Varying importance of cuticular hydrocarbons and iridoids in the species-specific mate recognition pheromones of three closely related Leptopilina species

Frontiers in Ecology and Evolution

Volumn 3, Issue MAR, 2015, Pages

  Weiss, Ingmar ^a   Hofferberth, John ^b   Ruther, Joachim ^a   Stökl, Johannes ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b KENYON COLLEGE   (United States)

Author keywords

Chemical diversity; Drosophila; Iridomyrmecin; Parasitoid wasp; Saltational evolution

Indexed keywords

EID: 84994760506     PISSN: None     EISSN: 2296701X     Source Type: Journal    
DOI: 10.3389/fevo.2015.00019     Document Type: Article

References (60)

1. R Core Team (2014). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing
2. Allemand, R., Lemaître, C., Frey, F., Boulétreau, M., Vavre, F., Nordlander, G., et al. (2002). Phylogeny of six African Leptopilina species (Hymenoptera: Cynipoidea, Figitidae), parasitoids of Drosophila, with description of three new species. Ann. Soc. Entomol. Fr. 38, 319-332. doi: 10.1080/00379271.2002.10697346
3. Ando, T., Inomata, S.-I., and Yamamoto, M. (2004). "Lepidopteran sex pheromones". in The Chemistry of Pheromones and Other Semiochemicals I Vol. 239 of Topics in Current Chemistry, ed S. Schulz (Berlin; Heidelberg: Springer), 51-96
4. Benelli, G., Bonsignorie, G., Stefanini, C., Dario, P., and Canale, A. (2013). Male wing fanning performance during successful and unsuccessful mating in the parasitic wasp Lariophagus distinguendus Förster (Hymenoptera: Pteromalidae). J. Insect Behav. 26, 228-237. doi: 10.1007/s10905-012-9356-2
5. Benelli, G., Kavallieratos, N. G., Donati, E., Giunti, G., Stefanini, C., and Canale, A. (2015). Singing on the wings! Male wing fanning performances affect female willingness to copulate in the aphid parasitoid Lysiphlebus testaceipes (Hymenoptera: Braconidae: Aphidiinae). Insect Sci. doi: 10.1111/1744-7917.12201. [Epub ahead of print]
6. Bin, F., Wäckers, F., Romani, R., and Isidoro, N. (1999). Tyloids in Pimpla turionellae (L.) are release structures of male antennal glands involved in courtship behaviour (Hymenoptera: Ichneumonidae). Int. J. Insect Morphol. Embryol. 28, 61-68. doi: 10.1016/S0020-7322(99)00015-X
7. Bordenstein, S. R., and Werren, J. H. (2007). Bidirectional incompatibility among divergent Wolbachia and incompatibility level differences among closely related Wolbachia in Nasonia. Heredity 99, 278-287. doi: 10.1038/sj.hdy.6800994
8. Breeuwer, J. A. J., and Werren, J. H. (1990). Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346, 558-560. doi: 10.1038/346558a0
9. Buellesbach, J., Gadau, J., Beukeboom, L. W., Echinger, F., Raychoudhury, R., Werren, J. H., et al. (2013). Cuticular hydrocarbon divergence in the jewel wasp Nasonia: evolutionary shifts in chemical communication channels? J. Evol. Biol. 26, 2467-2478. doi: 10.1111/jeb.12242
10. Buellesbach, J., Greim, C., Raychoudhury, R., and Schmitt, T. (2014). Asymmetric assortative mating behaviour reflects incomplete pre-zygotic isolation in the Nasonia species complex. Ethology 120, 834-843. doi: 10.1111/eth.12250
11. Calabria, G., Máca, J., Bächli, G., Serra, L., and Pascual, M. (2012). First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J. Appl. Entomol. 136, 139-147. doi: 10.1111/j.1439-0418.2010.01583.x
