Love makes smell blind: Mating suppresses pheromone attraction in Drosophila females via Or65a olfactory neurons

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Lebreton, Sébastien ^a,b   Grabe, Veit ^b   Omondi, Aman B ^a,c   Ignell, Rickard ^a   Becher, Paul G ^a   Hansson, Bill S ^b   Sachse, Silke ^b   Witzgall, Peter ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^c BIOVERSITY INTERNATIONAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID DERIVATIVE; CELL SURFACE RECEPTOR; CIS-VACCENYL ACETATE; DROSOPHILA PROTEIN; ISOPROTEIN; OLEIC ACID; OLFACTORY RECEPTOR; OR65A PROTEIN, DROSOPHILA; OR67D PROTEIN, DROSOPHILA; PHEROMONE;

ANIMAL; ANTENNA (ORGAN); COURTSHIP; CYTOLOGY; DROSOPHILA MELANOGASTER; FEMALE; FOOD DEPRIVATION; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; ODOR; OLFACTORY RECEPTOR; PHYSIOLOGY; SENSORY NERVE CELL; SEX DIFFERENCE; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION;

ACETATES; ANIMALS; ARTHROPOD ANTENNAE; COURTSHIP; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; FOOD DEPRIVATION; GENE EXPRESSION REGULATION; MALE; OLEIC ACIDS; PHEROMONES; PROTEIN ISOFORMS; RECEPTORS, CELL SURFACE; RECEPTORS, ODORANT; SENSORY RECEPTOR CELLS; SEX FACTORS; SEXUAL BEHAVIOR, ANIMAL; SIGNAL TRANSDUCTION; SMELL;

EID: 84922036010     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep07119     Document Type: Article

References (59)

