Abstract
Pyrrolizidine alkaloids (PAs), acquired by adults or larvae of Danainae and Ithomiinae butterflies and Arctiidae moths from plants, protect these lepidopterans against predators and are biosynthetic precursors of male sex pheromones. The investigation of PAs in many species of wild-caught adults of Ithomiinae showed lycopsamine (1) [(7R)-OH, (2′S)-OH, (3′S)-OH] as the main alkaloid. In incorporation experiments, PA-free (freshly emerged) adults of the ithomiineMechanitis polymnia were fed seven PAs: lycopsamine and four of its known natural stereoisomers—indicine (2) [(7R)-OH, (2′R)-OH, (3′S)-OH], intermedine (3) [(7R)-OH, (2′S)-OH, (3′R)-OH], rinderine (4) [(7S)-OH, (2′S)-OH, (3′R)-OH], and echinatine (5) [(7S)-OH, (2′S)-OH, (3′S)-OH], and two PAs without the 7-OH: supinine (6) [(2′S)-OH, (3′R)-OH] and amabiline (7) [(2′S)-OH, (3′S)-OH]. Males epimerized PAs 3, 4, and 5 mainly to lycopsamine (1). Females fed these same three PAs changed a smaller proportion to lycopsamine; their lesser capacity to modify PAs corresponds to their normal acquisition of already transformed PAs from males during mating rather than through visits of adults to plant sources of PAs. The alkaloids1 and2, both 7R and 3′S, were incorporated without or with minimum change by males and females. Feeding experiments with6 and7 (males only) showed an inversion at the 3′ center of6 and no change in7. The inversion from 7S to 7R (probably via oxyreduction) may be closely related to the evolution of acquisition of PAs by butterflies and moths. Two hypotheses are discussed: (1) The ancestral butterflies are probably adapted to tolerate, assimilate, and use (7R)-PAs (most common in plants; all widespread 1,2-unsaturated macrocyclic PA diesters show this configuration). The development of (7R)-PA receptors in the butterflies could lead to a specialization on this configuration in two ways: to help find PA plants and to utilize these components in sexual chemical communication. A later appearance of (7S)-PAs in plants could have selected an enzymatic system for the inversion of this chiral center in order to continue producing (7R)-PA-derived pheromones. (2) The inversion would be due to the evolution of a enzyme system specialized in the transport of (7R)-PAs to the integument; the failure of this system to carry (7S)-PAs led to an enzymatic system to invert them to transportable (7R)-PAs. In this case, the 7R configuration is an effect and not a cause of (7R)-PA-derived pheromones. In both hypotheses, the partial inversion of the 3′-asymmetric center, when the butterfly was fed intermedine (3), rinderine (4), and supinine (6), could be fortuitous due to the conformation of the molecule and/or the enzymatic system.
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References
Bell, T.W., andMeinwald, J. 1986. Pheromones of two arctiid moths (Creatonotos transiens andC. gangis): Chiral components from both sexes and achiral female components.J. Chem. Ecol. 12:385–409.
Bell, T.W., Boppré, M., Schneider, D., andMeinwald, J. 1984. Stereochemical course of pheromone biosynthesis in the arctiid moth,Creatonotos transiens.Experientia 40:713–714.
Biller, A., Boppré, M., Witte, L., andHartmann, T. 1994. Pyrrolizidine alkaloids inChromolaena odorata: Chemical and chemoecology aspects.Phytochemistry 35:615–619.
Bogner, F., andBoppré, M. 1989. Single cell recordings reveal hydroxydanaidal as the volatile compound attracting insects to pyrrolizidine alkaloids.Entomol. Exp. Appl. 50:171–184.
Boppré, M. 1978. Chemical communication, plant relationships and mimicry in the evolution of danaid butterflies.Entomol. Exp. Appl. 24:264–277.
Boppré, M. 1986. Insects pharmacophagously utilizing defensive plant chemicals (pyrrolizidine alkaloids).Naturwissenschaften 73:17–26.
Boppré, M. 1990. Lepidoptera and pyrrolizidine alkaloids. Exemplification of complexity in chemical ecology.J. Chem. Ecol. 16:165–185.
Bremer, K., Jansen, R.K., Karis, P.O., KÄllersjö, M., Keeley, S.C., Kim, K.J., Michaels, H.J., Palmer, J.D., andWallace, R.S. 1992. A review of the phylogeny and classification of the Asteraceae.Nord. J. Bot. 12:141–148.
Brown, K.S. 1984. Adult-obtained pyrrolizidine alkaloids defend ithomiine butterflies against a spider predator.Nature 307:707–709.
Brown, K.S. 1985. Chemical ecology of dehydropyrrolizidine alkaloids in adult Ithomiinae (Lepidoptera: Nymphalidae).Rev. Bras. Biol. 44:435–460.
Brown, K.S. 1987. Chemistry at the Solanaceae/lthomiinae interface.Ann. M. Bot. Gard. 74:359–397.
Coimbra-Filho, A.F. 1981. Animais predados ou rejeitados pelo Saui-Piranga,Leontopithecus r. rosalia (L., 1766) na sua area de ocorrÊncia primitiva (Callitrichidae: Primates).Rev. Bras. Biol. 41:717–731.
