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PLOS ONE  2012 

Volatile Drosophila Cuticular Pheromones Are Affected by Social but Not Sexual Experience

DOI: 10.1371/journal.pone.0040396

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Abstract:

Recognition of conspecifics and mates is based on a variety of sensory cues that are specific to the species, sex and social status of each individual. The courtship and mating activity of Drosophila melanogaster flies is thought to depend on the olfactory perception of a male-specific volatile pheromone, cis-vaccenyl acetate (cVA), and the gustatory perception of cuticular hydrocarbons (CHs), some of which are sexually dimorphic. Using two complementary sampling methods (headspace Solid Phase Micro-Extraction [SPME] and solvent extraction) coupled with GC-MS analysis, we measured the dispersion of pheromonal CHs in the air and on the substrate around the fly. We also followed the variations in CHs that were induced by social and sexual interactions. We found that all CHs present on the fly body were deposited as a thin layer on the substrate, whereas only a few of these molecules were also detected in the air. Moreover, social experience during early adult development and in mature flies strongly affected male volatile CHs but not cVA, whereas sexual interaction only had a moderate influence on dispersed CHs. Our study suggests that, in addition to their role as contact cues, CHs can influence fly behavior at a distance and that volatile, deposited and body pheromonal CHs participate in a three-step recognition of the chemical identity and social status of insects.