12. Carlson, D. A., Bernier, U. R., and Sutton, B. D. (1998). Elution patterns from capillary GC for methyl-branched-alkanes. J. Chem. Ecol. 24, 1845-1865. doi: 10.1023/A:1022311701355
13. Carlson, D. A. (1989). Dimethyl disulfide derivatives of long chain alkenes, alkadienes, and alkatrienes for gas chromatography/mass spectrometry. Anal. Chem. 61, 1564-1571. doi: 10.1021/ac00189a019
14. Chabert, S., Allemand, R., Poyet, M., Eslin, P., and Gilbert, P. (2012). Ability of European parasitoids (Hymenoptera) to control a new invasive Asiatic pest, Drosophila suzukii. Biol. Control 31, 40-47. doi: 10.1016/j.biocontrol.2012.05.005
15. Cini, A., Ioratti, C., and Anfora, G. (2012). A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bull. Insectol. 65, 149-160. Available online at: http://hdl.handle.net/10449/21029
16. Cook, J. M. (1993). Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71, 421-435. doi: 10.1038/hdy.1993.157
17. Cuthbertson, A. G. S., Blackburn, L. F., and Audsley, N. (2014). Efficacy of commercially available invertebrate predators against Drosophila suzukii. Insects 5, 952-960. doi: 10.3390/insects5040952
18. Debout, G., Fauvergue, X., and Fleury, F. (2002). The effect of foundress number on sex ratio under partial local mate competition. Ecol. Entomol. 27, 242-246. doi: 10.1046/j.1365-2311.2002.00402.x
19. Do Nascimento, R. R., Billen, J., Sant'ana, A. E. G., Morgan, E. D., and Harada, A. Y. (1998). Pygidial gland of Azteca nr. bicolor and Azteca chartifex: morphology and chemical identification of volatile components. J. Chem. Ecol. 24, 1629-1637. doi: 10.1023/A:1020864427854
20. El-Sayed, A. M. (2014). The Pherobase: Database of Pheromones and Semiochemicals. Available online at: http://www.pherobase.com
21. Fischman, C. J., Adler, S., and Hofferberth, J. E. (2013). Divergent diastereoselective synthesis of iridomyrmecin, isoiridomyrmecin, teucrimulactone, and dolicholactone from citronellol. J. Organ. Chem. 78, 7318-7323. doi: 10.1021/jo400884g
22. Fleury, F., Vavre, F., Ris, N., Fouillet, P., and Boulétrau, M. (2000). Physiological cost induced by the maternally-transmitted endosymbiont Wolbachia in the Drosophila parasitoid Leptopilina heterotoma. Parasitology 121, 493-500. doi: 10.1017/S0031182099006599
23. Forshage, M., Nordlander, G., and Buffington, M. L. (2013). Eucoilinae of North America: a revised catalog of genera and described species. Proc. Entomol. Soc. Wash. 115, 225-255. doi: 10.4289/0013-8797.115.3.225
24. Grillenberger, B. K., van de Zande, L., Bijlsma, R., Gadau, J., and Beukeboom, L. W. (2009). Reproductive strategies under multiparasitism in natural populations of the parasitoid wasp Nasonia (Hymenoptera). J. Evol. Biol. 22, 460-470. doi: 10.1111/j.1420-9101.2008.01677.x
25. Gueguen, G., Onemola, B., and Govind, S. (2012). Association of a new Wolbachia strain with, and its effects on, Leptopilina victoriae, a virulent waps parasitic to Drosophila spp. Appl. Environ. Microbiol. 78, 5962-5966. doi: 10.1128/AEM.01058-12
26. Hamilton, W. D. (1967). Extraordinary sex ratios. Science 156, 477-488. doi: 10.1126/science.156.3774.477
27. Hardie, J., and Minks, A. K. (eds.). (1999). Pheromones of Non-Lepidopteran Insects Associated with Agricultural Plants. Wallingford, UK: CABI Publishing
