The role of cuticular hydrocarbons in mate recognition in Drosophila suzukii

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Snellings, Yannick ^a   Herrera, Beatriz ^b   Wildemann, Bruna ^a   Beelen, Melissa ^a   Zwarts, Liesbeth ^a   Wenseleers, Tom ^a   Callaerts, Patrick ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROCARBON;

AGE; ANIMAL; ANIMAL COMMUNICATION; COURTSHIP; DROSOPHILA; FEMALE; MALE; MATE CHOICE; PHYSIOLOGY;

AGE FACTORS; ANIMAL COMMUNICATION; ANIMALS; COURTSHIP; DROSOPHILA; FEMALE; HYDROCARBONS; MALE; MATING PREFERENCE, ANIMAL;

EID: 85044283038     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-23189-6     Document Type: Article

References (72)

1. Howard, R. W. Chemical ecology and biochemistry of insect hydrocarbons. Ann. Rev. Entomol. 27, 149-172 (1982).
2. Gibbs, A. G., Fukuzato, F. & Matzkin, L. M. Evolution of water conservation mechanisms in. Drosophila. J. Exp. Biol. 206, 1183-1192 (2003).
3. Bontonou, G., Denis, B. & Wicker-Thomas, C. Interaction between temperature and male pheromone in sexual isolation in Drosophila melanogaster. J. Evol. Biol. 26, 2008-2020 (2013).
4. Ferveur, J. F. Cuticular hydrocarbons: Their evolution and roles in Drosophila pheromonal communication. Behav. Genet. 35, 279-295 (2005).
5. Van Oystaeyen, A. et al. Conserved class of queen pheromones stop social insect workers from reproducing. Science 343, 287-290 (2014).
6. Millar, J. Chemical synthesis of insect cuticular hydrocarbons. In Insect Hydrocarbons Biology, Biochemistry, and Chemical Ecology (ed. Blomquist, G. J. & Bagnères A.), pp. 163-186 (Cambridge University Press, 2010).
7. Romer, F. et al. The oenocytes of insects: differentiation, changes during molting and their possible involvement in the secretion of molting hormone. In Morphogenetic Hormones of Arthropods: Roles in Histogenesis, Organogenesis, and Morphogenesis (ed. Gupta, A. P.), pp. 542-566 (New Brunswick: Rutgers University Press, 1991).
8. Ferveur, J. F. et al. Genetic feminization of pheromones and its behavioral consequences in Drosophila males. Science 276, 1555-1558 (1997).
9. Krupp, J. J. & Levine, J. D. Dissection of oenocytes from adult Drosophila melanogaster. J. Vis. Exp. 41, e2242, https://doi. org/10. 3791/2242 (2010).
10. Farine, J. P., Ferveur, J. F. & Everaerts, C. Volatile Drosophila cuticular pheromones are affected by social but not sexual experience. PloS One 7, e40396, https://doi. org/10. 1371/journal. pone. 0040396 (2012).
11. Yew, J. Y. & Chung, H. Insect pheromones: An overview of function, form and discovery. Prog. Lipid Res. 59, 88-105 (2015).
12. Lin, C. C., Prokop-Pringe, K. A., Preti, G. & Potter, C. J. Food odors trigger Drosophila males to deposit a pheromone that guides aggregation and female oviposition decisions. eLife 30, e08688, https://doi. org/10. 7554/eLife. 08688 (2015).
13. Marcillac, F., Houot, B. & Ferveur, J. F. Revisited roles of Drosophila female pheromones. Chem. senses 30, 273-274 (2005).
14. Billeter, J. C. & Levine, J. D. Who is he and what is he to you Recognition in Drosophila melanogaster. Curr. Opin. Neurobiol. 23, 17-23 (2013).
15. Jallon, J. M., Antony, C. & Benamar, O. An anti-aphrodisiac produced by Drosophila melanogaster males and transferred to females during copulation. C. R. Acad. Sci. Ser. III 292, 1147-1149 (1981).