Conner, W.E., Eisner, T., Vander Meer, R.K., Guerrero, A., andMeinwald, J. 1981. Precopulatory sexual interaction in an arctiid moth (Utetheisa ornatrix): role of a pheromone derived from dietary alkaloids.Behav. Ecol. Sociobiol. 9:227–235.
Culvenor, C.C.J. 1978. Pyrrolizidine alkaloids—occurrence and systematic importance in angiosperms.Bot. Notiser 131:473–486.
Dussourd, D.E., Ubik, K., Harvis, C., Resch, J., Meinwald, J., andEisner, T. 1988. Biparental defensive endowment of eggs with acquired plant alkaloid in the mothUtetheisa ornatrix.Proc. Natl. Acad. Sci. U.S.A. 85:5992–5996.
Edgar, J.A. 1975. Danainae (Lep.) and 1,2-dehydropyrrolizidine alkaloid-containing plants-with reference to observations made in the New Hebrides.Phil. Trans. R. Soc. Lond. B. 272:467–476.
Edgar, J.A. 1982. Pyrrolizidine alkaloids sequestered by Solomon Island danainae butterflies. The feeding preferences of the Danainae and Ithomiinae.J. Zool. Lond. 196:385–399.
Edgar, J.A. 1984. Parsonsieae: ancestral larval foodplants of the Danainae and Ithomiinae, pp. 91–96,in P.A. Ackery, and R.I. Vane-Wright (eds.). The Biology of Butterflies. Academic Press, London.
Edgar, J.A., Culvenor, C.C.J., andSmith, L.W. 1971. Dihydropyrrolizine derivatives in the “hair-pencil” secretions of danaid butterflies.Experientia 27:761–762.
Edgar, J.A., Culvenor, C.C.J., andRobinson, G.S. 1973. Hairpencil dihydropyrrolizidines of Danainae the New Hebrides.J. Aust. Entomol. Soc., 12:144–150.
Edgar, J.A., Culvenor, C.C.J., andPliske, T.E. 1974. Coevolution of danaid butterflies with their host plants.Nature 250:646–648.
Edgar, J.A., Culvenor, C.C.J., andPliske, T.E. 1976. Isolation of a lactone structurally related to the esterifying acids of pyrrolizidine alkaloids from the costal fringes of male Ithomiinae.J. Chem. Ecol. 2:263–270.
Edgar, J.A., Boppré, M., andSchneider, D. 1979. Pyrrolizidine alkaloid storage in African and Australian Danaid butterflies.Experientia 35:1447–1448.
Eisner, T. 1982. For love of nature: exploration and discovery at biological field stations.Bioscience 32:321–326.
Eisner, T., andEisner, M. 1991. Unpalatability of the pyrrolizidine alkaloid-containing mothUtetheisa ornatrix, and its larva, to wolf spiders.Psyche 98:111–118.
Kelley, R.B., Seiber, J.N., Jones, A.D., Segall, H.J., andBrower, L.P. 1987. Pyrrolizidine alkaloids in overwintering monarch butterflies (Danaus plexippus) from Mexico.Experientia 43:943–946.
Krasnoff, S.B., andDussourd, D.E. 1989. Dihydropyrrolizine attractants for arctiid moths that visit plants containing pyrrolizidine alkaloids.J. Chem. Ecol. 15:47–60.
L'Empereur, K.M., Li, Y., andStermitz, F.R. 1989. Pyrrolizidine alkaloids fromHackelia californica andGnophaela latipennis, anH. californica-hosted arctiid moth.J. Nat. Prod. 52:360–366.
Mackay, M.F., andCulvenor, C.C.J. 1982. Structure of Senecionine, pyrrolizidine alkaloid.Acta Cryst. B38:2574–2578.
Mackay, M.F., Sadek, M., andCulvenor, C.C.J. 1983. Lycopsamine and intermedine, C15H25NO5: Diastereoisomeric pyrrolizidine alkaloids.Acta Cryst. C39:785–788.
Masters, A.R. 1990. Pyrrolizidine alkaloids in artificial nectar protect adult ithomiine butterflies from spider predator.Biotropica 22:298–304.
Masters, A.R. 1992. Chemical defense in Ithomiinae butterflies (Nymphalidae: Ithomiinae). PhD thesis. University of Florida, Gainesville, Florida.
Mattocks, A.R. 1986. Chemistry and Toxicology of Pyrrolizidine Alkaloids. Academic Press, New York.
Nishida, R., Kim, C., Fukami, H., andIrie, R. 1991. Ideamine N-oxides: Pyrrolizidine alkaloids sequestered by the Danaine butterfly.Idea leuconoe. Agric. Biol. Chem. 55:1787–1792.
Pasteels, J.M., Duffey, S., andRowell-Rahier, M. 1990. Toxins in chrysomelid beetles. Possible evolutionary sequence from de novo synthesis to derivation from food-plant chemicals.J. Chem. Ecol. 16:211–222.