1. Arnqvist, G. & Nilsson, T. The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav. 60, 145-164 (2000).
2. Fricke, C., Wigby, S., Hobbs, R. & Chapman, T. The benefits of male ejaculate sex peptide transfer in Drosophila melanogaster. J. Evol. Biol. 22, 275-286 (2009).
3. Long, T. A. F., Pischedda, A., Nichols, R. V. & Rice, W. R. The timing of mating influences reproductive success in Drosophila melanogaster: implications for sexual conflict. J. Evol. Biol. 23, 1024-1032 (2010).
4. Kvarnemo, C. & Simmons, L. W. Polyandry as a mediator of sexual selection before and after mating. Phil. Trans. R. Soc. B 368, 20120042 (2013).
5. Ringo, J. Sexual receptivity in insects. Annu. Rev. Entomol. 41, 473-494 (1996).
6. Vargas, M. A., Luo, N. G., Yamaguchi, A. & Kapahi, P. A role for S6 kinase and serotonin in postmating dietary switch and balance of nutrients in D. melanogaster. Curr. Biol. 20, 1006-1011 (2010).
7. Saveer, A. M. et al. Floral to green: mating switches moth olfactory coding and preference. Proc. R. Soc. B 279, 2314-2322 (2012).
8. Liu, H. F. & Kubli, E. Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proc. Natl. Acad. Sc. USA 100, 9929-9933 (2003).
9. Yapici, N., Kim, Y.-J., Ribeiro, C. & Dickson, B. J. A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451, 33-38 (2008).
10. Hasemeyer, M., Yapici, N., Heberlein, U. & Dickson, B. J. Sensory neurons in the Drosophila genital tract regulate female reproductive behavior. Neuron 61, 511-518 (2009).
11. Yang, C. H. et al. Control of the postmating behavioral switch in Drosophila females by internal sensory neurons. Neuron 61, 519-526 (2009).
12. Rezaval, C. et al. Neural circuitry underlying Drosophila female postmating behavioral responses. Curr. Biol. 22, 1155-1165 (2012).
13. Haussmann, I. U., Hemani, Y., Wijesekera, T., Dauwalder, B. & Soller, M. Multiple pathways mediate the sex peptide-regulated switch in female Drosophila reproductive behaviours. Proc. R. Soc. B 280, 20131938 (2013).
14. Chapman, T. et al. The sex peptide of Drosophila melanogaster: female post-mating responses analyzed by using RNA interference. Proc. Natl. Acad. Sci. USA 100, 9923-9928 (2003).
15. Wigby, S. & Chapman, T. Sex peptide causes mating costs in female Drosophila melanogaster. Curr. Biol. 15, 316-321 (2005).
16. Kuijper, B., Stewart, A. D. & Rice, W. R. The cost of mating rises nonlinearly with copulation frequency in a laboratory population of Drosophila melanogaster. J. Evol. Biol. 19, 1795-1802 (2006).
17. Manning, A. Control of sexual receptivity in female Drosophila. Anim. Behav. 15, 239-250 (1967).
18. Scott, D. The timing of the sperm effect on female Drosophila melanogaster receptivity. Anim. Behav. 35, 142-149 (1987).
19. Ram, K. R. & Wolfner, M. F. A network of interactions among seminal proteins underlies the long-term postmating response in Drosophila. Proc. Ntl. Acad. Sc. USA 106, 15384-15389 (2009).
20. Ejima, A. et al. Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr. Biol. 17, 599-605 (2007).
21. Bartelt, R. J., Schaner, A. M. & Jackson, L. L. cis-Vaccenyl acetate as an aggregation pheromone in Drosophila melanogaster. J. Chem. Ecol. 11, 1747-1756 (1985).
22. Kurtovic, A., Widmer, A. & Dickson, B. J. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446, 542-546 (2007).
23. Wang, L. & Anderson, D. J. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463, 227-231 (2010).
24. Keleman, K. et al. Dopamine neurons modulate pheromone responses in Drosophila courtship learning. Nature 489, 145-U210 (2012).
25. Ha, T. S. & Smith, D. P. A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J. Neurosc. 26, 8727-8733 (2006).
26. Van der Goes van Naters, W. & Carlson, J. R. Receptors and neurons for fly odors in Drosophila. Curr. Biol. 17, 606-612 (2007).
27. Kohl, J., Ostrovsky, A. D., Frechter, S. & Jefferis, G. S. X. E. A bidirectional circuit switch reroutes pheromone signals in male and female brains. Cell 155, 1610-1623 (2013).
28. Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirian, L. & Dickson, B. J. Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795-807 (2005).
29. Ruta, V. et al. A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 468, 686-U106 (2010).
30. Dauwalder, B. The roles of fruitless and doublesex in the control of male courtship. Int. Rev. Neurobiol. 99, 87-105 (2011).
31. Zhou, C., Pan, Y. F., Robinett, C. C., Meissner, G. W. & Baker, B. S. Central brain neurons expressing doublesex regulate female receptivity in Drosophila. Neuron 83, 149-163 (2014).