16. Zawistowski, S. & Richmond, R. C. Inhibition of courtship and mating of Drosophila melanogaster by the male-produced lipid, cisvaccenyl acetate. J Insect Physiol. 32, 189-192 (1986).
17. Scott, D. & Richmond, R. C. Evidence against an antiaphrodisiac role for cis-vaccenyl acetate in Drosophila melanogaster. J. Insect Physiol. 33, 363-369 (1986).
18. Davies, R. L. The scent of Drosophila sex. Neuron 54, 14-16 (2007).
19. Ferveur, J. F. & Sureau, G. Simultaneous influence on male courtship of stimulatory and inhibitory pheromones produced by live sex-mosaic Drosophila melanogaster. Proc. R. Soc. B. 263, 967-973 (1996).
20. Antony, C. & Jallon, J. M. The chemical basis for sex recognition in Drosophila melanogaster. J. Insect. Physiol. 28, 873-880 (1982).
21. Grillet, M., Dartevelle, L. & Ferveur, J. F. A drosophila male pheromone affects female sexual receptivity. Proc. R. Soc. C. 273, 315-323 (2006).
22. Foley, B., Chenoweth, S. F., Nuzhdin, S. V. & Blows, M. W. Natural genetic variation in cuticular hydrocarbon expression in male and female Drosophila melanogaster. Genetics 175, 1465-1477 (2007).
23. Tillman, J. A., Seybold, S. J., Jurenka, R. A. & Blomquist, G. J. Insect pheromones: An overview of biosynthesis and endocrine regulation. Insect Biochem. Mol. Biol. 29, 481-514 (1999).
24. Fan, P. et al. Genetic and neural mechanisms that inhibit Drosophila from mating with other species. Cell. 154, 89-102 (2013).
25. Chung, H. & Carroll, S. B. Wax, sex and the origin of species: dual roles of insect cuticular hydrocarbons in adaptation and mating. BioEssays 37, 822-830 (2015).
26. Dyer, K. A., White, B. E., Sztepanacz, J. L., Bewick, E. R. & Rundle, H. D. Reproductive character displacement of epicuticular compounds and their contribution to mate choice in Drosophila subquinaria and Drosophila recens. Evolution. 68, 1163-1175 (2014).
27. Greenberg, A. J., Moran, J. R., Coyne, J. A. & Wu, C. Ecological adaptation during incipient speciation revealed by precise gene replacement. Science 302, 1754-1757 (2003).
28. Howard, R. W., Jackson, L. L., Banse, H. & Blows, M. W. Cuticular hydrocarbons of Drosophila birchii and D. serrata: identification and role in mat choice in D. serrata. J. Chem. Ecol. 29, 961-976 (2003).
29. Rundle, H. D., Chenoweth, S. F., Doughty, P. & Blows, M. W. Divergent selection and the evolution of signal traits and mating preference. PLoS Biol. 12, e1001836, https://doi. org/10. 1371/journal. pbio. 1001836 (2005).
30. Savarit, F., Sureau, G., Cobb, M. & Ferveur, J.-F. Genetic elimination of known pheromones reveals the fundamental chemical bases of mating and isolation in Drosophila. Proc. Natl. Acad. Sci. USA 96, 9015-9020 (1999).
31. Smadja, C. & Butlin, R. K. On the scent of speciation: The chemosensory system and its role in premating isolation. Heredity 102, 77-97 (2009).
32. Wicker-Thomas, C., Guenachi, I. & Keita, Y. F. Contribution of oenocytes and pheromones to courtship behaviour in. Drosophila. BMC Biochem. 10, e147120911021, https://doi. org/10. 1186/1471-2091-10-21 (2009).
33. Kuo, T. H. et al. Aging modulates cuticular hydrocarbons and sexual attractiveness in Drosophila melanogaster. J. Exp. Biol. 215, 814-821 (2012).
