Eur. J. Entomol. 105 (4): 575-583, 2008 | DOI: 10.14411/eje.2008.077

Regulation of the development of flight muscles in long-winged adults of the flightless bug Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae)

Radomír SOCHA, Jan ŠULA
Biology Centre ASCR, Institute of Entomology, Branišovská 31, CZ-370 05 České Budějovice, Czech Republic;

We studied the development of the indirect flight muscles and reproductive organs in long-winged (macropterous) adults of the flightless bug Pyrrhocoris apterus (L.) and the factors involved in flight muscles histolysis by means of total protein analysis. Both the extirpation of the corpus allatum, an endocrine gland that is the sole source of juvenile hormone, and sham operation accelerated histolysis and decreased the level of the total protein content of the flight muscles to the same extent. Degeneration of flight muscles was not a result of allatectomy but rather a consequence of injury, followed by resumption of enhanced food intake, because it was stimulated also by the removal of wings. Transfer of penultimate instar larvae to a diapause-inducing short-day photoperiod did not prevent imaginal growth and histolysis of flight muscles, but inhibited growth of ovaries in females and maturation of accessory glands in adult males. Thus inactivation of the corpus allatum in diapausing macropters does not prevent imaginal growth of their flight muscles. Application of a high dose of methoprene to the surface of intact long-day macropterous adults induced precocious histolysis of flight muscles and growth of ovaries in females and accessory glands in males. Prolonged starvation of macropterous adults had only a small effect on the histolysis of their flight muscles. The results indicate that imaginal growth and histolysis of indirect flight muscles in macropterous individuals of P. apterus are largely juvenile hormone-independent processes that are programmed to occur spontaneously, but can be affected by various internal and external factors.

Keywords: Heteroptera, Pyrrhocoridae, Pyrrhocoris apterus, allatectomy, de-alation, diapause, flight muscles, methoprene, proteins, reproductive organs, starvation, firebug

Received: November 15, 2007; Revised: May 19, 2008; Accepted: May 19, 2008; Published: October 24, 2008  Show citation

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SOCHA, R., & ŠULA, J. (2008). Regulation of the development of flight muscles in long-winged adults of the flightless bug Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). EJE105(4), 575-583. doi: 10.14411/eje.2008.077
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References

