Skip to main content
Log in

Semiochemicals Mediating Defense, Intraspecific Competition, and Mate Finding in Leptopilina ryukyuensis and L. japonica (Hymenoptera: Figitidae), Parasitoids of Drosophila

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Deciphering the processes driving the evolution of the diverse pheromone-mediated chemical communication system of insects is a fascinating and challenging task. Understanding how pheromones have arisen has been supported by studies with the model organism Leptopilina heterotoma, a parasitoid wasp whose defensive compound (−)-iridomyrmecin also evolved as a component of the female sex pheromone and as a cue to avoid competition with other females during host search. To understand how compounds can evolve from being non-communicative to having a communicative function and to shed light on the evolution of the multi-functional use of iridomyrmecin in the genus Leptopilina, the chemical communication of two additional species, L. ryukyuensis and L. japonica, was studied. We demonstrate that in both species a species-specific mixture of iridoids is produced and emitted by wasps upon being attacked, consistent with their putative role as defensive compounds. In L. ryukyuensis these iridoids are also used by females to avoid host patches already exploited by other conspecific females. However, females of L. japonica do not avoid the odor of conspecific females during host search. We also show that the sex pheromone of female L. ryukyuensis consists of cuticular hydrocarbons (CHCs), as males showed strong courtship behavior (wing fanning) towards these compounds, but not towards the iridoid compounds. In contrast, males of L. japonica prefer their females’ iridoids but CHCs also elicit some courtship behavior. The use of iridoid compounds as defensive allomones seems to be common in the genus Leptopilina, while their communicative functions appear to have evolved in a species-specific manner.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300

    Google Scholar 

  • Blum MS (1996) Semiochemical parsimony in the Arthropoda. Annu Rev Entomol 41:353–374. https://doi.org/10.1146/annurev.en.41.010196.002033

    Article  CAS  PubMed  Google Scholar 

  • Boppré M (1986) Insects pharmacophagously utilizing defensive plant chemicals (pyrrolizidine alkaloids). Naturwissenschaften 73:17–26. https://doi.org/10.1007/BF01168801

    Article  Google Scholar 

  • Bradbury JW, Vehrencamp SL (2011) Principles of Animal Communication. Sinauer Associates, Sunderland

    Google Scholar 

  • Carlson DA, Roan CS, Yost RA, Hector J (1989) Dimethyl disulfide derivatives of long chain alkenes, alkadienes, and alkatrienes for gas chromatography/mass spectrometry. Anal Chem 61:1564–1571. https://doi.org/10.1021/ac00189a019

    Article  CAS  Google Scholar 

  • Carlson DA, Bernier UR, Sutton BD (1998) Elution patterns from capillary GC for methyl-branched alkanes. J Chem Ecol 24:1845–1865. https://doi.org/10.1023/A:1022311701355

    Article  CAS  Google Scholar 

  • Carton Y, Boulétreau M, van Alphen JJM, van Lenteren JC (1986) The Drosophila parasitic wasps. In: Ashburner M, Carson HL, Thompson JN (eds) The Genetics and Biology of Drosophila. Academic Press, Orlando, pp 347–394

  • Do Nascimento RR, Billen J, Sant'ana AEG, Morgan ED, Harada AY (1998) Pygidial gland of Azteca NR. bicolor and Azteca chartifex: morphology and chemical identification of volatile components. J Chem Ecol 24:1629–1637. https://doi.org/10.1023/A:1020864427854

  • El-Sayed AM (2018) The Pherobase: Database of Pheromones and Semiochemicals. www.pherobase.com. Accessed 16 Jan 2018

  • Fleury F, Gibert P, Ris N, Allemand R (2009) Ecology and life history evolution of frugivorous Drosophila parasitoids. In: Prevost G (ed) Parasitoids of Drosophila. Academic Press, London, pp 3–44

  • Geiselhardt S, Jakobschy D, Ockenfels P, Peschke K (2008) A sex pheromone in the desert tenebrionid beetle Parastizopus armaticeps. J Chem Ecol 34:1065–1071. https://doi.org/10.1007/s10886-008-9488-1