28. Hauser, M. (2011). A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Manag. Sci. 67, 1352-1357. doi: 10.1002/ps.2265
29. Heimpel, G. E., and de Boer, J. G. (2008). Sex determination in the Hymenoptera. Annu. Rev. Entomol. 53, 209-230. doi: 10.1146/annurev.ento.53.103106.093441
30. Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A., and Werren, J. H. (2008). How many species are infected with Wolbachia?-a statistical analysis of current data. FEMS Microbiol. Lett. 281, 215-220. doi: 10.1111/j.1574-6968.2008.01110.x
31. Howard, R. W. (1993). "Cuticular hydrocarbons and chemical communication". in Insect Lipids, eds D. W. Stanley and D. R. Nelson (Lincoln, NE: University of Nebraska Press), 179-226
32. Huth, A., and 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. doi: 10.1007/BF00988079
33. Isidoro, N., and Bin, F. (1995). Male antennal gland of Amitus spiniferus (Brethes) (Hymenoptera: Platygastridae), likely involved in courtship behavior. Int. J. Insect Morphol. 24, 365-373. doi: 10.1016/0020-7322(95)00014-U
34. Isidoro, N., Bin, F., Romani, R., Pujade-Villar, J., and Palmira, R.-F. (1999). Diversity and function of male antennal glands in Cynipoidea (Hymenoptera). Zool. Scr. 28, 165-174. doi: 10.1046/j.1463-6409.1999.00013.x
35. Kühbandner, S., Sperling, S., Mori, K., and Ruther, J. (2012). Deciphering the signature of cuticular lipids with contact sex pheromone function in a parasitic wasp. J. Exp. Biol. 215, 2471-2478. doi: 10.1242/jeb.071217
36. Kasuya, N., Mitsui, H., Shinsuke, I., Watada, M., and Kimura, M. T. (2013). Ecological, morphological and molecular studies on Ganaspis individuals (Hymenoptera: Figitidae) attacking Drosophila suzukii (Diptera: Drosophilidae). Appl. Entomol. Zool. 48, 87-92. doi: 10.1007/s13355-012-0156-0
37. Löfstedt, C., Herrebout, W. M., and Menken, S. B. J. (1991). Sex pheromones and their potential role in the evolution of reproductive isolation in smale ermine moths (Yponomeutidae). Chemoecology 2, 20-28. doi: 10.1007/BF01240662
38. Nelson, D. R. (1993). "Methyl-branched lipids in insects". in Insect Lipids, eds D. W. Stanley and D. R. Nelson (Lincoln, NE: University of Nebraska Press), 271-316
39. Nordlander, G., and Grijpma, P. (1991). Systematics and biology of Rhoptromeris strobigena sp. n., a parasitoid of chloropids inhabiting conifer cones (Hymenoptera: Cynipoidea: Eucoilidae). Entomol. Scand. 22, 209-218. doi: 10.1163/187631291X00084
40. Nordlander, G. (1980). Revision of the genus Leptopilina Förster, 1869, with notes on the status of some other genera (Hymenoptera, Cynipoidea: Eucoilidae). Entomol. Scand. 11, 428-453
41. Novkovic, B., Mitsui, H., Suwito, A., and Kimura, M. T. (2011). Taxonomy and phylogeny of Leptopilina species (Hymenoptera: Cynipoidea: Figitidae) attacking frugivorous drosophilid flies in Japan, with description of three new species. Entomol. Sci. 14, 333-346. doi: 10.1111/j.1479-8298.2011.00459.x
42. Pintureau, B., Chapelle, L., and Delobel, B. (1999). Effects of repeated thermic and antibiotic treatments on a Trichogramma (Hym., Trichogrammatidae) symbiont. J. Appl. Entomol. 123, 473-483. doi: 10.1046/j.1439-0418.1999.00412.x
