Advertisement

Journal of Chemical Ecology

, Volume 35, Issue 1, pp 1–7 | Cite as

Biparental Endowment of Endogenous Defensive Alkaloids in Epilachna paenulata

  • Soledad Camarano
  • Andrés González
  • Carmen Rossini
Article

Abstract

Coccinellid beetles contain a variety of defensive alkaloids that render them unpalatable to predators. Epilachna paenulata (Coleoptera: Coccinellidae) is a South American ladybird beetle that feeds on plants of the Cucurbitaceae family. The defensive chemistry of E. paenulata has been characterized as a mixture of systemic piperidine, homotropane, and pyrrolidine alkaloids. Whole body extracts of adult beetles contain four major alkaloids: 2-(2′-oxopropyl)-6-methylpiperidine (1); 1-(6-methyl-2,3,4,5-tetrahydro-pyridin-2-yl)-propan-2-one (2); 1-methyl-9-azabicyclo[3.3.1]nonan-3-one (3); and 1-(2″-hydroxyethyl)-2-(12′-aminotridecyl)-pyrrolidine (4). Comparative studies of the defensive chemistry of eggs, larvae, pupae, and adults showed differences in alkaloid composition and concentration among life stages. While adults contained mainly the homotropane 1-methyl-9-azabicyclo[3.3.1]nonan-3-one (3), eggs showed the highest concentration of the piperidine 2-(2′-oxopropyl)-6-methylpiperidine (1). We studied the origin of this alkaloid in the eggs by feeding newly emerged, virgin adult beetles with [2-13C]-labeled acetate, and by performing crosses between 13C-fed and unlabeled males and females. GC-MS analysis of alkaloids from 13C-fed males and females showed high incorporation of 13C into the alkaloids, as evidenced from a 20–30% increase of isotopic peaks in diagnostic fragment ions, confirming the expected endogenous origin of these alkaloids. In addition, analyses of eggs from different crosses showed that labeled alkaloids from both parents are incorporated into eggs, indicating that E. paenulata males transfer alkaloids to the females at mating. Biparental endowment of chemical defenses into eggs has been shown previously in insects that acquire defensive compounds from dietary sources. To our knowledge, this is the first report of biparental egg endowment of endogenous defenses.

Keywords

Epilachna paenulata Nuptial gift Biparental endowment Egg defense Coleoptera Coccinellidae 

Notes

Acknowledgments

We are thankful for the financial support from the National Institutes of Health (NIH-USA), the International Foundation for Science (IFS), and the Program for the Development of Basic Sciences (PEDECIBA, Uruguay).

Supplementary material

10886_2008_9570_MOESM1_ESM.doc (100 kb)
ESM 1 (DOC 100 KB)

