Advertisement

Journal of Chemical Ecology

, Volume 42, Issue 1, pp 17–23 | Cite as

Parapheromones for Thynnine Wasps

  • Björn Bohman
  • Amir Karton
  • Ruby C. M. Dixon
  • Russell A. Barrow
  • Rod Peakall
Article

Abstract

Sexually deceptive orchids produce floral volatiles that attract male insect pollinators. This interaction between flower and pollinator normally is highly specific. In the few cases where the chemical composition of the volatiles is known, the compounds have been found to be identical to those that comprise the sex pheromone of the female wasp. In this study, we investigated whether there is potential for flexibility in the molecular structure of the chemical cues used to mediate these specific interactions. Specifically, we asked whether strong sexual attraction can be maintained with structural modifications of sex pheromone components. Our study focused on the orchid, Drakaea glyptodon, which is pollinated by males of the thynnine wasp, Zaspilothynnus trilobatus. Three alkylpyrazines and a unique hydroxymethylpyrazine are components of the female produced sex pheromone of Z. trilobatus, and also the semiochemicals produced by the orchid that lures the males as pollinators. A blend of 2-butyl-3,5-dimethylpyrazine and 2-hydroxymethyl-3,5-diethyl-6-methylpyrazine (3:1) is as attractive as the full blend of four compounds. Therefore, in this study we substituted 2-hydroxymethyl-3,5-diethyl-6-methylpyrazine with one of five structurally related parapheromones in a blend with 2-butyl-3,5-dimethylpyrazine. All blends tested stimulated approaches by male wasps, with some also eliciting landing and attempted copulation. High-level calculations (G4(MP2)) showed the energy differences between the structural isomers were small, although the degree of sexual attraction varied, indicating the importance of structural factors for activity. One of the parapheromones, 2-hydroxymethyl-3,5-dimethyl-6-ethylpyrazine, elicited similar proportions of approaches, landings, and attempted copulations as the sex pheromone at the ratio and dose tested. The findings suggest that there is potential for chemical flexibility in the evolution of sexual deception.

Keywords

Drakaea Sexual deception Pyrazine Parapheromone Specificity 

Notes

Acknowledgments

We thank Ryan Phillips and Alyssa Weinstein for insightful comments on the manuscript. Funding was provided by the Australian Research Council (LP0989338 and LP130100162 to RP and RAB).