  • Gibbs AG, Rajpurohit S (2010) Cuticular lipids and water balance. In: Bagnères A-G, Blomquist GJ (eds) Insect Hydrocarbons. Biology, Biochemistry, and Chemical Ecology. Cambridge University Press, Cambridge, pp 100–120

  • Greenspan RJ, Ferveur J-F (2000) Courtship in Drosophila. Annu Rev Genet 34:205–232

  • Hübner G, Dettner K (2000) Hyperparasitoid defense strategies against spiders: the role of chemical and morphological protection. Entomol Exp Appl 97:67–74. https://doi.org/10.1046/j.1570-7458.2000.00717.x

    Article  Google Scholar 

  • Hübner G, Völkl W, Francke W, Dettner K (2002) Mandibular gland secretions in alloxystine wasps (Hymenoptera, Cynipoidea, Charipidae): do ecological or phylogenetical constraints influence occurrence or composition? Biochem Syst Ecol 30:505–523. https://doi.org/10.1016/S0305-1978(01)00137-5

    Article  Google Scholar 

  • Huth A, Dettner K (1990) Defense chemicals from abdominal glands of 13 rove beetle species of subtribe Staphylinina (Coleoptera: Staphylinidae, Staphylininae). J Chem Ecol 16:2691–2711. https://doi.org/10.1007/BF00988079

    Article  CAS  PubMed  Google Scholar 

  • Isidoro N, Bin F, Romani R, Pujade-Villar J, Ros-Farre P (1999) Diversity and function of male antennal glands in Cynipoidea (Hymenoptera). Zool Scr 28:165–174. https://doi.org/10.1046/j.1463-6409.1999.00013.x

    Article  Google Scholar 

  • Karlson P, Lüscher M (1959) Pheromone. Naturwissenschaften 46:63–64. https://doi.org/10.1007/BF00599084

    Article  CAS  Google Scholar 

  • Kühbandner S, Sperling S, Mori K, Ruther J (2012) Deciphering the signature of cuticular lipids with contact sex pheromone function in a parasitic wasp. J Exp Biol 215:2471–2478. https://doi.org/10.1242/jeb.071217

    Article  CAS  PubMed  Google Scholar 

  • Lockey LH (1988) Lipids of the insect cuticle: origin, composition and function. Comp Biochem Physiol B 89:595–645

    Article  Google Scholar 

  • Löfqvist J (1976) Formic acid and saturated hydrocarbons as alarm pheromones for the ant Formica rufa. J Insect Physiol 22:1331–1346. https://doi.org/10.1016/0022-1910(76)90155-4

  • Mori K, Shikichi Y, Shankar S, Yew JY (2010) Pheromone synthesis. Part 244: Synthesis of the racemate and enantiomers of (11Z, 19Z)-CH503 (3-acetoxy-11, 19-octacosadien-1-ol), a new sex pheromone of male Drosophila melanogaster to show its (S)-isomer and racemate as bioactive. Tetrahedron 66:7161–7168

  • Pfeiffer L, Ruther J, Hofferberth J, Stökl J (2018) Interference of chemical defence and sexual communication can shape the evolution of chemical signals. Sci Rep 8:970. https://doi.org/10.1038/s41598-017-18376-w

    Article  CAS  Google Scholar 

  • R Core Team (2017). R: A language and environment for statistical computing. https://www.R-project.org. Accessed 8 Mar 2018

  • Ruther J, Reinecke A, Tolasch T, Hilker M (2001) Make love not war: a common arthropod defence compound as sex pheromone in the forest cockchafer Melolontha hippocastani. Oecologia 128:44–47. https://doi.org/10.1007/s004420100634

  • Stacey N, Sorensen P (2009) Hormonal pheromones in fish. In: Pfaff DW (ed) Hormones, Brain and Behavior. Elsevier, Amsterdam, pp 639–682

  • Steiger S, Schmitt T, Schaefer HM (2011) The origin and dynamic evolution of chemical information transfer. Proc R Soc Lond B 278:970–979. https://doi.org/10.1098/rspb.2010.2285