References

[1]  Greenspan RJ, Ferveur JF (2000) Courtship in Drosophila. Annu Rev Genet 34: 205–232.
[2]  Hall JC (2002) Courtship lite: a personal history of reproductive behavioral neurogenetics in Drosophila. Journal of Neurogenetics 16: 135–163.
[3]  O’Dell K (2003) The voyeurs’ guide to Drosophila melanogaster courtship. Behav Process 64: 211–223.
[4]  Lasbleiz C, Ferveur JF, Everaerts C (2006) Courtship behaviour of Drosophila melanogaster revisited. Anim Behav 72: 1001–1012.
[5]  Yamamoto D, Jallon JM, Komatsu A (1997) Genetic dissection of sexual behavior in Drosophila melanogaster. Annu Rev Entomol 42: 551–585.
[6]  Meissner G, Manoli D, Chavez J, Knapp J, Lin T, et al. (2011) Functional dissection of the neural substrates for sexual behaviors in Drosophila melanogaster. Genetics 189: 195–U875. DOI:10.1534/genetics.111.129940.
[7]  Wyatt TD (2003) Pheromones and animal behaviour. Communication by smell and taste. (Cambridge University Press, Cambridge) 1st Ed p 391.
[8]  Becher PG, Bengtsson M, Hansson BS, Witzgall P (2010) Flying the fly: long-range flight behavior of Drosophila melanogaster to attractive odors J Chem Ecol 36: 599–607.
[9]  Budick SA, Dickinson MH (2006) Free-flight responses of Drosophila melanogaster to attractive odors. J Exp Biol 209: 3001–3017.
[10]  Hansson BS, Knaden M, Sachse S, Stensmyr MC, Wicher D (2010) Towards plant-odor-related olfactory neuroethology in Drosophila. Chemoecology 20: 51–61.
[11]  Griffith LC, Ejima A (2009) Multimodal sensory integration of courtship stimulating cues in Drosophila melanogaster. Ann N Y Acad Sci 1170: 394–398.
[12]  Butterworth FM (1969) Lipids of Drosophila: a newly detected lipid in the male. Science 163: 1356–1357.
[13]  Bartelt RJ, Schaner AM, Jackson LL (1985) Cis-Vaccenyl acetate as an aggregation pheromone in Drosophila melanogaster. J Chem Ecol 11: 1747–1756.
[14]  Grosjean Y, Rytz R, Farine JP, Abuin L, Cortot J, et al. (2011) An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478: 236–240.
[15]  Ayasse M, Paxton RJ, Tengo J (2001) Mating behavior and chemical communication in the order Hymenoptera. Annu Rev Entomol 46: 31–78.
[16]  Sivinski J, Epsky N, Heath RR (1994) Pheromone deposition on leaf territories by male Caribbean fruit flies, Anastrepha suspensa (Loew) (Diptera: Tephritidae). J Insect Behav 7: 43–51.
[17]  Shelly T (2004) Scent marking by males of the mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). J Insect Behav 17: 709–722.
[18]  Droney D, Hock M (1998) Male sexual signals and female choice in Drosophila grimshawi (Diptera: Drosophilidae). J Insect Behav 11: 59–71.
[19]  Widemo F, Johansson BG (2006) Male-male pheromone signalling in a lekking Drosophila. Proc Biol Sci 273: 713–717.
[20]  Jallon JM, Antony C, Benamar O (1981) An anti-aphrodisiac produced by Drosophila melanogaster males and transferred to females during copulation. C R Acad Sci Ser III Sci Vie 292: 1147–1149.
[21]  Zawistowski S, Richmond RC (1986) inhibition of courtship and mating of Drosophila melanogaster by the male-produced lipid, cis-vaccenyl acetate. J Insect Physiol 32: 189–192.
[22]  Kurtovic A, Widmer A, Dickson BJ (2007) A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446: 542–546.
[23]  Wang L, Anderson DJ (2010) Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463: 227–231.
[24]  Symonds MRE, Wertheim B (2005) The mode of evolution of aggregation pheromones in Drosophila species. J Evol Biol 18: 1253–1263.
[25]  Ferveur JF (2005) Cuticular hydrocarbons: Their evolution and roles in Drosophila pheromonal communication. Behavior Genetics 35: 279–295.
[26]  Wicker-Thomas C (2007) Pheromonal communication involved in courtship behavior in Diptera. J Insect Physiol 53: 1089–1100.
[27]  Howard RW, Blomquist GJ (1982) Chemical ecology and biochemistry of insect hydrocarbons. Annu Rev Entomol 27: 149–172.
[28]  Blomquist G, Nelson D, de Renobales M (1987) Chemistry, biochemistry, and physiology of insect cuticular lipids. Arch Insect Biochem Physiol 6: 227–265.
[29]  Gibbs AG, Fukuzato F, Matzkin LM (2003) Evolution of water conservation mechanisms in Drosophila. J Exp Biol 206: 1183–1192.
[30]  Rouault JD, Marican C, Wicker-Thomas C, Jallon JM (2004) Relations between cuticular hydrocarbon (HC) polymorphism, resistance against desiccation and breeding temperature; a model for HC evolution in D. melanogaster and D. simulans. Genetica 120: 195–212.