34. Everaerts, C., Farine, J. P., Cobb, M. & Ferveur, J. F. Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PloS One 5, e9607, https://doi. org/10. 1371/journal. pone. 0009607 (2010).
35. Rajpurohit, S. et al. Adaptive dynamics of cuticular hydrocarbons in Drosophila. J. Evol. Biol. 30, 66-80 (2017).
36. Fedina, T. Y. et al. Dietary effects on cuticular hydrocarbons and sexual attractiveness in Drosophila. PLoS One 7, e49799, https://doi. org/10. 1371/journal. pone. 0049799 (2012).
37. Chiang, Y. N. et al. Steroid hormone signaling is essential for pheromone production and oenocyte survival. PLoS Genet. 12, e1006126, https://doi. org/10. 1371/journal. pgen. 1006126 (2016).
38. Shirangi, T. R., Dufour, H. D., Williams, T. M. & Carroll, S. B. Rapid evolution of sex pheromone-producing enzyme expression in Drosophila. PLoS Biol. 7, e1000168, https://doi. org/10. 1371/journal. pbio. 1000168 (2009).
39. Krupp, J. J. et al. Social experience modifies pheromone expression and mating behavior in male Drosophila melanogaster. Curr. Biol. 18, 1373-1383 (2008).
40. Rota-Stabbelli, O., Blaxter, M. & Anfora, G. Drosophila suzukii. Curr. Biol. 23, R8-R9 (2013).
41. Dreves, A., Walton, V. & Fisher, G. A new pest attacking healthy ripening fruit in Oregon. OSU extension catalog, https://catalog. extension. oregonstate. edu/em8991 (2009).
42. Dreves, A. IPM program development for an invasive pest: coordination, outreach and evaluation. Pest Manag. Sci. 67, 1403-1420 (2011).
43. Hauser, M. 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 (2011).
44. Calabria, G., Máca, J., Bächli, G., Serra, L. & Pascual, M. First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J. Appl. Entomol. 136, 139-147 (2012).
45. Dekker, T. et al. Loss of Drosophila pheromone reverses its role in sexual communication in Drosophila suzukii. Proc. R. Soc. B. 282, 20143018, https://doi. org/10. 1098/rspb. 2014. 3018 (2015).
46. Revadi, S. et al. Sexual behavior of Drosophila suzukii. Insects 6, 183-196 (2015).
47. Blomquist, G. J. et al. Hydrocarbon and hydrocarbon derived sex pheromones in insects: biochemistry and endocrine regulation. In Insect Lipids: Chemistry, Biochemistry and Biology, pp. 317-351 (U. of Nebraska Press, 1993).
48. Gleason, J. M., James, R. A., Wicker-Thomas, C. & Ritchie, M. G. Identification of quantitative trait loci function through analysis of multiple cuticular hydrocarbons differing between Drosophila simulans and Drosophila sechellia females. Heredity 103, 416-424 (2009).
49. Ferveur, J. F. Genetic control of pheromones in Drosophila simulans. I. Ngbo, a locus on the second chromosome. Genetics 128, 293-301 (1991).
50. Gleason, J. M., Jallon, J. M., Rouault, J. D. & Ritchie, M. G. Quantitative trait loci for cuticular hydrocarbons associated with sexual isolation between Drosophila simulans and Drosophila sechellia. Genetics 17, 1789-1798 (2005).
51. Liimatainen, J. O. & Jallon, J. M. Genetic analysis of cuticular hydrocrbons and their effect on courtship in Drosophila virilis and D. lummei. Behav. Genet. 37, 713-725 (2007).
52. Laturney, M. & Billeter, J. C. Drosophila melanogaster females restore their attractiveness after mating by removing male antiaphrodisiac pheromones. Nat. Commun. 7, 12322, https://doi. org/10. 1038/ncomms12322 (2016).