References

  1. Ando T, Kuroko H, Nakagaki S, Saito O, Oku T, Takahashi N (1981) Multi-component sex attractants in systematic field tests of male Lepidoptera. Agric Biol Chem 45:487–495CrossRefGoogle Scholar
  2. Ayasse M, Dötterl S (2014) The role of preadaptations or evolutionary novelties for the evolution of sexually deceptive orchids. New Phytol 203:710–712CrossRefPubMedGoogle Scholar
  3. Ayasse M, Paxton R, Tengö J (2001) Mating behavior and chemical communication in the order Hymenoptera. Annu Rev Entomol 46:31–78CrossRefPubMedGoogle Scholar
  4. Ayasse M, Schiestl FP, Paulus HF, Ibarra F, Francke W (2003) Pollinator attraction in a sexually deceptive orchid by means of unconventional chemicals. Proc R Soc B 270:517–522PubMedCentralCrossRefPubMedGoogle Scholar
  5. Ayasse M, Stökl J, Francke W (2011) Chemical ecology and pollinator-driven speciation in sexually deceptive orchids. Phytochemistry 72:1667–1677CrossRefPubMedGoogle Scholar
  6. Beani L, Dessì-Fulgheri F, Cappa F, Toth A (2014) The trap of sex in social insects: from the female to the male perspective. Neurosci Biobehav Rev 46:519–533CrossRefPubMedGoogle Scholar
  7. Bierl BA, Beroza M, Collier C (1970) Potent sex attractant of the gypsy moth: its isolation, identification, and synthesis. Science 170:87–89CrossRefPubMedGoogle Scholar
  8. Bohman B, Peakall R (2014) Pyrazines attract Catocheilus thynnine wasps. Insects 5:474–487PubMedCentralCrossRefPubMedGoogle Scholar
  9. Bohman B, Jeffares L, Flematti G, Byrne LT, Skelton BW, Phillips RD, Dixon KW, Peakall R, Barrow RA (2012a) Discovery of tetrasubstituted pyrazines as semiochemicals in a sexually deceptive orchid. J Nat Prod 75:1589–1594CrossRefPubMedGoogle Scholar
  10. Bohman B, Jeffares L, Flematti G, Phillips RD, Dixon KW, Peakall R, Barrow RA (2012b) The discovery of 2-hydroxymethyl-3-(3-methylbutyl)-5-methylpyrazine: a semiochemical in orchid pollination. Org Lett 14:2576–2578CrossRefPubMedGoogle Scholar
  11. Bohman B, Berntsson B, Dixon RCM, Stewart CD, Barrow RA (2014a) Alkylations and hydroxymethylations of pyrazines via green Minisci-type reactions. Org Lett 16:2787–2789CrossRefPubMedGoogle Scholar
  12. Bohman B, Phillips RD, Menz MHM, Berntsson BW, Flematti GR, Barrow RA, Dixon KW, Peakall R (2014b) Discovery of pyrazines as pollinator sex pheromones and orchid semiochemicals: implications for the evolution of sexual deception. New Phytol 203:939–953CrossRefPubMedGoogle Scholar
  13. Borg-Karlson A-K (1985) Chemical basis for the relationship between Ophrys orchids and their pollinators. Chem Scr 25:283–294Google Scholar
  14. Borg-Karlson A-K (1987) Chemical basis for the relationship between Ophrys orchids and their pollinators. Chem Scr 27:313–325Google Scholar
  15. Borg-Karlson A-K (1990) Chemical and ethological studies of pollination in the genus Ophrys (Orchidaceae). Phytochemistry 29:1359–1387CrossRefGoogle Scholar
  16. Cardé RT. 1990. Principles of mating disruption. Behavior-modifying chemicals for pest management: Applications of pheromones and other attractants. Marcel Dekker, New York:47–71Google Scholar
  17. Coleman E (1929) Pollination of an Australian orchid by the male ichneumonid Lissopimpla semipunctata, Kirby. Trans R Entomol Soc Lond 76:533–539CrossRefGoogle Scholar
  18. Curtiss LA, Redfern PC, Raghavachari K (2007) Gaussian-4 theory using reduced order perturbation theory. The J Chem Phys 127:124105CrossRefPubMedGoogle Scholar
  19. Francke W, Schulz S (2010) 4.04 - Pheromones of terrestrial invertebrates. In: Liu H-W, Mander L (eds) Comprehensive natural products II. Elsevier, Oxford, pp. 153–223CrossRefGoogle Scholar
  20. Franke S, Ibarra F, Schulz CM, Twele R, Poldy J, Barrow RA, Peakall R, Schiestl FP, Francke W (2009) The discovery of 2,5-dialkylcyclohexan-1,3-diones as a new class of natural products. Proc Natl Acad Sci U S A 106:8877–8882PubMedCentralCrossRefPubMedGoogle Scholar
  21. Frisch M, Trucks G, Schlegel H, Scuseria G, Robb M, Cheeseman J, Scalmani G, Barone V, Mennucci B, Petersson G (2009) Gaussian 09, revision D. 01. Gaussian, Wallingford, CT, USAGoogle Scholar
  22. Gaskett AC (2011) Orchid pollination by sexual deception: pollinator perspectives. Biol Rev 86:33–75CrossRefPubMedGoogle Scholar
  23. Griffiths KE, Trueman JWH, Brown GR, Peakall R (2011) Molecular genetic analysis and ecological evidence reveals multiple cryptic species among thynnine wasp pollinators of sexually deceptive orchids. Mol Phylogenet Evol 59:195–205CrossRefPubMedGoogle Scholar
  24. Kullenberg B (1950) Investigations on the pollination of Ophrys species. Oikos 2:1–19CrossRefGoogle Scholar
