Abstract
The differences in the metabolism and endocrine control of reserve mobilization in long-winged (macropterous) and short-winged (brachypterous) males of a flightless firebug (Pyrrhocoris apterus) were studied. We found that protein content in the gut was significantly lower in 5–10 day-old macropterous males due to their fasting and higher in 28 day-old ones than in the same aged brachypterous counterparts as the result of renewed food intake. Overall protease activity was significantly lower in 10–14 day-old macropters, while an abrupt increase in the activity starting on day 21 after adult ecdysis was also associated with renewal of the food intake. The levels of carbohydrates in haemolymph were only slightly lower in 1–10 day-old macropterous males than in the same aged brachypters. However, more than twofold higher lipid content in haemolymph of 7–10 day-old macropterous males than in the same aged brachypterous males was found. Higher mobilization of lipid reserves from the fat bodies in macropterous males was accompanied by more intensive adipokinetic response and higher levels of adipokinetic hormone in the body. It is the first report of endocrine regulation of wing morph-related differences in the lipid mobilization in males of wing-polymorphic insects.
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Abbreviations
- AKH:
-
Adipokinetic hormone
- CNS:
-
Central nervous system
- CC:
-
Corpus cardiacum
- CA:
-
Corpus allatum
- JH:
-
Juvenile hormone
- JHa:
-
Juvenile hormone analogue
References
Applebaum SW (1985) Biochemistry of digestion. In: Kerkut GA, Gilbert LI, (eds), Comprehensive insect physiology, biochemistry and pharmacology, vol 4. Pergamon, Oxford, pp 279–311
Ayali A, Golenser E, Pener MP (1996) Flight fuel related differences between solitary and gregarious locusts (Locusta migratoria migratorioides). Physiol Entomol 21:1–6
Chavira RJ, Burnett TJ, Hagemann JH (1984) Assaying proteinases with azocoll. Anal Biochem 136:446–450
Chen PS (1984) The functional morphology and biochemistry of male accessory glands and their secretions. Annu Rev Entomol 29:233–253
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Goldsworthy GJ (1990) Hormonal control of flight metabolism in locusts. Adv Insect Physiol 17:149–204
Goldsworthy GJ, Kodrík D, Comley R, Lightfoot M (2002) A quantitative study of the adipokinetic hormone of the firebug, Pyrrhocoris apterus. J Insect Physiol 48:1103–1109
Happ GM (1992) Maturation of the male reproductive system and its endocrine regulation. Annu Rev Entomol 37:303–320
Hardie J, Lees AD (1985) Endocrine control of polymorphism and polyphenism. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 8. Pergamon Press, Oxford, pp 441–490
Hodek I (1968) Diapause in females of Pyrrhocoris apterus L (Heteroptera). Acta Entomol Bohemoslov 65:422–435
Hodková 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
Hodková M (2001) Regulation of corpora allata in females of Pyrrhocoris apterus (Heteroptera) (a mini-review). In Vitro Cell Dev Biol Anim 37:560–563
Honěk A (1976) Factors influencing the wing polymorphism in Pyrrhocoris apterus (Heteroptera, Pyrrhocoridae). Zool Jb Syst 103:1–22
Honěk A (1981) Temperature and wing polymorphism in natural populations of Pyrrhocoris apterus L (Heteroptera, Pyrrhocoridae). Zool Jb Syst 108:487–501
Honěk A (1995) Factors and consequences of a non-functional alary polymorphism in Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). Res Popul Ecol 37:111–118
Hrubešová H, Sláma K (1967) The effects of hormones on the intestinal proteinase activity of adult Pyrrhocoris apterus L (Hemiptera). Acta Entomol Bohemoslov 64:175–183
Ketterson ED, Nolan V (1999) Adaptation, exaptation, and constraint: a hormonal perspective. Am Nat 154:S4-S25
Kodrík D, Socha R, Šimek P, Zemek R, Goldsworthy GJ (2000) A new member of the AKH/RPCH family that stimulates locomotory activity in the firebug, Pyrrhocoris apterus (Heteroptera). Insect Biochem Mol Biol 30:489–498
Kodrík D, Socha R, Zemek R (2002) Topical application of Pya-AKH stimulates lipid mobilization and locomotion in the flightless bug, Pyrrhocoris apterus (L) (Heteroptera). Physiol Entomol 27:15–20
Kodrík D, Socha R, Syrová Z (2003) Developmental and diel changes of adipokinetic hormone in CNS and haemolymph of the flightless wing-polymorphic bug, Pyrrhocoris apterus (L). J Insect Physiol 49:53–61
Langellotto GA, Denno RF, Ott JR (2000) A trade-off between flight capability and reproduction in males of a wing-dimorphic insect. Ecology 81:865–875