    Article  Google Scholar 

  • Stökl J, Herzner G (2016) Morphology and ultrastructure of the allomone and sex-pheromone producing mandibular gland of the parasitoid wasp Leptopilina heterotoma (Hymenoptera: Figitidae). Arthropod Struct Dev 45:333–340. https://doi.org/10.1016/j.asd.2016.06.003

  • Stökl J, Steiger S (2017) Evolutionary origin of insect pheromones. Curr Opin Insect Sci 24:36–42. https://doi.org/10.1016/j.cois.2017.09.004

    Article  PubMed  Google Scholar 

  • Stökl J, Hofferberth J, Pritschet M, Brummer M, Ruther J (2012) Stereoselective chemical defense in the Drosophila parasitoid Leptopilina heterotoma is mediated by (−)-iridomyrmecin and (+)-isoiridomyrmecin. J Chem Ecol 38:331–339. https://doi.org/10.1007/s10886-012-0103-0

  • Stökl J, Machacek Z, Ruther J (2015) Behavioural flexibility of the chemical defence in the parasitoid wasp Leptopilina heterotoma. Sci Nat 102:67. https://doi.org/10.1007/s00114-015-1317-0

  • Symonds MRE, Elgar MA (2008) The evolution of pheromone diversity. Trends Ecol Evol 23:220–228. https://doi.org/10.1016/j.tree.2007.11.009

    Article  PubMed  Google Scholar 

  • Völkl W, Hübner G, Dettner K (1994) Interactions between Alloxysta brevis (Hymenoptera, Cynipoidea, Alloxystidae) and honeydew-collecting ants: how an aphid hyperparasitoid overcomes ant aggression by chemical defense. J Chem Ecol 20:2901–2915. https://doi.org/10.1007/BF02098397

  • Wachi N, Nomano FY, Mitsui H, Kasuya N, Kimura MT (2015) Taxonomy and evolution of putative thelytokous species of Leptopilina (Hymenoptera: Figitidae) from Japan, with description of two new species. Entomol Sci 18:41–54. https://doi.org/10.1111/ens.12089

  • Weiss I, Rössler T, Hofferberth J, Brummer M, Ruther J, Stökl J (2013) A nonspecific defensive compound evolves into a competition-avoidance cue and a female sex-pheromone. Nat Commun 4:2767. https://doi.org/10.1038/ncomms3767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss I, Hofferberth J, Ruther J, Stökl J (2015a) Varying importance of cuticular hydrocarbons and iridoids in the species-specific mate recognition pheromones of three closely related Leptopilina species. Front Ecol Evol 3:19. https://doi.org/10.3389/fevo.2015.00019

  • Weiss I, Ruther J, Stökl J (2015b) Species specificity of the putative male antennal aphrodisiac pheromone in Leptopilina heterotoma, Leptopilina boulardi, and Leptopilina victoriae. Biomed Res Int 2015:202965. https://doi.org/10.1155/2015/202965

  • Welzel KF, Lee SH, Dossey AT, Chauhan KR, Choe D-H (2018) Verification of Argentine ant defensive compounds and their behavioral effects on heterospecific competitors and conspecific nestmates. Sci Rep 8:1477. https://doi.org/10.1038/s41598-018-19435-6

  • Wheeler CA, Cardé RT (2013) Defensive allomones function as aggregation pheromones in diapausing ladybird beetles, Hippodamia convergens. J Chem Ecol 39:723–732. https://doi.org/10.1007/s10886-013-0293-0

  • Wyatt TD (2014) Pheromones and Animal Behavior. Cambridge University Press, Cambridge

Download references

Acknowledgements

We would like to express our special thanks to Prof. M. T. Kimura (Hokkaido University, Japan) who has provided us with wasps; and the German Research Foundation DFG for funding (STO 966/1-2 and STO 966/2-1).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Johannes Stökl.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Böttinger, L.C., Hofferberth, J., Ruther, J. et al. Semiochemicals Mediating Defense, Intraspecific Competition, and Mate Finding in Leptopilina ryukyuensis and L. japonica (Hymenoptera: Figitidae), Parasitoids of Drosophila. J Chem Ecol 45, 241–252 (2019). https://doi.org/10.1007/s10886-019-01052-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-019-01052-w

Keywords

Navigation