Skip to main content

Neuroendocrine regulation of insect development

  • Chapter
Biomechanisms Regulating Growth and Development

Abstract

Insect development is characterized by a series of post-embryonic growth cycles, each culminating with a cuticular molt. Towards the end of each cycle, tissues respond to a complex hormonal millieu and become committed to express the cellular products of their future developmental stage. This hormonal millieu is largely specified by hormones released from two types of endocrine glands; the ecdysone producing prothoracic glands, and juvenile hormone producing corpora allata. Quantitative and qualitative features of the hormonal environment defined by the activities of these glands are largely under neuroendocrine and interendocrine control. As expected, a complex circuit of feedback loops integrates these systems. Specific examples of these developmental endocrine circuits are illustrated with our work on the tobacco hornworm, Manduca sexta.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Schneiderman, H.A. and Gilbert, L.I. 1964. Control of growth and development in insects. Science 143: 325–333.

    Article  PubMed  CAS  Google Scholar 

  2. Williams, C.M. 1967. Third-Generation Pesticides. Scientific American 217: 13–17.

    Article  PubMed  CAS  Google Scholar 

  3. Tobe, S.S. and Feyereisen, R. 1983. Juvenile hormone biosynthesis: Regulation and Assay. In: Endocrinology of Insects (Downer, R.G.H. and Laufer, H. eds.) pp. 161–178, Alan R. Liss, Inc., New York.

    Google Scholar 

  4. Dahm, K.H., Bhaskaran, G., Peter, M.G., Shirk, P.D., Seshan, K.R. and Roller, H. 1976. On the identity of the juvenile hormone in insects. In: The Juvenile Hormones (Gilbert, L.I. ed.), pp. 19–47, Plenum Press, New York.

    Google Scholar 

  5. Schooley, D.A., Judy, K.J., Bergot, B.J., Hall, M.S. and Jennings, R.C. 1976. Determination of the physiological levels of juvenile hormones in several insects and biosynthesis of the carbon skeletons of the juvenile hormones. In: The Juvenile Hormones (Gilbert, L.I. ed.), pp. 101–117, Plenum Press, New York.

    Google Scholar 

  6. Horn, D.H.S. and Bergamasco, R. 1985. Chemistry of ecdysteroids. In: Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 7, (Kerkut, G.A. and Gilbert, G.A. eds.), pp. 185–248. Pergamon Press, Oxford.

    Google Scholar 

  7. Bollenbacher, W.E. 1987. Interendocrine regulation of larval-pupal development in Manduca sexta. J. Insect Physiol. (in press).

    Google Scholar 

  8. Baker, F.C., Tsai, L.W., Reuter, C.C. and Schooley, D.A. 1987. In vivo fluctuation of JH, JH acid, and ecdysteroid titer, and JH esterase activity, during development of fifth stadium Manduca sexta. Insect Biochem. (in press).

    Google Scholar 

  9. Kopec, S. 1922. Studies on the necessity of the brain for the inception of insect metamorphosis. Biol. Bull. 42: 323–342.

    Article  Google Scholar 

  10. Karlson, P. 1983. General considerations and historical perspectives. In: Endocrinology of Insects. (Downer, R.G.H. and Laufer, H. eds.), pp. 1–9, Alan R. Liss Inc., New York.

    Google Scholar 

  11. Sedlack, B.J. 1985. Structure of endocrine glands. In Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 7. (Kerkut, G.A. and Gilbert, L.I. eds.), pp. 25–60, Pergamon Press, Oxford.

    Google Scholar 

  12. Raabe, M. 1982. Insect neurohormones, Plenum Press, New York.

    Google Scholar 

  13. Gupta, A.J. 1983. Neurohemal organs of arthropods, Charles C. Thomas Pub., Springfield, IL.

    Google Scholar 

  14. Eaton, J.L. and Dickens, J.C. 1974. Rectrocerebral endocrine glands and the brain of the adult tobacco hornworm, Manduca sexta (L.). J. Insect Morphol. Embryol. 3: 273–278.

    Article  Google Scholar 

  15. Sedlack, B.J. 1981. An ultrastructural study of neurosecretory fibers within the corpora allata of Manduca sexta. Gen. Comp. Endocrinol. 44: 207–218.

    Article  Google Scholar 

  16. Bhaskaran, G., Jones, G. and Jones, D. 1980. Neuroendocrine regulation of corpus allatum activity in Manduca sexta: Sequential neurohormonal and nervous inhibition in the last-instar larva. Proc. Natl. Acad. Sci. USA 77: 4407–4411.