32. Liu, W. W. et al. Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila. Nat. Neurosc. 14, 896-U119 (2011).
33. Wigby, S. et al. Seminal fluid protein allocation and male reproductive success. Curr. Biol. 19, 751-757 (2009).
34. Fricke, C., Bretman, A. & Chapman, T. Adult male nutrition and reproductive success in Drosophila melanogaster. Evolution 62, 3170-3177 (2008).
35. Yew, J. Y., Cody, R. B. & Kravitz, E. A. Cuticular hydrocarbon analysis of an awake behaving fly using direct analysis in real-time time-of-flight mass spectrometry. Proc. Natl. Acad. Sci. USA 105, 7135-7140 (2008).
36. Yew, J. Y. et al. A new male sex pheromone and novel cuticular cues for chemical communication in Drosophila. Curr. Biol. 19, 1245-1254 (2009).
37. Everaerts, C., Farine, J.-P., Cobb, M. & Ferveur, J.-F. Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PloS One 5, e9607 (2010).
38. Butterworth, F. M. Lipids of Drosophila: a newly detected lipid in the male. Science 163, 1356-1357 (1969).
39. Zawistowski, S. & Richmond, R. C. Inhibition of courtship and mating of Drosophila melanogaster by the male-produced lipid, cis-vaccenyl acetate. J. Insect Physiol. 32, 189-192 (1986).
40. Cachero, S., Ostrovsky, A. D., Yu, J. Y., Dickson, B. J. & Jefferis, G. S. X. E. Sexual dimorphism in the fly brain. Curr. Biol. 20, 1589-1601 (2010).
41. Sweeney, S. T., Broadie, K., Keane, J., Niemann, H. & O'Kane, C. J. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14, 341-351 (1995).
42. Couto, A., Alenius, M. & Dickson, B. J. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535-1547 (2005).
43. Olsen, S. R. & Wilson, R. I. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452, 956-960 (2008).
44. Das, S. et al. Plasticity of local GABAergic interneurons drives olfactory habituation. Proc. Natl. Acad. Sci. USA 108, E646-E654 (2011).
45. Root, C. M. et al. A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59, 311-321 (2008).
46. Chapman, T., Liddle, L. F., Kalb, J. M., Wolfner, M. F. & Partridge, L. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373, 241-244 (1995).
47. Pitnick, S. & García-González, F. Harm to females increases with male body size in Drosophila melanogaster. Proc. R. Soc. B 269, 1821-1828 (2002).
48. Wigby, S., Chapman, T., Building, D. & Street, G. Sex peptide causes mating costs in female Drosophila melanogaster. Curr. Biol. 15, 316-321 (2005).
49. Wolfner, M. F. Battle and ballet: molecular interactions between the sexes in Drosophila. J. Hered. 100, 399-410 (2009).
50. Pischedda, A. & Rice, W. R. Partitioning sexual selection into its mating success and fertilization success components. Proc. Natl. Acad. Sci. USA 109, 2049-2053 (2012).
51. Kvarnemo, C. & Simmons, L. W. Polyandry as a mediator of sexual selection before and after mating. Phil. Trans. R. Soc. B 368, 20120042 (2013).
52. Markow, T. A., Quaid, M. & Kerr, S. Male mating experience and competitive courtship success in Drosophila melanogaster. Nature 276, 821-822 (1978).
53. Van Vianen, A. & Bijlsma, R. The adult component of selection in Drosophila melanogaster - some aspects of early-remating activity of females. Heredity 71, 269-276 (1993).
54. Avila, F. W., Sirot, L. K., LaFlamme, B. A., Rubinstein, C. D. & Wolfner, M. F. Insect seminal fluid proteins: identification and function. Annu. Rev. Entomol. 56, 21-40 (2011).
55. Hunt, J., Breuker, C. J., Sadowski, J. A. & Moore, A. J. Male-male competition, female mate choice and their interaction: determining total sexual selection. J. Evol. Biol. 22, 13-26 (2009).
56. Ruebenbauer, A., Schlyter, F., Hansson, B. S., Löfstedt, C. & Larsson, M. C. Genetic variability and robustness of host odor preference in Drosophila melanogaster. Curr. Biol. 18, 1438-1443 (2008).
57. Lebreton, S., Becher, P. G., Hansson, B. S. & Witzgall, P. Attraction of Drosophila melanogaster males to food-related and fly odours. J. Insect Physiol. 58, 125-129 (2012).
58. Becher, P. G., Bengtsson, M., Hansson, B. S. & Witzgall, P. Flying the fly: long-range flight behavior of Drosophila melanogaster to attractive odors. J. Chem. Ecol. 36, 599-607 (2010).
59. Strutz, A., Völler, T., Riemensperger, T., Fiala, A. & Sachse, S. Calcium imaging of neural activity in the olfactory system of Drosophila. Neuromethods/Genetically Encoded Functional Indicators, pp 43-70, ed. Martin, J.-R. (Humana Press, Totowa, NJ, 2012).