Eur. J. Entomol. 110 (2): 241-245, 2013 | 10.14411/eje.2013.035

Differential accumulation of energy by the colour morphs of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae) mirrors their ecological adaptations

Seyed Mohammad AHSAEI, Seyed Mohammad TABADKANI*, Vahid HOSSEININAVEH*, Hossein ALLAHYARI, Mahdieh BIGHAM
Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, PO Box 4111, Karaj, Iran

The pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae), is a well-studied species in terms of its colour polymorphism, where it occurs as two distinct colour morphs, red and green. It is proposed that the occurrence and maintenance of this polymorphism is an adaptive response to environmental factors, in particular natural enemies and host plant quality. We hypothesized that these adaptations are directly mirrored in the energy reserves accumulated by the different colour morphs during their pre-adult stages and reflect their specialization for particular ecological roles. We quantitatively measured the different energy reserves of red and green pea aphids and found that the total energy reserves of these morphs did not differ. Interestingly, these reserves were made up of different components in the red and green colour morphs. There was a higher percentage content of water-soluble carbohydrates and lipids in the red clones and higher percentage content of protein in green clones. These finding are in accordance with green clones being more fecund than red ones and needing more protein for reproduction than red clones, which produce more winged offspring when crowded or in response to the presence of natural enemies and so, need more lipids and carbohydrates to fuel their walking and flight. Apparently, different colour morphs are physiologically specialized to adjust their energy reserves in relation to their specific ecological adaptations and maximize their fitness in terms of dispersal, reproduction, defense and survival.

Keywords: Hemiptera, Aphididae, Acyrthosiphon pisum, adaptation, colour morph, dispersal, available energy, environmental factors, pea aphid, polymorphism, reproduction, specialization

Received: October 26, 2012; Accepted: December 11, 2012; Published: April 11, 2013