    Article  PubMed  CAS  Google Scholar 

  17. Granger, N.A., Bollenbacher, W.E. and Gilbert, L.I. 1981. An in vitro approach for investigating the regulation of the corpora allata during larval-pupal metamorphosis. In: Current Topics in Insect Endocrinology and Nutrition, (Bhaskaran, G., Friedman, S. and Rodriguez, J.G. eds.), pp. 83–105, Plenum Press, New York.

    Google Scholar 

  18. Granger, N.A., Niemiec, S.M., Gilbert, L.I. and Bollenbacher, W.E. 1982. Juvenile hormone synthesis in vitro by larval and pupal corpora allata of Manduca sexta. Mol. cell. Endocrinol. 28: 587–604.

    Article  PubMed  CAS  Google Scholar 

  19. Granger, N.A., Mitchell, L.J., Janzen, W.P. and Bollenbacher, W.E. 1984. Activation of Manduca sexta corpora allata in vitro by a cerebral neuropeptide. Mol. cell. Endocrinol. 37: 349–358.

    Article  PubMed  CAS  Google Scholar 

  20. DeKort, C.A.D. and Granger, N.A. 1981. Regulation of the juvenile hormone titer. An. Rev. Entomol. 26: 1–28.

    Article  CAS  Google Scholar 

  21. Feyereisen, R. 1985. Regulation of juvenile hormone titer: Synthesis. In: Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 7, (Kerkut, G.A. and Gilbert, L.I. eds.), pp. 391–429, Pergamon Press, Oxford.

    Google Scholar 

  22. Bollenbacher, W.E., Agui, N., Granger, N.A. and Gilbert, L.I. 1980. Insect prothoracic glands in vitro: A system for studying the prothoracicotropic hormone. In: Invertebrate Systems in vitro. (Kurstak, E., Maramorosch, K. and Dubendorfer, A. eds.), pp. 253–271, Elsevier North Holland, Amsterdam.

    Google Scholar 

  23. Bollenbacher, W.E. and Gilbert, L.I. 1981. Neuroendocrine control of postembryonic development in insects, the prothoracicotropic hormone. In: Neurosecretion: Molecules, Cells, Systems, (Farner, D.S. and Lederis, K. eds.), pp. 361–370, Plenum Press, New York.

    Google Scholar 

  24. Granger, N.A. and Bollenbacher, W.E. 1981. Hormonal control of insect metamorphosis. In: Metamorphosis: A Problem in Developmental Biology. (Gilbert, L.I. and Frieden, E. eds.), pp. 105–137, Plenum Press, New York.

    Google Scholar 

  25. Gilbert, L.I., Bollenbacher, W.E., Agui, N., Granger, N.A., Sedlack, B.J., Gibbs, D. and Buys, C.M. 1981. The prothoracicotropes: Source of prothoracicotropic hormone. Amer. Zool. 21: 641–653.

    CAS  Google Scholar 

  26. Bollenbacher, W.E. and Bowen, M.F. 1983. The prothoracicotropic hormone. In: Endocrinology of Insects. (Laufer, H. and Downer, R.G.H. eds.), pp. 89–99, Alan R. Liss, New York.

    Google Scholar 

  27. Bollenbacher, W.E., Granger, N.A., Smith, W.A. and Gilbert, L.I. 1984. Neurohormonal regulation of molting and metamorphosis in the tobacco hornworm, Manduca sexta. In: Biosynthesis, Metabolism and Mode of Action of Invertebrate Hormones. (Hoffmann, J. and Porchet, M. eds.), pp. 78–91, Springer-Verlag, Berlin.

    Google Scholar 

  28. Bollenbacher, W.E. and Granger, N.A. 1985. Endocrinology of the prothoracicotropic hormone. In: Comprehensive Insect Physiology, Biochemistry and Pharmacology. (Kerkut, G.A. and Gilbert, L.I. eds.), pp. 109–151, Pergamon Press, Oxford.

    Google Scholar 

  29. Agui, N. 1975. Activiation of prothoracic glands by brains in vitro. J. Insect Physiol. 21: 903–913.

    Article  Google Scholar 

  30. Bollenbacher, W.E., Agui, N., Granger, N.A. and Gilbert, L.I. 1979. In vitro activation of insect prothoracic glands by the prothoracicotropic hormone. Proc. Natl. Acad. Sci. USA 76: 5148–5152.

    Article  PubMed  CAS  Google Scholar 

  31. Agui, N., Bollenbacher, W.E. and Gilbert, L.I. 1983. In vitro analysis of prothoracicotropic hormone specificity and prothoracic gland sensitivity in Lepidoptera. Experientia 39: 984–988.