[31]  Foley BR, Telonis-Scott M (2011) Quantitative genetic analysis suggests causal association between cuticular hydrocarbon composition and desiccation survival in Drosophila melanogaster. Heredity 106: 68.
[32]  Antony C, Jallon JM (1982) The chemical basis for sex recognition in Drosophila melanogaster. J Insect Physiol 28: 873–880.
[33]  Jallon JM (1984) A few chemical words exchanged by Drosophila during courtship and mating. Behavior Genetics 14: 441–478.
[34]  Marcillac F, Grosjean Y, Ferveur JF (2005) A single mutation alters production and discrimination of Drosophila sex pheromones. Proc R Soc Biol Sci Ser B 272: 303–309.
[35]  Ferveur JF, Sureau G (1996) Simultaneous influence on male courtship of stimulatory and inhibitory pheromones produced by live sex-mosaic Drosophila melanogaster. Proc R Soc Biol Sci Ser B 263: 967–973.
[36]  Lacaille F, Hiroi M, Twele R, Inoshita T, Umemoto D, et al. (2007) An inhibitory sex pheromone tastes bitter for Drosophila males. PLoS One 2(8): e661.
[37]  Svetec N, Ferveur JF (2005) Social experience and pheromonal perception can change male-male interactions in Drosophila melanogaster. J Exp Biol 208: 891–898.
[38]  Grillet M, Dartevelle L, Ferveur JF (2006) A Drosophila male pheromone affects female sexual receptivity. Proc R Soc Biol Sci Ser. B 273: 315–323.
[39]  Scott D, Shields A, Straker M, Dalrymple H, Dhillon PK, et al. (2011) Variation in the male pheromones and mating success of wild caught Drosophila melanogaster. PLoS One 6(8): e23645.
[40]  Siwicki KK, Riccio P, Ladewski L, Marcillac F, Dartevelle L, et al. (2005) The role of cuticular pheromones in courtship conditioning of Drosophila males. Learning, Memory 12: 636–645.
[41]  Krupp JJ, Kent C, Billeter JC, Azanchi R, So AKC, et al. (2008) Social experience modifies pheromone expression and mating behavior in male Drosophila melanogaster. Curr Biol 18: 1373–1383.
[42]  Boll W, Noll M (2002) The Drosophila Pox neuro gene: control of male courtship behavior and fertility as revealed by a complete dissection of all enhancers. Development 129: 5667–5681.
[43]  Shanbhag S, Park S, Pikielny C, Steinbrecht R (2001) Gustatory organs of Drosophila melanogaster: fine structure and expression of the putative odorant-binding protein PBPRP2. Cell Tissue Res 304: 23–437.
[44]  Stocker RF (1994) The organization of the chemosensory system in Drosophila melanogaster - a review. Cell Tissue Res 275: 3–26.
[45]  van der Goes van Naters W, Carlson JR (2007) Receptors and neurons for fly odors in Drosophila. Curr Biol 17: 606–612.
[46]  Mehren JE (2007) Mate recognition: Should fly stay, or should fly go? Curr Biol 17: R240–R242.
[47]  Lebreton S, Becher PG, Hansson BH, Witzgall P (2012) Attraction of Drosophila melanogaster males to food-related and fly odours. J Insect Physiol 58: 125–129.
[48]  Arthur CL, Pawliszyn J (1990) Solid-phase microextraction with thermal-desorption using fused-silica optical fibers. Anal Chem 62: 2145–2148.
[49]  Ferveur JF, Jallon JM (1993) Genetic-control of pheromones in Drosophila simulans.2. Kete, a locus on the X-chromosome. Genetics 133: 561–567.
[50]  Kent C, Azanchi R, Smith B, Formosa A, Levine JD (2008) Social context influences chemical communication in D. melanogaster males. Curr Biol 18: 1384–1389.
[51]  Liu W, Liang X, Gong J, Yang Z, Zhang YH, et al. (2011) Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila. Nat Neurosci 14: 896–902.
[52]  Everaerts C, Farine JP, Cobb M, Ferveur JF (2010) Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PLoS One 5(3): e9607.
[53]  Sturtevant AH (1915) Experiments on sex recognition and the problems of sexual selection in Drosophila. Anim Behav 5: 351–366.
[54]  Shorey H, Bartell R (1970) Role of a volatile female sex pheromone in stimulating male courtship behaviour in Drosophila melanogaster. Anim Behav 18: 159–164.
[55]  Rybak F, Aubin T, Moulin B, Jallon JM (2002) Acoustic communication in Drosophila melanogaster courtship: are pulse- and sine-song frequencies important for courtship success? Can J Zool 80: 987–996.
[56]  Everaerts C, Lacaille F, Ferveur JF (2010) Is mate choice in Drosophila males guided by olfactory or gustatory pheromones? Anim Behav 79: 1135–1146.
[57]  Chikos JS, Wilson JA (1994) Vaporization enthalpies at 298.15 K of the n-alkanes from C21 to C28 and C30. J Chem Eng Data 42: 190–197.
[58]  Said I, Gaertner C, Renou M, Rivault C (2005) Perception of cuticular hydrocarbons by the olfactory organs in Periplaneta americana (L.) (Insecta : Dictyoptera). J Insect Physiol 51: 1384–1389.