43. Pintureau, B., Lassablière, F., Daumal, J., and Grenier, S. (2002). Does a cyclic natural thermal cure occur in Wolbachia-infected Trichogramma species? Ecol. Entomol. 27, 466-372. doi: 10.1046/j.1365-2311.2002.00416.x
44. Quinlan, J. (1988). A revision of some aftrotropical genera of Eucoilidae (Hymenoptera). Bull. Br. Mus. Nat. Hist. 56, 171-229
45. Ridley, M. (1993). Clutch size and mating frequency in parasitic Hymenoptera. Am. Nat. 142, 893-910. doi: 10.1086/285579
46. Romani, R., Isidoro, N., Riolo, P., Bin, F., Fortunato, A., Turillazzi, S., et al. (2005). A new role for antennation in paper wasps (Hymenoptera, Vespidae): antennal courtship and sex dimorphic glands in antennomeres. Insectes Soc. 52, 92-102. doi: 10.1007/s00040-004-0780-y
47. Ruther, J. (2013). "Novel insights into pheromone-mediated communication in parasitic hymenopterans". in Chemical Ecology of Insect Parasitoids, eds E. Wajnberg and S. Colazza (Hoboken, NJ: Wiley-Blackwell), 112-144
48. Saul, G. B. II. (1961). An analysis of non-reciprocal cross incompatibility in Mormoniella vitripennis (Walker). Z. Vererbungsl. 92, 28-33. doi: 10.1007/BF01854097
49. Stökl, J., Hofferberth, J., Pritschet, M., Brummer, M., and Ruther, J. (2012). Stereoselective chemical defense in the Drosophila parasitoid Leptopilina heterotoma is mediated by (-)-iridomymrecin and (+)-isoiridomyrmecin. J. Chem. Ecol. 38, 331-339. doi: 10.1007/s10886-012-0103-0
50. Stökl, J., Dandekar, A.-T., and 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, 159-168. doi: 10.1007/s10886-014-0378-4
51. Steiner, S., Hermann, N., and Ruther, J. (2006). Characterization of a female-produced courtship pheromone in the parasitoid Nasonia vitripennis. J. Chem. Ecol. 32, 1687-1702. doi: 10.1007/s10886-006-9102-3
52. Stewart-Jones, A., Dewhirst, S. Y., Durrant, L., Fitzgerald, J. D., Hardie, J., Hooper, A. M., et al. (2007). Structure, ratio and patterns of release in the sex pheromone of an aphid, Dysaphis plantaginea. J. Exp. Biol. 210, 4335-4344. doi: 10.1242/jeb.009944
53. Symonds, M. R. E., and Elgar, M. A. (2004). The mode of pheromone evolution: evidence from bark beetles. Proc. Biol. Sci. 271, 839-846. doi: 10.1098/rspb.2003.2647
54. Symonds, M. R. E., and Elgar, M. A. (2008). The evolution of pheromone diversity. Trends Ecol. Evol. 23, 220-228. doi: 10.1016/j.tree.2007.11.009
55. Völkl, W., Hübner, G., and 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. doi: 10.1007/BF02098397
56. van den Assem, J., Jachmann, F., and Simbolotti, P. (1980). Courtship behaviour of Nasonia vitripennis (Hym., Pteromalidae): Some qualitative, experimental evidence for the role of pheromones. Behaviour 75, 301-307. doi: 10.1163/156853980X00456
57. van den Assem, J. (1968). Reproductive behaviour of Pseudeucoila bochei (Hymenoptera: Cynipidae). Neth. J. Zool. 19, 641-649. doi: 10.1163/002829669X00080
58. van den Assem, J. (1986). Insect Parasitoids Chapter Mating Behaviour in Parasitic Wasps. London: Academic Press. 137-167
59. Weiss, I., Rössler, T., Hofferberth, J., Brummer, M., Ruther, J., and Stökl, J. (2013). A nonspecific defensive compound evolves into a competition avoidance cue and a female sex pheromone. Nat. Commun. 4:2767. doi: 10.1038/ncomms3767
60. Wyatt, T. D. (2014). Pheromones and Animal Behaviour: Chemical Signals and Signatures, 2nd Edn. Cambridge, UK: Cambridge University Press