Download citation

References

  1. AGAWA H. & KAWATA M. 1995: The effect of color polymorphism on mortality in the aphid Macrosiphoniella yomogicola. - Ecol. Res. 10: 301-306 Go to original source...
  2. BRAENDLE C. & WEISSER W.W. 2001: Variation in escape behavior of red and green clones of the pea aphid. - J. Insect Behav. 14: 497-509 Go to original source...
  3. BROWN J.J. 1980: Haemolymph protein reserves of diapausing and nondiapausing codling moth larvae, Cydia pomonella (L.) (Lepidoptera: Tortricidae). - J. Insect Physiol. 26: 487-491 Go to original source...
  4. CAILLAUD M.C. & LOSEY J.E. 2010: Genetics of color polymorphism in the pea aphid, Acyrthosiphon pisum. - J. Insect Sci. 10: 95 Go to original source...
  5. CHAPMAN R.F. 1998: The Insects: Function and Structure. Cambridge University Press, Camridge, 788 pp
  6. DIXON A.F.G. 1985: Aphid Ecology. Chapman and Hall, London, 300 pp
  7. DOWNER R.G.H. & MATTHEWS J.R. 1976: Patterns of lipid distribution and utilization in insects. - Am. Zool. 16: 733-745 Go to original source...
  8. FARHOUDI F. 2012: A Comparison on the Developmentalreproductive Parameters of Red and Green Morphs of Pea Aphid Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) and its Defensive Behavior Against the Ladybird, Hippodamia variegata. MSc thesis, University of Tehran, 73 pp. [in Persian with English abstr.]
  9. FEBVAY G., RAHBE Y., RYNKIEWICZ M., GUILLAUD J. & BONNOT G. 1999: Fate of dietary sucrose and neosynthesis of amino acids in the pea aphid, Acyrthosiphon pisum, reared on different diets. - J. Exp. Biol . 202: 2639-2652
  10. FORAY V., PELISSON P.F., BEL-VENNER M.C., DESOUHANT E., VENNER S., MENU F., GIRON D. & REY B. 2012: A handbook for uncovering the complete energetic budget in insects: the van Handel's method (1985) revisited. - Physiol. Entomol. 37: 295-302 Go to original source...
  11. FUTUYMA D.J. 1986: Evolutionary Biology. 2nd ed. Sinauer Associates, Sunderland, MA, xiv + 600 pp
  12. HANSFORD R.G. & JOHNSON R.H. 1975: The nature and control of tricarboxylate cycle in beetle flight muscle. - Biochem. J. 148: 389-402 Go to original source...
  13. GNAIGER E. 1983: Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In Gnaiger E. & Forstner H. (eds): Polarographic Oxygen Sensors. Aquatic and Physiological Applications. Springer, Berlin, pp. 337-345
  14. KAROWE D.N. & MARTIN M.M. 1989: The effects of quantity and quality of nitrogen diet on the growth, efficiency of food utilization, nitrogen budget, and metabolic rate of fifth-instar Spodoptera eridania larvae (Lepidoptera: Noctuidae). - J. Insect Physiol. 35: 699-708 Go to original source...
  15. LANE A. & WALTERS K.F.A. 1991: Effect of pea aphid (Acyrthosiphon pisum) on the yield of combining peas. - Aspest Appl. Biol. 27: 363-368
  16. LIM S.J & LEE S.S. 1981: The effects of starvation on haemolymph metabolites, fat body, and ovarian development in Oxya japonica (Acrididae: Orthoptera). - J. Insect Physiol. 27: 93-96 Go to original source...
  17. LOSEY J.E., IVES A.R., HARMON J., BROWN C. & BALLANTYNE F. 1997: A polymorphism maintained by opposite patterns of parasitism and predation. - Nature 388: 269-272 Go to original source...
  18. LOUGHEED K. 2012: Photosynthesis-like process found in insects. - Nature (DOI: 10.1038/nature.2012.11214) Go to original source...
  19. LOWRY O.H., ROSEMBROUGH N.J., FARR A.L. & RANDDALL R.J. 1951: Protein measurement with the Folin phenol reagent. - J. Biol. Chem. 193: 267-275
  20. MARKKULA M. 1963: Studies on the pea aphid, Acyrthosiphon pisum, with special reference to the differences in the biology of the green and red forms. - Ann. Agr. Fenn. 2: 1-30
  21. MARTIN M.M. & LIEB T.J. 1979: Patterns of fuel utilization by the thoracic muscles of adult worker ants. The use of lipid by a hymenopteran. - Comp. Biochem. Physiol. 64: 387-390. Go to original source...
  22. MAYNARD SMITH J. 1998: Evolutionary Genetics. 2nd ed. Oxford University Press, Oxford, 354 pp
  23. NEWTON C.J. 1954: Effects of starvation on composition of Japanese beetle larvae (Popillia japonica Newman). - Am. Nat. 85: 337-352
  24. OLSON D.M., FADAMIRO H., LUNDGREN J.G. & HEIMPEL G.E. 2000: Effects of sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp. - Physiol. Entomol. 25: 17-26 Go to original source...
  25. PECCOUD J., OLLIVIER A., PLANTEGENEST M. & SIMON J.C. 2009a: A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. - Proc. Natl. Acad. Sci. USA 106: 7495-7500 Go to original source...
  26. PECCOUD J., SIMON J.C., MCLAUGHLIN H.J. & MORAN N.A. 2009b: Post-Pleistocene radiation of the pea aphid complex revealed by rapidly evolving endosymbionts. - Proc. Natl. Acad. Sci. USA 106: 16315-16320 Go to original source...
  27. PEREZ-MENDOZA J., DOVER B.A., HAGSTRUM D.W. & HOPKINS T.L. 1999: Effect of crowding, food deprivation, and diet on flight initiation and lipid reserves of the lesser grain borer, Rhyzopertha dominica. - Entomol. Exp. Appl. 91: 317-326 Go to original source...
  28. RAIKHEL A.S. & DHADIALLA T.S. 1992: Accumulation of yolk proteins in insect oocytes. - Annu. Rev. Entomol. 37: 217-251 Go to original source...
  29. RANKIN M.A. & BURCHSTED J.C.A. 1992: Cost of migration in insects. - Annu. Rev. Entomol. 37: 533-559 Go to original source...
  30. RIVERO A. & WEST S.A. 2002: The physiological costs of being small in a parasitic wasp. - Evol. Ecol. Res. 4: 407-420
  31. SATAKE S., KAWABE Y. & MIZOGUCHI A. 2000: Carbohydrate metabolism during starvation in the silkworm Bombyx mori. - Arch. Insect Biochem. Physiol. 44: 90-98 Go to original source...
  32. SLANSKI F. JR & SCRIBER M.R. 1985: Food consumption and utilization. In Kerkut S.A. & Gilbert J.F. (eds): Comprehensive Insect Physiology, Biochemistry and Pharmacology. Pergamon Press, Oxford, pp. 87-151
  33. STEVENS N.M. 1904: A study of the germ cells of Aphis rosae and Aphis oenotherae. - J. Exp. Zool. 2: 313-333 Go to original source...
  34. TSUCHIDA T., KOGA R., HORIKAWA M., TSUNODA T., MAOKA T., MATSUMOTO S., SIMON J.C. & FUKATSU T. 2010: Symbiotic bacterium modifies aphid body color. - Science 330: 1102-1104 Go to original source...
  35. URS K.D.C. & HOPKINS T.L. 1973: Effect of moisture on the lipid content and composition of two strains of Tenebrio molitor L. (Coleoptera: Tenebrionidae). - J. Stored Prod. Res. 8: 299-305 Go to original source...
  36. VALMALETTE J.C., DOMBROVSKY A., BRAT P., MERTZ C., CAPOVILLA M. & ROBICHON A. 2012: Light-induced electron transfer and ATP synthesis in a carotene synthesizing insect. - Sci. Rep. 2: 579 Go to original source...
  37. VAN HANDEL E. 1965: Microseparation of glycogen, sugars, and lipids. - Anal. Biochem. 11: 266-271 Go to original source...
  38. VAN HANDEL E. 1985a: Rapid determination of glycogen and sugars in mosquitoes. - J. Am. Mosq. Control Assoc. 1: 299-301
  39. VAN HANDEL E. 1985b: Rapid determination of total lipids in mosquitoes. - J. Am. Mosq. Control Assoc. 1: 302-304
  40. VAN HANDEL E. & DAY J. 1988: Assay of lipids, glycogen and sugars in individual mosquitoes: correlations with wing length in fieldcollected Aedes vexans. - J. Am. Mosq. Control Assoc. 4: 549-550
  41. WEISSER W.W. & BRAENDLE C. 2001: Body color and genetic variation in winged morph production in the pea aphid. - Entomol. Exp. Appl. 99: 217-223 Go to original source...
  42. WHEELER D.E. & BUCK N.A. 1992: Protein, lipid and carbohydrate utilization during metamorphosis in the western fire ant, Solenopsis xyloni. - Physiol. Entomol. 17: 397-403 Go to original source...