53. Weiss, I., Hoffenberth, J., Ruther, J. & Stökl, J. Varying importance of cuticular hydrocarbons and iridoids in the species-specific mate recognition pheromones of three closely related Leptopilina species. Front. Ecol. Evol. 16, e201500019, https://doi. org/10. 3389/ fevo. 2015. 00019 (2015).
54. Singer, T. L. Roles of hydrocarbons in recognition systems of insects. Amer. Zool. 38, 394-405 (1998).
55. Dweck, H. K. et al. Pheromones mediating copulation and attraction in Drosophila. Proc. Natl. Acad. Sci. USA 112, E2829-E2835 (2015).
56. Landolt, P. J., Adams, T. & Rogg, H. Trapping spotted wing Drosophila, Drosophila suzukii (Diptera: Drosophilidae), with combinations of vinegars and wine, and acetic acid and ethanol. J. Appl. Entomol. 95, 148-154 (2012).
57. Walsh, D. et al. Drosophila suzukii (Diptera: Drosophilidae): Invasive pest of ripening soft fruit expanding its geographic range and damage potential. J. Int. Pest Manag. 2, G1-G7 (2011).
58. Shani, A. Chemical communication agents (pheromones) in integrated pest management. Drug Dev. Res. 50, 400-405 (2000).
59. Witzgall, P., Kirsch, P. & Cork, A. Sex pheromones and their impact on pest management. J. Chem. Ecol. 36, 80-100 (2010).
60. El-Sayed, A. M., Suckling, D. M., Byers, J. A., Jang, E. B. & Wearing, C. H. Potential of lure and kill in long-term pest management and eradication of invasive species. J. Econ. Entomol. 102, 815-835 (2009).
61. El-Sayed, A. M., Suckling, D. M., Wearing, C. H. & Byers, J. A. Potential of mass trapping for long-term pest management and eradication of invasive species. J. Econ. Entomol. 99, 1550-1564 (2006).
62. Byers, J. A. Simulation of mating disruption and mass trapping with competitive attraction and camouflage. Environ. Entomol. 36, 1328-1338 (2007).
63. Messadi, D., Helaimia, F., Ali-Mokhnache, S. & Boumahraz, M. Accurate determination of retention indices in programmed temperature gas chromatography. Chromatographia 29, 429-434 (1990).
64. Carlson, D. A., Bernier, U. R. & Sutton, B. D. Elution patterns from capillary GC for methyl-branced alkanes. J. Chem. Ecol. 24, 1845-1865 (1998).
65. Krkosova, Z., Kubinex, R., Sojak, L. & Amann, A. Temperature-programmed gas chromatography linear retention indices of all C4-C30 monomethylalkanes on methylsilicone OV-1 stationary phase: contribution towards a better understanding of volatile organic compounds in exhaled breath. J. Chromatogr. A 1179, 59-68 (2008).
66. Carlson, D. A., Roan, C. S., Yost, R. A. & Hector, J. Dimethyl disulfide derivatives of long chain alkenes, alkadienes, and alkatrienes for gas chromatography/mass spectrometry. Anal. Chem. 61, 1564-1571 (1989).
67. Mazzoni, V., Anfora, G. & Virant-Doberlet, M. Substrate vibrations during courtship in three Drosophila species. PloS One 8, e80708, https://doi. org/10. 1371/journal. pone. 0080708 (2013).
68. Bontonou, G. & Wicker-Thomas, C. Sexual communication in the Drosophila genus. Insects 5, 439-458 (2014).
69. Aitchison, J. The Statistical Analysis of Compositional Data. Caldwell, NJ: Blackburn Press (2003).
70. Huber, P. J. Robust Statistics (2nd ed.). Hoboken, NJ: John Wiley & Sons Inc (2005).
71. Firth, D. Bias reduction of maximum likelihood estimates. Biometrika 80, 27-38 (1993).
72. Heinze, G. A comparative investigation of methods for logistic regression with separated or nearly separated data. Stat. Med. 24, 4216-4226 (2006).