References

  1. Attygalle, A., McCormick, K., Blankespoor, C., Eisner, T., and Meinwald, J. 1993a. Azamacrolides: A family of alkaloids from the pupal defensive secretion of a ladybird beetle (Epilachna varivestis). Proc. Natl. Acad. Sci. USA 90:5204–5208.PubMedCrossRefGoogle Scholar
  2. Attygalle, A., Shang-Cheng, X., McCormick, K., Meinwald, J., Blankespoor, C., and Eisner, T. 1993b. Alkaloids of the Mexican bean beetle, Epilachna varivestis (Coccinellidae). Tetrahedron 49:9333–9342.CrossRefGoogle Scholar
  3. Attygalle, A., Blankespoor, C., Eisner, T., and Meinwald, J. 1994. Biosynthesis of a defensive insect alkaloid: Epilachnene from oleic acid and serine. Proc. Nat. Acad. Sci. USA 91:12790–12793.PubMedCrossRefGoogle Scholar
  4. Attygalle, A., Svatos, A., Veith, M., Farmer, J., Meinwald, J., Smedley, S., González, A., and Eisner, T. 1999. Biosynthesis of epilachnene, a macrocyclic defensive alkaloid of the Mexican bean beetle. Tetrahedron 55:955–966.CrossRefGoogle Scholar
  5. Blum, M. S. 1992. Ingested allelochemicals insect wonderland: a menu of remarkable functions. Amer. Entomol. 38:222–234.Google Scholar
  6. Braekman, J. C., Charlier, A., Daloze, D., Heilporn, S., Pasteels, J. M., Plasman, V., and Wang, S. F. 1999. New piperidine alkaloids from two ladybird beetles of the genus Calvia (Coccinellidae). Eur. J. Org. Chem. 1749–1755.Google Scholar
  7. Camarano, S. 2008. Estudios de biosíntesis y flujo de defensas químicas en Epilachna paenulata (Coleoptera: Coccinellidae). Departamento de Química Orgánica, Universidad de la República, Montevideo.Google Scholar
  8. Camarano, S., González, A., and Rossini, C. 2006. Chemical defense of the ladybird beetle Epilachna paenulata. Chemoecology 16:179–184.CrossRefGoogle Scholar
  9. Carrel, J., Doom, J., and McCormick, J. L. 1986. Identification of cantharidin in false blister beetles (Coleoptera, Oedemeridae) from Florida. J. Chem. Ecol. 12:741–747.CrossRefGoogle Scholar
  10. Carrel, J. E., McCairel, M. H., Slagle, A. J., Doom, J. P., Brill, J., and McCormick, J. P. 1993. Cantharidin production in a blister beetle. Experientia 49:171–174.PubMedCrossRefGoogle Scholar
  11. Dewick, P. 1997. Medicinal Natural Products: A Biosynthetic Approach. John Wiley & Sons Ltd, West Sussex.Google Scholar
  12. Dussourd, D., Ubik, K., Harvis, C., Resch, J., Meinwald, J., and Eisner, T. 1988. Biparental defensive endowment of eggs with acquired plan alkaloid in the moth Utetheisa ornatrix. Proc. Natl. Acad. Sci. USA 85:5992–5996.PubMedCrossRefGoogle Scholar
  13. Eisner, T., Goetz, M., Aneshansley, D., Ferstandig, A., and Meinwald, J. 1986. Defensive alkaloid in blood of Mexican bean beetle Epilachna varivestis. Experientia 42:204–207.PubMedCrossRefGoogle Scholar
  14. Eisner, T., Rossini, C., González, A., Iyengar, V., Siegler, M., and Smedley, S. 2002. Paternal investment in egg defence, pp. 91–116, in M. Hilker, and T. Meiners (eds.). Chemoecology of Insect Eggs and Egg DepositionBlackwell Publishing, Berlin.Google Scholar
  15. Farmer, J., Attygalle, A., Smedley, S., Eisner, T., and Meinwald, J. 1997. Absolute configuration of insect-produced epilachnene. Tetrahedron Lett 38:2787–2790.CrossRefGoogle Scholar
  16. Ferguson, J. E., Metcalf, R. L., and Fischer, D. C. 1985. Disposition and fate of cucurbitacin B in five species of diabroticites. J. Chem. Ecol. 11:1307–1321.CrossRefGoogle Scholar
  17. Glisan King, A., and Meinwald, J. 1996. Review of the defensive chemistry of Coccinellids. Chem. Rev.96:1105–1122.PubMedCrossRefGoogle Scholar
  18. González, A., Hare, J. F., and Eisner, T. 1999a. Chemical egg defence in Photuris firefly “femmes fatales”. Chemoecology 9:177–185.CrossRefGoogle Scholar
  19. González, A., Rossini, C., Eisner, M., and Eisner, T. 1999b. Sexually transmitted chemical defense in a moth (Utetheisa ornatrix). Proc. Natl. Acad. Sci. USA 96:5570–5574.PubMedCrossRefGoogle Scholar
  20. Hartmann, T. 1999. Chemical ecology of pyrrolizidine alkaloids. Planta 207:483–495.CrossRefGoogle Scholar
  21. Hess, S., Van Beek, J., and Pannell, L. 2002. Acid hydrolysis of silk fibroins and determination of the enrichment of isotopically labeled amino acids using precolumn derivatization and high performance liquid chromatography-electrospray ionization-mass spectrometry. Anal. Biochem. 311:19–26.PubMedCrossRefGoogle Scholar