  1. BORDEN J.H. & SLATER C.E. 1968: Induction of flight muscle degeneration by synthetic juvenile hormone in Ips confusus (Coleoptera: Scolytidae). Z. Vergl. Physiol. 61: 366-368 Go to original source...
  2. DAVIS N.T. 1975: Hormonal control of flight muscle histolysis in Dysdercus fulvoniger. Ann. Entomol. Soc. Am. 68: 710-714 Go to original source...
  3. DE KORT C.A.D. 1990: Thirty-five years of diapause research with the Colorado potato beetle. Entomol. Exp. Appl. 56: 1-13 Go to original source...
  4. DINGLE H. 1985: Migration. In Kerkut G.A. & Gilbert L.I. (eds): Comprehensive Insect Physiology, Biochemistry and Pharmacology. Vol. 9. Pergamon Press, Oxford, pp. 375-415
  5. DINGLE H. & ARORA G. 1973: Experimental studies of migration in bugs of the genus Dysdercus . Oecologia 12: 119-140. Go to original source...
  6. EDWARDS F.J. 1969: Development and histolysis of the indirect flight muscles in Dysdercus intermedius. J. Insect Physiol. 15: 1591-1599 Go to original source...
  7. EDWARDS F.J. 1970: Endocrine control of flight muscle histolysis in Dysdercus intermedius. J. Insect Physiol. 16: 2027-2031 Go to original source...
  8. FINLAYSON L.H. 1975: Development and degeneration. In Usherwood P.N.R. (ed.): Insect Muscle. Academic Press, London, pp. 75-149
  9. GOMI T., OKUDA T. & TANAKA S. 1995: Protein synthesis and degradation in the flight muscles of adult cricket (Gryllus bimaculatus). J. Exp. Biol. 198: 1071-1077 Go to original source...
  10. HARRISON R.G. 1980: Dispersal polymorphism in insects. Annu. Rev. Ecol. Syst. 11: 95-118 Go to original source...
  11. HODEK I. 1968: Diapause in females of Pyrrhocoris apterus L. (Heteroptera). Acta Entomol. Bohemoslov. 65: 422-435
  12. HODKOVA M. 1976: Nervous inhibition of corpora allata by photoperiod in Pyrrhocoris apterus. Nature 263: 521-523 Go to original source...
  13. HODKOVA M. 1982: Interaction of feeding and photoperiod in regulation of the corpus allatum activity in females of Pyrrhocoris apterus L. (Hemiptera). Zool. Jb. Physiol. 86: 477-488
  14. HODKOVA M. 2001: Regulation of corpora allata in females of Pyrrhocoris apterus (Heteroptera) (a mini-review). In Vitro Cell. Dev. Biol. Anim. 37: 560-563 Go to original source...
  15. HODKOVA M. & SOCHA R. 2006: Endocrine regulation of the reproductive arrest in the long-winged females of a flightless bug, Pyrrhocoris apterus (L.). Eur. J. Entomol. 103: 523-529 Go to original source...
  16. HONEK A. 1976: Factors influencing the wing polymorphism in Pyrrhocoris apterus (Heteroptera, Pyrrhocoridae). Zool. Jb. Syst. 103: 1-22
  17. HONEK A. 1981: Temperature and wing polymorphism in natural populations of Pyrrhocoris apterus L. (Heteroptera, Pyrrhocoridae). Zool. Jb. Syst. 108: 487-501
  18. JOHANSSON A.A. 1958: Relation of nutrition to endocrine reproductive functions in the milkweed bug Oncopeltus fasciatus (Dallas) (Heteroptera: Lygaeidae). Nytt. Mag. Zool. 7: 1-132 Go to original source...
  19. JOHNSON C.G. 1969: Migration and Dispersal of Insect by Flight. Methuen, London, xxii + 764 pp
  20. KINGSOLVER J.G. & KOEHL M.A.R. 1994: Selective factors in the evolution of insect wings. Annu. Rev. Entomol. 39: 425-451 Go to original source...
  21. KOBAYASHI M. & ISHIKAWA H. 1994: Involvement of juvenile hormone and ubiquitin-dependent proteolysis in flight muscle breakdown of alate aphid (Acyrthosiphon pisum). J. Insect Physiol. 40: 107-111 Go to original source...
  22. LORENZ M.W. 2007: Oogenesis-flight syndrome in crickets: Age-dependent egg production, flight performance, and biochemical composition of flight muscles in adult females Gryllus bimaculatus. J. Insect Physiol. 53: 819-932 Go to original source...
  23. MARDEN J.H. 2000: Variability in the size, composition, and function of insect flight muscles. Annu. Rev. Entomol. 62: 157-178 Go to original source...
  24. NAIR C.R.M. & PRABHU V.K.K. 1979: Effect of starvation, mating, ovariectomy and juvenile hormone analogue on indirect flight muscle histolysis in Dysdercus cingulatus. Entomon 4: 285-288
  25. NAIR C.R.M. & PRABHU V.K.K. 1985: Entry of proteins from degenerating flight muscles into oocytes in Dysdercus cingulatus (Heteroptera: Pyrrhocoridae). J. Insect Physiol. 31: 383-388 Go to original source...
  26. OLIVER R.H., ALBURY A.N.J. & MOUSSEAU T.A. 2007: Programmed cell death in flight muscle histolysis of the house cricket. J. Insect Physiol. 53: 30-39 Go to original source...
  27. PENER M.P. 1985: Hormonal effects on flight and migration. In Kerkut G.A. & Gilbert L.I. (eds): Comprehensive Insect Physiology, Biochemistry and Pharmacology. Vol. 8. Pergamon Press, Oxford, pp. 491-550 Go to original source...
  28. RANKIN M.A. & BURCHSTED J.C.A. 1992: The cost of migration in insects. Annu. Rev. Entomol. 37: 533-559 Go to original source...
  29. RANKIN M.A. & RIDDIFORD L.M. 1977: Hormonal control of migratory flight in Oncopeltus fasciatus: The effects of the corpus cardiacum, corpus allatum, and starvation on migration and reproduction. Gen. Comp. Endocrinol. 33: 309-321 Go to original source...
  30. ROFF D.A. 1990: The evolution of flightlessness in insects. Ecol. Monogr. 60: 389-421 Go to original source...