Maxová A, Kodrík D, Zemek R, Socha R (2001) Diel changes in adipokinetic response and walking activity of Pyrrhocoris apterus (L.) (Heteroptera) in relation to physiological status and wing dimorphism. Eur J Entomol 98:433–438
Mayer RJ, Candy DJ (1969) Control of haemolymph lipid concentration during locust flight: adipokinetic hormone from the corpora cardiaca. J Insect Physiol 15:611–620
Muraleedharan D, Prabhu VKK (1978) Food intake and midgut protease activity in the red cotton bug, Dysdercus cingulatus Fabr. (Heteroptera: Pyrrhocoridae). Entomon 3:11–17
Muraleedharan D, Prabhu VKK (1979) Role of the median neurosecretory cells in secretion of protease and invertase in the red cotton bug, Dysdercus cingulatus. J Insect Physiol 25:237–240
Nijhout HF (1994) Insect Hormones. Princeton University Press, Princeton
Ohtsu T, Kimura MT, Hori SH (1992) Energy storage during reproductive diapause in the Drosophila melanogaster species group. J Comp Physiol B 162:203–208
Rankin MA, Burchsted JCA (1992) The cost of migration in insects. Annu Rev Entomol 37:533–559
Schneider M, Wiesel G, Dorn A (1995) Effects of JH III and JH analogues on phase-related growth, egg maturation and lipid metabolism in Schistocerca gregaria females. J Insect Physiol 41:23–31
Socha R (1993) Pyrrhocoris apterus (Heteroptera) - an experimental model species: a review. Eur J Entomol 1:241–286
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
Socha R, Kodrík D (1999) Differences in adipokinetic responses of Pyrrhocoris apterus (Heteroptera) in relation to wing dimorphism and diapause. Physiol Entomol 24:278–284
Socha R., Šula 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
Socha R, Zemek R (2000a) Wing movement behavior in long- and short-winged morphs of flightless bug Pyrrhocoris apterus L (Heteroptera: Pyrrhocoridae). J Insect Behav 13:741–750
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
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
Socha R, Zemek R (2004) Wing morph-related differences in the pattern of mating activity in a flightless bug, Pyrrhocoris apterus (L) (Heteroptera). Invertebr Reprod Dev 46:11–18
Socha R, Šula 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
Socha R, Šula J, Kodrík D (2001) Sexual activity in macropterous and brachypterous males of a flightless bug, Pyrrhocoris apterus (Heteroptera). Eur J Entomol 98:19–24
Socha R, Šula J, Kodrík 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
Soulages JL, Wells MA (1994) Lipophorin: the structure of an insect lipoprotein and its role in lipid transport in insects. In: Schumaker VN (eds), Advances in protein chemistry, vol 45. Lipoproteins, apolipoproteins, and lipases. Academic, San Diego, pp 371–415
Stoscheck CM (1990) Quantitation of proteins. In: Deutscher MP (ed), Methods in enzymology, vol 182. Academic, London, pp. 50–68
Šula J, Socha R, Zemek R (1998) Wing morph-related physiological differences in adults of temperate population of Pyrrhocoris apterus (L) (Heteroptera: Pyrrhocoridae). Comp Biochem Physiol A 121:365–373
Wedde M, Weise Ch, Kopáček P, Franke P, Vilcinskas A (1998) Purification and characterization of an inducible metalloprotease inhibitor from the hemolymph of greater wax moth larvae, Galleria mellonella. Eur J Biochem 255:535–543
Woodring J, Das S, Kellner R., Gäde G (1990) The sequence of Acheta adipokinetic hormone and the variation in corpus cardiacum content and hyperlipaemic response with age. Z F Naturforsch C 45:1176–1184
Zera AJ, Denno RF (1997) Physiology and ecology of dispersal polymorphism in insects. Annu Rev Entomol 42:207–231
Ziegler R, Schulz M (1986) Regulation of lipid metabolism during flight in Manduca sexta. J Insect Physiol 32:903–908
Zöllner N, Kirsch K (1962) Über die quantitative Bestimmung von Lipoide (Mikromethode) mittels der vielen natürlichen Lipoiden (allen bekannten Plasmalipoiden) gemeinsamen Sulfo-phosphovanillin-Reaktion. Z Ges Exper Med 135:545–561
Acknowledgements
This study was supported by grant no. A 6007301 from the Grant Agency of the Czech Academy of Sciences (RS). The authors thank Mrs. D. Rienesslová and H. Radová for their technical assistance.
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Socha, R., Kodrík, D. & Šula, J. Wing morph-specific differences in the metabolism and endocrine control of reserve mobilization in adult males of a flightless bug, Pyrrhocoris apterus (L.) (Heteroptera). J Comp Physiol B 175, 557–565 (2005). https://doi.org/10.1007/s00360-005-0016-0
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DOI: https://doi.org/10.1007/s00360-005-0016-0