduca sexta, in the absence of prothoracic glands.Arch. Insect Biochem. Physiol.,18, 13–36.
Tang, J. D., Charlton, R. E., Cardé, R. T. and Yin, C.-M. (1987) Effect of allatectomy and ventral nerve cord transection on calling, pheromone emission and pheromone production inLymantria dispar.J. Insect Physiol,33, 469–476.
Tang, J. D., Charlton, R. E., Jurenka, R. A., Wolf, W. A., Phelan, P. L., Sreng, L. and Roelofs, W. L. (1989) Regulation of pheromone biosynthesis by a brain hormone in two moth species.Proc. Natl. Acad. Sci. USA,86, 1806–1810.
Teal, P. E. A., Tumlinson, J. H. and Oberlander, H. (1989) Neural regulation of sex pheromone biosynthesis inHeliothis moths.Proc. Natl. Acad. Sci. USA,86, 2488–2492.
Thorn, R. S. and Truman, J. W. (1989) Sex-specific neuronal respecification during the metamorphosis of the genital segments of the tobacco hornworm mothManduca sexta.J. Comp. Neurol.,284, 489–503.
Thyagaraja, B. S. and Raina, A. K. (1994) Regulation of pheromone production in the gypsy moth,Lymantria dispar, and development of anin vitro bioassay.J. Insect Physiol.,40, 969–974.
Tublitz, N., Brink, D., Broadie, K. S., Loi, P. and Sylwester, A. W. (1991) From behavior to molecules: an integrated approach to the study of neuropeptides.Trends Neurosci.,14, 254–259.
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Christensen, T.A., Hildebrand, J.G. Neural regulation of sex-pheromone glands in Lepidoptera. Invertebrate Neuroscience 1, 97–103 (1995). https://doi.org/10.1007/BF02331907
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DOI: https://doi.org/10.1007/BF02331907