  25. Menz MHM, Phillips RD, Anthony JM, Bohman B, Dixon KW, Peakall R (2015) Ecological and genetic evidence for cryptic ecotypes in a rare sexually deceptive orchid, Drakaea elastica. Bot J Linn Soc 177:124–140CrossRefGoogle Scholar
  26. Niehuis O, Buellesbach J, Gibson JD, Pothmann D, Hanner C, Mutti NS, Judson AK, Gadau J, Ruther J, Schmitt T (2013) Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones. Nature 494:345–348CrossRefPubMedGoogle Scholar
  27. Ono M, Sasaki M (1987) Sex pheromones and their cross-activities in six Japanese sympatri species of the genus Vespa. Insect Soc 34:252–260CrossRefGoogle Scholar
  28. Paulus H, Gack C (1990) Pollinators as prepollinating isolation factors: evolution and speciation in Ophrys (Orchidaceae). Israel J Bot 39:43–79Google Scholar
  29. Peakall R (1990) Responses of male Zaspilothynnus trilobatus wasps to females and the sexually deceptive orchid it pollinates. Funct Ecol 4:159–167CrossRefGoogle Scholar
  30. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  31. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539PubMedCentralCrossRefPubMedGoogle Scholar
  32. Peakall R, Ebert D, Poldy J, Barrow RA, Francke W, Bower CC, Schiestl FP (2010) Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: implications for pollinator-driven speciation. New Phytol 188:437–450CrossRefPubMedGoogle Scholar
  33. Phillips RD, Faast R, Bower CC, Brown GR, Peakall R (2009) Implications of pollination by food and sexual deception for pollinator specificity, fruit set, population genetics and conservation of Caladenia (Orchidaceae). Aust J Bot 57:287–306CrossRefGoogle Scholar
  34. Phillips RD, Scaccabarozzi D, Retter BA, Hayes C, Brown GR, Dixon KW, Peakall R (2014) Caught in the act: pollination of sexually deceptive trap-flowers by fungus gnats in Pterostylis (Orchidaceae). Ann Bot 113:629–641PubMedCentralCrossRefPubMedGoogle Scholar
  35. Renou M, Guerrero A (2000) Insect parapheromones in olfaction research and semiochemical-based pest control strategies. Annu Rev Entomol 45:605–630CrossRefPubMedGoogle Scholar
  36. Roelofs WL, Comeau A (1968) Sex pheromone perception. Nature 220:600–601CrossRefPubMedGoogle Scholar
  37. Roelofs WL, Comeau A (1969) Sex pheromone specificity: taxonomic and evolutionary aspects in Lepidoptera. Science 165:398–400CrossRefPubMedGoogle Scholar
  38. Schiestl FP, Cozzolino S (2008) Evolution of sexual mimicry in the orchid subtribe Orchidinae: the role of preadaptations in the attraction of male bees as pollinators. BMC Evol Biol 8:27PubMedCentralCrossRefPubMedGoogle Scholar
  39. Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399:421–422CrossRefGoogle Scholar
  40. Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (2000) Sex pheromone mimicry in the early spider orchid (Ophrys sphegodes): patterns of hydrocarbons as the key mechanism for pollination by sexual deception. J Comp Phys A 186:567–574CrossRefGoogle Scholar
  41. Schiestl FP, Peakall R, Mant JG, Ibarra F, Schulz C, Franke S, Francke W (2003) The chemistry of sexual deception in an orchid-wasp pollination system. Science 302:437–438CrossRefPubMedGoogle Scholar
  42. Schlüter PM, Schiestl FP (2008) Molecular mechanisms of floral mimicry in orchids. Trends Plant Sci 13:228–235CrossRefPubMedGoogle Scholar
  43. Schneider D, Lange R, Schwarz F, Beroza M, Bierl BA (1974) Attraction of male gypsy and nun moths to Disparlure and some of its chemical analogues. Oecologia 14:19–36CrossRefGoogle Scholar
  44. Stökl J, Dandekar A-T, Ruther J (2014) High chemical diversity in a wasp pheromone: a blend of methyl 6-methylsalicylate, fatty alcohol acetates and cuticular hydrocarbons releases courtship behavior in the Drosophila parasitoid Asobara tabida. J Chem Ecol 40:159–168CrossRefPubMedGoogle Scholar
  45. Symonds MR, Elgar MA (2008) The evolution of pheromone diversity. Trends Ecol Evol 23:220–228CrossRefPubMedGoogle Scholar
  46. Vereecken NJ, Schiestl FP (2008) The evolution of imperfect floral mimicry. Proc Natl Acad Sci U S A 105:7484–7488PubMedCentralCrossRefPubMedGoogle Scholar
  47. Whitehead MR, Peakall R (2014) Pollinator specificity drives strong prepollination reproductive isolation in sympatric sexually deceptive orchids. Evolution 68:1561–1575CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Björn Bohman
    • 1
    • 2
    • 3
  • Amir Karton
    • 3
  • Ruby C. M. Dixon
    • 1
  • Russell A. Barrow
    • 1
  • Rod Peakall
    • 2
    • 3
  1. 1.Research School of ChemistryThe Australian National UniversityCanberraAustralia
  2. 2.Research School of BiologyThe Australian National UniversityCanberraAustralia
  3. 3.School of Chemistry and BiochemistryThe University of Western AustraliaCrawleyAustralia

Personalised recommendations