  22. Hilker, M. 1994. Egg deposition and protection of eggs in Chrysomelidae, pp. 263–276, in P. H. Jolivet, M. L. Cox, and E. Petitpierre (eds.). Novel Aspects of the Biology of ChrysomelidaeKluwer Academic Publishers, Dordrecht.Google Scholar
  23. Hinton, H. E. 1981. Biology of Insect Eggs. Pergamon Press, Oxford.Google Scholar
  24. Holz, C., Streil, G., Dettner, K., Dütemeyer, J., and Boland, W. 1994. Intersexual transfer of a toxic terpenoid during copulation and its paternal allocation to developmental stages: quantification of cantharidin in oedemerids and pyrochroids. Zeitschrift füe Naturforschung 49c:856–864.Google Scholar
  25. Laurent, P., Lebrun, B., Braekman, J., Daloze, D., and Pasteels, J. 2001. Biosynthetic studies on adaline and adalinine, two alkaloids from ladybird beetles (Coleoptera: Coccinellidae). Tetrahedron 51:3403–3412.CrossRefGoogle Scholar
  26. Laurent, P., Braekman, J. C., Daloze, D., and Pasteels, J. 2002. In vitro production of adaline and coccinelline, two defensive alkaloids from ladybird beetles (Coleoptera: Coccinellidae). Insect Biochem. & Mol. Biol. 32:1017–1023.CrossRefGoogle Scholar
  27. McCormick, J. L., and Carrel, J. 1987. Cantharidin Biosynthesis and Function in Meloid BeetlesAcademic Press, New York.Google Scholar
  28. Meyer, D., Schlatter, C., Schlatter-LAnz, I., Schmid, H., and Bovey, P. 1968. Die Zucht von Lytta vesicatoria im Laboratorium und Nachweis der Cantharidinsynthese in Larven. Experientia 24:995–998.PubMedCrossRefGoogle Scholar
  29. Nikbakhtzadeh, M. R., Dettner, K., Boland, W., Gade, G., and Dotterl, S. 2007. Intraspecific transfer of cantharidin within selected members of the family Meloidae (Insecta: Coleoptera). J. Insect Physiol. 53:890–899.PubMedCrossRefGoogle Scholar
  30. Nishida, R., and Fukami, H. 1989. Ecological adaptation of an Aristolochiaceae-feeding swallowtail butterfly, Atrophaneura alcinous, to aristolochic acids. J. Chem. Ecol. 15:2549–2563.CrossRefGoogle Scholar
  31. Pasteels, J. M. 2007. Chemical defence, offence and alliance in ants-aphids-ladybirds relationships. Pop. Ecol. 49:5–14.CrossRefGoogle Scholar
  32. Radford, P., Attygalle, A., Meinwald, J., Smedley, S., and Eisner, T. 1997. Pyrrolidinooxazolidine alkaloids from two species of ladybird beetles. J. Nat. Prod. 60:755–759.PubMedCrossRefGoogle Scholar
  33. Rossini, C., González, A., and Eisner, T. 2001. Fate of an alkaloidal nuptial gift in the moth Utetheisa ornatrix: systemic allocation for defense of self by the receiving female. J. Ins. Physiol. 47:639–647.CrossRefGoogle Scholar
  34. Schlatter, C., Waldner, E. E., and Schmid, H. 1968. Zur Byosyntheses des Cantharidins. I. Experientia 24:994–995.PubMedCrossRefGoogle Scholar
  35. Schroeder, F., Farmer, J., Attygalle, A., Smedley, S., Eisner, T., and Meinwald, J. 1998a. Combinatorial chemistry in insects: A library of defensive macrocyclic polyamines. Science 281:428–431.CrossRefGoogle Scholar
  36. Schroeder, F., Farmer, J., Smedley, S., Eisner, T., and Meinwald, J. 1998b. Absolute configuration of the polyazamacrolides, macrocyclic polyamines produced by a ladybird beetle. Tetrahedron Lett. 39:6625–6628.CrossRefGoogle Scholar
  37. Sierra, J. R., Woggon, W., and Schmid, H. 1976. Transfer of cantharidin during copulation from the adult male to the female of Lytta vesicatoria (“Spanish flies”). Experientia 32:142–144.CrossRefGoogle Scholar
  38. Vahed, K. 1998. The function of nuptial feeding in insects: review of empirical studies. Biol. Rev. 73:43–78.CrossRefGoogle Scholar
  39. Vahed, K. 2007. All that glisters is not gold: Sensory bias, sexual conflict and nuptial feeding in insects and spiders. Ethology 113:105–127.CrossRefGoogle Scholar
  40. Witte, L., Ehmke, A., and Hartmann, T. 1990. Interspecific flow of pyrrolizidine alkaloids. Naturwissenschaten 77:540–543.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Soledad Camarano
    • 1
  • Andrés González
    • 1
  • Carmen Rossini
    • 1
  1. 1.Laboratorio de Ecología Química, Departamento de Química Orgánica, Facultad de QuímicaUniversidad de la RepúblicaMontevideoUruguay

Personalised recommendations