[59]  Bland JM, Osbrink WLA, Cornelius ML, Lax AR, Vigo CG (2001) Solid-phase microextraction for the detection of termite cuticular hydrocarbons. J Chromatogr A 932: 119–127.
[60]  Levine J, Billeter JC, Krull U, Sodhi R (2011) The cuticular surface of D. melanogaster: ToF-SIMS on the fly. Surf Interface Anal 43: 317–321.
[61]  Chow D, Frye M (2009) The neuro-ecology of resource localization in Drosophila. Fly 3: 50–61.
[62]  Bell W, Tortorici C, Roggero R, Kipp L, Tobin T (1985) Sucrose-stimulated searching behavior of Drosophila melanogaster in a uniform habitat – modulation by period of deprivation. Anim Behav 33: 436–448.
[63]  Tortorici C, Brody A, Bell W (1986) Influence of spatial patterning of resources on search orientation of adult Drosophila melanogaster. Anim Behav 34: 1568–1570.
[64]  Metzger M, Fischbein D, Auguste A, Fauvergue X, Bernstein C, et al. (2010) Synergy in information use for mate finding: demonstration in a parasitoid wasp. Anim Behav 79: 1307–1315.
[65]  Lecomte C, Thibout E, Pierre D, Auger J (1998) Transfer, perception, and activity of male pheromone of Acrolepiopsis assectella with special reference to conspecific male sexual inhibition. J Chem Ecol 24: 655–671.
[66]  Schlief ML, Wilson RI (2007) Olfactory processing and behavior downstream from highly selective receptor neurons. Nat Neurosci 10: 623–630.
[67]  Kohatsu S, Koganezawa M, Yamamoto D (2011) Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 69: 498–508.
[68]  Inoshita T, Martin JR, Marion-Poll F, Ferveur JF (2011) Peripheral, central and behavioral responses to the cuticular pheromone bouquet in Drosophila melanogaster males. PLoS One 6(5): e19770.
[69]  Bray S, Amrein H (2003) A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39: 1019–1029.
[70]  Miyamoto T, Amrein H (2008) Suppression of male courtship by a Drosophila pheromone receptor. Nat Neurosci 11: 874–876.
[71]  Moon SJ, Lee Y, Jiao Y, Montell C (2009) A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr Biol 19: 1623–1627.
[72]  Ronderos DS, Smith DP (2010) Activation of the T1 neuronal circuit is necessary and sufficient to induce sexually dimorphic mating behavior in Drosophila melanogaster. J Neurosci 30: 2595–2599.
[73]  Wang L, Han X, Mehren J, Hiroi M, Billeter JC, et al. (2011) Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat Neurosci 14: 757–762.
[74]  Thomas ML, Simmons LW (2011) Short-term phenotypic plasticity in long-chain cuticular hydrocarbons. Proc Biol Sci 278: 3123–3128.
[75]  Svetec N, Houot B, Ferveur JF (2005) Effect of genes, social experience, and their interaction on the courtship behaviour of transgenic Drosophila males. Genet Res 85: 183–193.
[76]  Fernandez MP, Chan YB, Yew JY, Billeter JC, Dreisewerd K, et al. (2010) Pheromonal and behavioral cues trigger male-to-female aggression in Drosophila. PLoS Biol. 8(11): e1000541.
[77]  Villaverde ML, Girotti JR, Mijailovsky SJ, Pedrini N, Juarez MP (2009) Volatile secretions and epicuticular hydrocarbons of the beetle Ulomoides dermestoides. Comp Biochem Physiol B Biochem Mol Biol 154: 381–386.
[78]  Vrontou E, Nilsen SP, Demir E, Kravitz EA, Dickson BJ (2006) fruitless regulates aggression and dominance in Drosophila. Nat Neurosci 9: 1469–1471.
[79]  Zwarts L, Magwire MM, Carbone MA, Versteven M, Herteleer L, et al. (2011) Complex genetic architecture of Drosophila aggressive behavior. Proc Natl Acad Sci USA 108: 17070–17075.
[80]  Svetec N, Cobb M, Ferveur JF (2005) Chemical stimuli induce courtship dominance in Drosophila. Curr Biol 15: R790–R792.
[81]  Savarit F, Sureau G, Cobb M, Ferveur JF (1999) Genetic elimination of known pheromones reveals the fundamental chemical bases of mating and isolation in Drosophila. Proc Natl Acad Sci USA. 96: 9015–9020.
[82]  Marcillac F, Ferveur JF (2004) A set of female pheromones affects reproduction before, during and after mating in Drosophila. J Exp Biol 207: 3927–3933.
[83]  Carlson DA, Bernier UR, Sutton BD (1998) Elution patterns from capillary GC for methyl-branched alkanes. J Chem Ecol 24: 1845–1865.
[84]  Addinsoft (1995–2011) XLstat. Data analysis and statistics with Microsoft Excel (Paris, France), 2011.4.02/MacOS.
[85]  Aitchison J (1986) The statistical analysis of compositional data. Mono-graphs on statistics and applied probability. (Chapman, Hall Ltd., London (UK)) p 416.
[86]  Thió-Henestrosa S, Martín-Fernández JA (2005) Dealing with compositional data: the freeware CoDaPack. Mathematical Geology. 37(7): 773–793.

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