    Article  CAS  Google Scholar 

  32. Agui, N., Bollenbacher, W.E., Granger, N.A. and Gilbert, L.I. 1980. Corpus allatum is release site for insect prothoracicotropic hormone. Nature 285: 669–670.

    Article  CAS  Google Scholar 

  33. Nijhout, H.F. 1975. Axonal pathways in the brain-retrocerebral neuroendocrine complex of Manduca sexta (L.) (Lepidoptera: Sphingidae). Int. J. Insect Morph. Embryol. 4: 529–538.

    Article  Google Scholar 

  34. Buys, C.M. and Gibbs, D. 1981. The anatomy of neurons projecting to the corpus cardiacum from the larval brain of the tobacco hornworm, Manduca sexta (L.). Cell Tiss. Res. 215: 505–513.

    Article  CAS  Google Scholar 

  35. Agui, N., Granger, N.A., Gilbert, L.I. and Bollenbacher, W.E. 1979. Cellular localization of the insect prothoracicotropic hormone: In vitro assay of a single neurosecretory cell. Proc. Natl. Acad. Sci. USA 76: 5694–5698.

    Article  PubMed  CAS  Google Scholar 

  36. Carrow, G.M., Calabrese, R.L. and Williams, C.M. 1984. Architecture and physiology of insect cerebral neurosecretory cells. J. Neurosci. 4: 1034–1044.

    PubMed  CAS  Google Scholar 

  37. Copenhaver, P.F. and Truman, J.W. 1986. Metamorphosis of the cerebral neuroendoerine system in the moth Manduca sexta. J. Comp. Neurol. 249: 186–204.

    Article  PubMed  CAS  Google Scholar 

  38. Kingan, T.G. 1981. Purification of the prothoracicotropic hormone from the tobacco hornworm. Manduca sexta. Life Sci. 28: 2585–2594.

    Article  PubMed  CAS  Google Scholar 

  39. Bollenbacher, W.E. 1984. Chemical and biological properties of the prothoracicotropins of Manduca sexta. In: Insect Neurochemistry and Neurophysiology. (Borkovec, A.B. and Kelly, T.J. eds.), pp. 325–328, Plenum Press, New York.

    Google Scholar 

  40. Bollenbacher, W.E., Katahira, E.J., O’Brien, M., Gilbert, L.I., Thomas, M.K., Agui, N. and Baumhover, A.H. 1984. Insect prothoracicotropic hormone: Evidence for two molecular forms. Science 224: 1243–1245.

    Article  PubMed  CAS  Google Scholar 

  41. O’Brien, M.A., Granger, N.A., Agui, N., Gilbert, L.I. and Bollenbacher, W.E. 1986. Prothoracicotropic hormone in the developing brain of the tobacco hornworm, Manduca sexta: Relative amounts of two molecular forms. J. Insect Physiol. 32: 719–725.

    Article  Google Scholar 

  42. O’Brien, M.A., Flanagan, T.R., Agui, N., Haughton, G., Katahari, E. and Bollenbacher, W.E. 1987. Approaches to generating monoclonal antibodies to the 29 kD prothoracicotropic hormone of Manduca sexta. In: Insect Neurochemistry and Neurophysiology. (Borkovec, A.B. and Gelman, D. eds.), pp. 179–182, Humana Press, Boca Raton, FL.

    Google Scholar 

  43. O’Brien, M.A., Flanagan, T.R., Haughton, G., Arnold, L., Katahari, E. and Bollenbacher, W.E. 1988. A monoclonal antibody to the insect prothoracicotropic hormone J. Neurosci.

    Google Scholar 

  44. Flanagan, T.R., O’Brien, M.A., Agui, N. and Bollenbacher, W.E. 1988. Production of murine antibodies to rare, identifiable neurosecretory cells. Proc. Natl. Acad. Sci. USA.

    Google Scholar 

  45. Wisenton, L.R., Kelly, T.J. and Bollenbacher, W.E. 1987. Multiple forms of cerebral peptides with steroidogenic functions in pupal and adult brains of the yellow fever mosquito, Aedes aegypti. Mol. cell. Endocrinol. 50: 3–14.

    Article  Google Scholar 

  46. Dorn, A., Gilbert, L.I. and Bollenbacher, W.E. 1987. Prothoracicotropic hormone activity in the embryonic brain of the tobacco hornworm, Manduca sexta. J. Comp. Physiol. B 157: 279–283.

    CAS  Google Scholar 

  47. Chen, J.H., Fugo, H., Nakajima, M., Nagasawa, H. and Suzuki, A. 1987. Neurohormones in developing embryos of the silkworm, Bombyx mori: The presence and characteristics of prothoracicotropic hormone B. J. Insect Physiol. 33: 243–248.