  31. ROFF D.A. & FAIRBAIRN D.J. 1991: Wing dimorphisms and the evolution of migratory polymorphisms among the Insecta. Am. Zool. 31: 243-251 Go to original source...
  32. SLAMA K. 1964: Hormonal control of respiratory metabolism during growth, reproduction, and diapause in male adults of Pyrrhocoris apterus (L.) (Hemiptera). Biol. Bull. 127: 499-510 Go to original source...
  33. SLAMA K., ROMANUK M. & SORM F. 1974: Insect Hormones and Bioanalogues. Springer, New York and Wien, ix + 477 pp Go to original source...
  34. SMITH D.S. 1964: The structure and development of flightless Coleoptera: a light and electron microscope study of the wings, thoracic exoskeleton and rudimentary flight musculature. J. Morphol. 114: 107-183 Go to original source...
  35. SOCHA R. 1993: Pyrrhocoris apterus (Heteroptera) - an experimental model species: a review. Eur. J. Entomol. 90: 241-286
  36. SOCHA R. 2001: Latitudinal gradient in response of wing polymorphism to photoperiod in a flightless bug, Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). Eur. J. Entomol. 98: 167-169 Go to original source...
  37. SOCHA R. 2004: Decreased mating propensity of macropterous morph in a flightless wing-polymorphic insect, Pyrrhocoris apterus L. (Heteroptera). Eur. J. Entomol. 101: 539-545 Go to original source...
  38. SOCHA R. 2006: Endocrine control of wing morph-related differences in mating success and accessory gland size in male firebugs. Anim. Behav. 71: 1273-1281 Go to original source...
  39. SOCHA R. 2007: Factors terminating ovarian arrest in longwinged females of a flightless bug, Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). Eur. J. Entomol. 104: 15-22 Go to original source...
  40. SOCHA R. & HODKOVA M. 2006: Corpus allatum volumedependent differences in accessory gland maturation in longand short-winged males of Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). Eur. J. Entomol. 103: 27-32 Go to original source...
  41. SOCHA R. & SULA J. 1996: Differences in haemolymph proteins in relation to diapause and wing dimorphism in Pyrrhocoris apterus (L.) (Heteroptera: Pyrrhocoridae). J. Comp. Physiol. (B) 166: 382-387 Go to original source...
  42. SOCHA R. & SULA J. 2006: Flight muscles polymorphism in a flightless bug, Pyrrhocoris apterus (L.): Developmental pattern, biochemical profile and endocrine control. J. Insect Physiol. 52: 231-239 Go to original source...
  43. SOCHA R. & ZEMEK R. 2000a: Wing movement behavior in longand short-winged morphs of flightless bug Pyrrhocoris apterus L. (Heteroptera: Pyrrhocoridae). J. Insect Behav. 13: 741-750 Go to original source...
  44. SOCHA R. & ZEMEK R. 2000b: Locomotor activity in adult Pyrrhocoris apterus (Heteroptera) in relation to sex, physiological status and wing dimorphism. Physiol. Entomol. 25: 383-389 Go to original source...
  45. SOCHA R. & ZEMEK R. 2003: Wing morph-related differences in the walking pattern and dispersal in a flightless bug, Pyrrhocoris apterus (L.) (Heteroptera). Oikos 100: 35-43 Go to original source...
  46. SOCHA R. & ZEMEK R. 2007: Temporal pattern of feeding activity in the firebug Pyrrhocoris apterus and its relation to sex, wing dimorphism and physiological state of adults. Physiol. Entomol. 32: 16-25. Go to original source...
  47. SOCHA R., SULA J. & ZEMEK R. 1997: Feeding, drinking and digestive enzyme activities in short- and long-day females of Pyrrhocoris apterus (Heteroptera). Physiol. Entomol. 22: 161-169 Go to original source...
  48. SOCHA R., SULA J. & ZEMEK R. 1998: Feeding behaviour, digestive physiology and lipid content in macropterous females of Pyrrhocoris apterus (L.) (Heteroptera: Pyrrhocoridae). Physiol. Entomol. 23: 91-96 Go to original source...
  49. SOCHA R., SULA J. & KODRIK D. 2004: Wing morph-related differences in developmental pattern of accessory gland proteins in adult males of Pyrrhocoris apterus (L.) and their endocrine control. J. Insect Physiol. 50: 893-901 Go to original source...
  50. SOCHA R., SULA J., KODRIK D. & GELBIC I. 1991: Hormonal control of vitellogenin synthesis in Pyrrhocoris apterus (L.) (Heteroptera). J. Insect Physiol. 37: 805-816 Go to original source...
  51. STOSCHECK C.M. 1990: Quantitation of proteins. In Deutscher M.P. (ed.): Methods in Enzymology. Vol. 182. Academic Press, London, pp. 50-68 Go to original source...
  52. TANAKA S. 1994: Endocrine control of ovarian development and flight muscle histolysis in a wing dimorphic cricket, Modicogryllus confirmatus. J. Insect Physiol. 40: 483-490 Go to original source...
  53. TOBE S.S. & CHAPMAN C.S. 1979: The effect of starvation and subsequent feeding on juvenile hormone synthesis and oocyte growth in Schistocerca americana gregaria. J. Insect Physiol. 25: 701-708 Go to original source...
  54. WEAVER R.J. & PRATT G.E. 1981: Effect of starvation and feeding upon corpus allatum activity and oocyte growth in adult female Periplaneta americana. J. Insect Physiol. 27: 75-83 Go to original source...
  55. ZERA A.J. & DENNO R.F. 1997: Physiology and ecology of dispersal polymorphism in insects. Annu. Rev. Entomol. 42: 207-231 Go to original source...

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