Pliske, T.E. 1975a. Pollination of pyrrolizidine alkaloid containing plants by male Lepidoptera.Environ. Entomol. 4:474–479.
Pliske, T.E. 1975b. Attraction of Lepidoptera to plants containing pyrrolizidine alkaloids.Environ. Entomol. 4:455–473.
Rizk, A.F.M. 1991. The pyrrolizidine alkaloids: Plant sources and properties, pp. 1–90, in A.F.M. Rizk (ed.). Naturally Occurring Pyrrolizidine Alkaloids. CRC Press, Boca Raton, Florida.
Rothschild, M., andEdgar, J.A. 1978. Pyrrolizidine alkaloids fromSenecio vulgaris sequestered and stored byDanaus plexippus.J. Zool. London 186:347–349.
Rowell-Rahier, M., Witte, L., Ehmke, A., Hartmann, T., andPasteels, J.M. 1991. Sequestration of plant pyrrolizidine alkaloids by chrysomelid beetles and selective transfer into the defensive secretions.Chemoecology 2:41–48.
Schneider, D., Boppré, M., Schneider, H., Thompson, W.R., Boriack, C.J., Petty, R.L., andMeinwald, J. 1975. A pheromone precursor and its uptake in maleDanaus butterflies.J. Comp. Physiol. 97:245–256.
Schulz, S. 1987. Die Chemie Duftorgane mÄnnlicher Lepidopteren. Doctoral thesis. Institut für Organische Chemie, UniversitÄt Hamburg, Hamburg, Germany.
Schulz, S. 1992. Absolute configuration and synthesis of 2-hydroxy-2-(1-hydroxyethyl)-3-methyl-γ-butyrolactone, a presumed pheromone of ithomiine butterflies.Liebigs Ann. Chem. 1992:829–834.
Schulz, S., Francke, W., Edgar, J., andSchneider, D. 1988. Volatile compounds from androconial organs of danaine and ithomiine butterflies.Z. Naturforsch 43c:99–104.
Schulz, S., Francke, W., Boppré, M., Eisner, T., andMeinwald, J. 1993. Insect pheromone biosynthesis: stereochemical pathway of hydroxydanaidal production from alkaloidal precursors inCreatonotos transiens (Lepidoptera, Arctiidae).Proc. Natl. Acad. Sci. U.S.A. 90:6834–6838.
Stelljes, M.E., andSeiber, J.N. 1990. Pyrrolizidine alkaloids in an overwintering population of monarch butterflies (Danaus plexippus) in California.J. Chem. Ecol. 16:1459–1470.
Trigo, J.R. 1993. Alcalóides pirrolizidínicos em borboletas Ithomiinae. Alguns aspectos em ecologia química. Doctoral thesis. Instituto de Química, UNICAMP, Campinas, SP, Brazil.
Trigo, J.R., andBrown, K.S. 1990. Variation of pyrrolizidine alkaloids in Ithomiinae: a comparative study between species feeding on Apocynaceae and Solanaceae.Chemocecology 1:22–29.
Trigo, J.R., andMotta, P.C. 1990. Evolutionary implications of pyrrolizidine alkaloid assimilation by danaine and ithomiine larvae (Lepidoptera: Nymphalidae).Experientia 46:332–334.
Trigo, J.R., Witte, L., Brown, K.S., Hartmann, T., andBarata, L.E.S. 1993. Pyrrolizidine alkaloids in the arctiid mothHyalurga syma.J. Chem. Ecol. 19:669–679.
Wink, M., Schneider, D., andWitte, L. 1988. Biosynthesis of pyrrolizidine alkaloid-derived pheromones in the arctiid moth,Creatonotos transiens: Stereochemical conversion of heliotrine.Z. Naturforsch 43c:737–741.
Witte, L., Rubiolo, P., Bicchi, C., andHartmann, T. 1993. Comparative analysis of pyrrolizidine alkaloids from natural sources by gas chromatography-mass spectrometry.Phytochemisiry 32:187–196.
Wodak, S.J. 1975. The crystal structure of heliotrine: A pyrrolizidine alkaloid monoester.Acta Cryst. B 31:569–573.
Wunderer, H., Hansen, K., Bell, T.W., Schneider, D., andMeinwald, J. 1986. Sex pheromones of two Asian moths (Creatonotos transiens, C. gangis; Lepidoptera—Arctiidae): Behavior, morphology, chemistry and electrophysiology.Exp. Biol. 46:11–27.
Zikan-Cardoso, M. 1991. Defesa química por alcalóides pirrolizidínicos (PAs) em Lepidoptera: testes corn um predador vertebrado. Master's thesis. Instituto de Biologia, UNICAMP, Campinas, SP, Brazil.
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This paper is part of the doctoral thesis of J.R.T.
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Trigo, J.R., Barata, L.E.S. & Brown, K.S. Stereochemical inversion of pyrrolizidine alkaloids byMechanitis polymnia (Lepidoptera: Nymphalidae: Ithomiinae): Specificity and evolutionary significance. J Chem Ecol 20, 2883–2899 (1994). https://doi.org/10.1007/BF02098396
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DOI: https://doi.org/10.1007/BF02098396