    Article  Google Scholar 

  48. Purves, D. and Lichtman, J.W. 1985. Principles of Neural Development. Sinauer Assoc. Inc., Sunderland, MA.

    Google Scholar 

  49. Truman, J.W. 1972. Physiology of insect rhythms I. Circadian Organization of the endocrine events underlying the moulting cycle of larval tobacco hornworms, Manduca sexta. J. exp. Biol. 57: 805–820.

    CAS  Google Scholar 

  50. Truman, J.W. and Riddiford, L.M. 1974. Physiology of insect rhythms III. The temporal Organization of the endocrine events underlying pupation of the tobacco hornworm. J. exp. Biol. 60: 371–382.

    PubMed  CAS  Google Scholar 

  51. Bell, R.A., Rasul, C.G. and Joachim, F.G. 1975. Photoperiodic induction of the pupal diapause in the tobacco hornworm, Manduca sexta. J. Insect Physiol. 21: 1471–1480.

    Article  Google Scholar 

  52. Bodenstein D. 1933. Beintransplantationen an Lepidopteren Raupen. I. Transplantationen zur Analyse der Raupen und Puppenhautung. Wilhelm Roux Archiv. Ent. Mech. 128: 564–583.

    Article  Google Scholar 

  53. Wilson, G.R. and Larsen, J.R. 1974. Debraining and diapause development in Manduca sexta pupae. J. Insect Physiol. 20: 2459–2473.

    Article  PubMed  CAS  Google Scholar 

  54. Bowen, M.F., Bollenbacher, W.E. and Gilbert, L.I. 1984. In vitro studies on the role of the brain and prothoracic glands in the pupal diapause of Manduca sexta. J. exp. Biol. 108: 9–24.

    CAS  Google Scholar 

  55. Truman, J.W. 1976. Extraretinal photoreception in insects. Photochem. Photobiol. 23: 215–225.

    Article  CAS  Google Scholar 

  56. Bowen, M.F., Saunders, D.S., Bollenbacher, W.E. and Gilbert, L.I. 1984. In vitro reprogramming of the photoperiodic clock in an insect brain-retrocerebral complex Proc. Natl. Acad. Sci. USA 81: 5881–5884.

    Article  CAS  Google Scholar 

  57. Bradfield, J.Y. and Denlinger, D.L. 1980. Diapause development in the tabacco hornworm: A role for ecdysone or juvenile hormone? Gen. Comp. Endocrinol. 41: 101–107.

    Article  PubMed  CAS  Google Scholar 

  58. Rountree, D.R. and Bollenbacher, W.E. 1986. The release of the prothoracicotropic hormone in the tobacco hornworm, Manduca sexta, is controlled intrinsically by juvenile hormone. J. exp. Biol. 120: 41–58.

    PubMed  CAS  Google Scholar 

  59. Nijhout, H.F. and Williams, C.M. 1974. Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): Cessation of juvenile hormone secretion as a trigger for pupation. J. exp. Biol. 61: 493–501.

    PubMed  CAS  Google Scholar 

  60. Fain, M.J. and Riddiford, L.M. 1976. Reassessment of the critical periods for prothoracicotropic hormone and juvenile hormone secretion in the larval molt of the tobacco hornworm, Manduca sexta. Gen. Comp. Endocrinol. 30: 131–141.

    Article  PubMed  CAS  Google Scholar 

  61. Carrow, G., Calabrese, R.L. and Williams, C.M. 1981. Spontaneous and evoked release of prothoracicotropin from multiple neurohemal organs of the tobacco hornworm. Proc. Natl. Acad. Sci. USA 78: 5866–5870.

    Article  PubMed  CAS  Google Scholar 

  62. Keeley, L.L. and Hayes, T.K. 1987. Speculations on biotechnology applications for insect neuroendocrine research. Insect Biochem. 17: 639–651.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

George L. Steffens Theron S. Rumsey

Rights and permissions

Reprints and permissions

Copyright information

© 1988 Kluwer Academic Publishers

About this chapter

Cite this chapter

Flanagan, T.R., Tomioka, K., O’brien, M.A., Westbrook, A.L., Agui, N., Bollenbacher, W.E. (1988). Neuroendocrine regulation of insect development. In: Steffens, G.L., Rumsey, T.S. (eds) Biomechanisms Regulating Growth and Development. Beltsville Symposia in Agricultural Research, vol 12. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-1395-0_11

Download citation

  • DOI: https://doi.org/10.1007/978-94-009-1395-0_11

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-7123-9

  • Online ISBN: 978-94-009-1395-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics