Genes and circuits of courtship behaviour in drosophila males

Nature Reviews Neuroscience

Volumn 14, Issue 10, 2013, Pages 681-692

  Yamamoto, Daisuke ^a   Koganezawa, Masayuki ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COURTSHIP; DROSOPHILA; GENE; GENE EXPRESSION; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SEXUAL BEHAVIOR;

ANIMALS; CENTRAL NERVOUS SYSTEM; COURTSHIP; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; MALE; NERVE TISSUE PROTEINS; NEURONS; SEXUAL BEHAVIOR, ANIMAL; TRANSCRIPTION FACTORS;

EID: 84884575862     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn3567     Document Type: Review

References (89)

1. Baker, B. S. Taylor, B. J. & Hall, J. C. Are complex behaviors specified by dedicated regulatory genes? Reasoning from Drosophila. Cell 105, 13-24 (2001). (Pubitemid 32323913)
2. Dickson, B. J. Wired for sex: the neurobiology of Drosophila mating decisions. Science 322, 904-909 (2008).
3. Bastock, M. & Manning, A. The courtship of Drosophila melanogaster. Behaviour 8, 85-111 (1955).
4. Greenspan, R. J. & Ferveur, J. Courtship in Drosophila. Annu. Rev. Genet. 34, 205-232 (2000). (Pubitemid 32065921)
5. Hall, J. C. Genetics of the nervous system in Drosophila. Q. Rev. Biophys. 15, 223-479 (1982).
6. Ferveur, J. F. Drosophila female courtship and mating behaviors: sensory signals, genes, neural structures and evolution. Curr. Opin. Neurobiol. 20, 764-769 (2010).
7. Kim, W. J., Jan, L. Y. & Jan, Y. N. Contribution of visual and circadian neural circuits to memory for prolonged mating induced by rivals. Nature Neurosci. 15, 876-883 (2012).
8. Siegel, R. W. & Hall, J. C. Conditioned responses in courtship behavior of normal and mutant Drosophila. Proc. Natl Acad. Sci. USA 76, 3430-3434 (1979). (Pubitemid 9233974)
9. Gill, K. S. A mutation causing abnormal courtship and mating behavior in males of Drosophila melanogaster. Am. Zool. 3, 507 (1963).
10. Hall, J. C. Portions of the central nervous system controlling reproductive behavior in Drosophila melanogaster. Behav. Genet. 7, 291-312 (1977). (Pubitemid 8173406)
11. Ito, H. et al. Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc. Natl Acad. Sci. USA 93, 9687-9692 (1996). (Pubitemid 26296670)
12. Ryner, L. C. et al. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87, 1079-1089 (1996). (Pubitemid 26427991)
13. Goodwin, S. F. et al. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics 154, 725-745 (2000). (Pubitemid 30096594)
14. Heinrichs, V., Ryner, L. C. & Baker, B. S. Regulation of sex-specific selection of fruitless 5' splice sites by transformer and transformer-2. Mol. Cell. Biol. 18, 450-458 (1998). (Pubitemid 28021056)
15. Lee, G. et al. Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. J. Neurobiol. 15, 404-426 (2000). (Pubitemid 30409628)
16. Usui-Aoki, K. et al. Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nature Cell Biol. 2, 500-506 (2000).
17. Anand, A. et al. Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics 158, 1569-1595 (2001). (Pubitemid 32783142)
18. Rideout, E. J., Dornan, A. J., Neville, M. C., Eadie, S. & Goodwin, S. F. Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nature Neurosci. 13, 458-466 (2010).
19. Robinett, C. C., Vaughan, A. G., Knapp, J. & Baker, B. S. Sex and the single cell. II. There is a time and place for sex. PLoS Biol. 8, e1000365 (2010).
20. Sanders, L. E. & Arbeitman, M. N. Doublesex establishes sexual dimorphism in the Drosophila central nervous system in an isoform-dependent manner by directing cell number. Dev. Biol. 320, 378-390 (2008).
21. Lee, G., Hall, J. C. & Park, J. H. doublesex gene expression in the central nervous system of Drosophila melanogaster. J. Neurogenet. 16, 229-248 (2002). (Pubitemid 36745195)
22. Burtis, K. C. & Baker, B. S. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56, 997-1010 (1989). (Pubitemid 19091012)
23. Demir, E. & Dickson, B. J. fruitless splicing specifies male courtship behavior in Drosophila. Cell 121, 785-794 (2005). (Pubitemid 40797600)
24. Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirián, L. & Dickson, B. J. Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795-807 (2005). (Pubitemid 40797601)
25. Manoli, D. S. et al. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436, 395-400 (2005). (Pubitemid 41059049)
26. Ferri, S. L., Bohm, R. A., Lincicome, H. E. & Hall, J. C. & Villella, A. fruitless gene products truncated of their male-like qualities promote neural and behavioral maleness in Drosophila if these proteins are produced in the right places at the right times. J. Neurogenet. 22, 17-55 (2008). (Pubitemid 351431185)
27. Boerjan, B., Tobback, J., De Loof, A., Schoofs, L. & Huybrechts, R. Fruitless RNAi knockdown in males interferes with copulation success in Schistocerca gregaria. Insect Biochem. Mol. Biol. 41, 340-347 (2011).
28. Clynen, E., Ciudad, L., Belles, X. & Piulachs, M. D. Conservation of fruitless' role as master regulator of male courtship behaviour from cockroaches to flies. Dev. Genes Evol. 221, 43-48 (2011).
29. Gailey, D. A. et al. Functional conservation of the fruitless male sex-determination gene across 250 Myr of insect evolution. Mol. Biol. Evol. 23, 633-643 (2006). (Pubitemid 43278275)
30. Ito, H. et al. Fruitless recruits two antagonistic chromatin factors to establish single-neuron sexual dimorphism. Cell 149, 1327-1338 (2012).
31. Dalton, J. E., Lebo, M. S., Sanders, L. E., Sun, F. & Arbeitman, M. N. Ecdysone receptor acts in fruitless-expressing neurons to mediate Drosophila courtship behaviors. Curr. Biol. 19, 1447-1452 (2009).
32. Kimura, K., Ote, M., Tazawa, T. & Yamamoto, D. Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Nature 438, 229-233 (2005). (Pubitemid 41599875)
33. Cashero, S., Ostrovsky, A. D., Yu, J. Y., Dickson, B. J. & Jefferis, G. S. Sexual dimorphism in the fly brain. Curr. Biol. 20, 1589-1601 (2010).
34. Chiang, A. et al. Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr. Biol. 21, 1-11 (2011).
35. Ito, M., Masuda, N., Shinomiya, K., Endo, K. & Ito, K. Systematic analysis of neural projections reveals clonal composition of the Drosophila brain. Curr. Biol. 23, 644-655 (2013).
36. Jefferis, G. S. et al. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128, 1187-1203 (2007). (Pubitemid 46427875)
37. Yu, H. H. et al. Clonal development and organization of the adult Drosophila central brain. Curr. Biol. 23, 633-643 (2013).
38. Yu, J. Y., Kanai, M. I., Demir, E., Jefferis, G. S. & Dickson, B. J. Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr. Biol. 20, 1602-1614 (2010).
39. Ruta, V. et al. A dimorphic pheromone circuit in Drosophila from sensory input descending output. Nature 468, 686-690 (2010).
40. Jallon, J. M. A few chemical words exchanged by Drosophila during courtship and mating. Behav. Genet. 14, 441-478 (1984). (Pubitemid 15172211)
41. Kurtovic, A., Widmer, A. & Dickson, B. J. A single class of olfactory neurons mediates behavioural responses to Drosophila sex pheromone. Nature 446, 542-546 (2007). (Pubitemid 46514730)
42. Kondoh, Y., Kaneshiro, K. Y., Kimura, K. & Yamamoto, D. Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc. R. Soc. Lond. B 270, 1005-1013 (2003). (Pubitemid 36605634)
43. Datta, S. R. et al. The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452, 473-477 (2008). (Pubitemid 351450846)
44. Kimura, K., Hachiya, T., Koganezawa, M., Tazawa, T. & Yamamoto, D. Fruitless and Doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 59, 759-769 (2008).
45. Kohatsu, S., Koganezawa, M. & Yamamoto, D. Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 69, 498-508 (2011).
46. vonPhilipsborn, A. C. et al. Neuronal control of Drosophila courtship song. Neuron 69, 509-522 (2011).
47. Villella, A. et al. Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics 147, 1107-1130 (1997). (Pubitemid 27467454)
48. Pan, Y., Robinett, C. C. & Baker, B. S. Turning males on: activation of male courtship behavior in Drosophila melanogaster. PLoS ONE 6, e21144 (2011).
49. Pan, Y., Messner, G. W. & Baker, B. S. Joint control of Drosophila male courtship behavior by motion cues and activation of male-specific P1 neurons. Proc. Natl Acad. Sci. USA 109, 10065-10070 (2012).
50. Rubinstein, C. D., Rivlin, P. K. & Hoy, R. R. Genetic feminization of the thoracic nervous system disrupts courtship song in male Drosophila melanogaster. J. Neurogenet. 24, 234-245 (2010).
51. Clyne, J. D. & Miesenböck, G. Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133, 354-363 (2008). (Pubitemid 351508297)
52. Billeter, J. C., Atallah, J., Krupp, J. J., Millar, J. G. & Levine, J. D. Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461, 987-991 (2009).
53. Everaerts, C. Farine, J., Cobb, M. & Ferveur, J. Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PLoS ONE 5, e9607 (2010).
54. Yew, J. Y. et al. A new male sex pheromone and cuticular cues for chemical communication in Drosophila. Curr. Biol. 19, 1245-1254 (2009).
55. 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). (Pubitemid 29374699)
56. Butterworth, F. M. Lipids of Drosophila: a newly detected lipid in the male. Science 163, 1356-1357 (1969).
57. Wang, L. & Anderson, D. J. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463, 227-231 (2010).
58. Wang, L. et al. Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nature Neurosci. 14, 757-762 (2011).
59. Lacaille, F. et al. An inhibitory sex pheromone tastes bitter for Drosophila males. PLoS ONE 8, e661 (2007).
60. Thistle, R., Cameron, P., Ghorayshi, A., Dennison, L. & Scott, K. Contact chemoreceptors mediate male-male repulsion male-female attraction during Drosophila courtship. Cell 149, 1140-1151 (2012).
61. Lin, H., Mann, K. J., Starostina, E., Kinser, R. D. & Pikielny, C. W. A Drosophila DEG/ENaC channel subunit is required for male response to female pheromones. Proc. Natl Acad. Sci. USA 102, 12831-12836 (2005). (Pubitemid 41279451)
62. Liu, T., Starostina, E., Vijayan, V. & Pikielny, C. W. Two Drosophila DEG/ENaC channel subunits have distinct functions in gustatory that active male courtship. J. Neurosci. 32, 11879-11889 (2012).
63. Lu, B., LaMora, A., Sun, Y. & Welsh, M. J. & Ben-Shahar, Y. ppk23-dependent chemosensory functions contribute to courtship behavior in Drosophila melanogaster. PLoS Genet. 8, e1002587 (2012).
64. Starostina, E. et al. A Drosophila DEG/ENaC subunit functions specifically in gustatory neurons required for male courtship behavior. J. Neurosci. 32, 4665-4674 (2012).
65. Toda, H., Zhao, X. & Dickson, B. J. The Drosophila female aphrodisiac pheromone actives ppk23+ sensory neurons to elicit male courtship behavior. Cell Rep. 1, 599-607 (2012).
66. Mellert, D. J., Knapp, J., Manoli, D. S., Meissner, G. W. & Baker, B. S. Midline crossing by gustatory receptor neuron axons is regulated by fruitless, doublesex and Roundabout receptors. Development 137, 323-332 (2010).
67. Possidente, D. R. & Murphey, R. K. Genetic control of sexually dimorphic axon morphology in Drosophila sensory neurons. Dev. Biol. 132, 448-457 (1989). (Pubitemid 19107514)
68. Krstic, D., Boll, W. & Noll, M. Sensory integration regulating male courtship behavior in Drosophila. PLoS ONE 4, e4457 (2009).
69. Koganezawa, M., Haba, D., Matsuo, T. & Yamamoto, D. The shaping of male courtship posture by lateralized gustatory inputs to male-specific interneurons. Curr. Biol. 20, 1-8 (2010).
70. Hardelan, R. Lighting conditions and mating behavior in Drosophila. Am. Nat. 105, 198-200 (1971).
71. Fan, P. et al. Genetic and neural mechanisms that inhibit Drosophila from mating with other species. Cell 154, 89-102 (2013).
72. White, J. Q. & Jorgensen, E. M. Sensation in a single neuron pair represses male behavior in hermaphrodites. Neuron 75, 593-600 (2012).
73. Kimchi, T., Xu, J. & Dulac, C. A functional circuit underlying male sexual behavior in the female mouse brain. Nature 448, 1009-1014 (2007). (Pubitemid 47345587)
74. Robertson, D. R. Social control of sex reversal in a coral-reef fish. Science 77, 1007-1009 (1972).
75. Hardie, R. C. & Franze, K. Photomechanical responses in Drosophila photoreceptors. Science 338, 260-263 (2012).
76. Sato, K. et al. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452, 1002-1006 (2008). (Pubitemid 351589615)
77. Laughlin, J. D., Ha, T. S., Jones, D. N. & Smith, D. P. Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133, 1255-1265 (2008). (Pubitemid 351852909)
78. Benton, R., Vannice, K. S., Gomez-Diaz, C. & Vosshall, L. B. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136, 149-162(2009).
79. Grosjean, Y. et al. An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478, 236-240 (2011).
80. Sato, K., Tanaka, K. & Touhara, K. Sugar-regulated cation channel formed by an insect gustatory receptor. Proc. Natl Acad. Sci. USA 108, 11680-11685 (2011).
81. Moon, S. J., Lee, Y., Jiao, Y. & Montell, C. A. Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr. Biol. 19, 623-1627 (2009).
82. Miyamoto, T. & Amrein, H. Suppression of male courtship by a Drosophila pheromone receptor. Nature Neurosci. 11, 874-876 (2008).
83. Kim, S. E., Coste, B., Chadha, A., Cook, B. & Patapoutian, A. The role of Drosophila Piezo in mechanical nociception. Nature 483, 209-212 (2012).
84. Yan, Z. et al. Drosophila NOMPC is a mechanotransduction channel subunit for gentle-touch sensation. Nature 493, 221-225 (2013).
85. Effertz, T., Nadrowski, B., Piepenbrock, D., Albert, J. T. & Gopfert, M. C. Direct gating and mechanical integrity of Drosophila auditory transducers require TRPN1. Nature Neurosci. 15, 1198-1200 (2012).
86. Senthilan, P. R. et al. Drosophila auditory organ genes and genetic hearing defects. Cell 150, 1042-1054 (2012).
87. Berl, D. F., Duyk, G. M. & Perrimon, N. A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 94, 14837-14842 (1997). (Pubitemid 28041461)
88. Fabre, C. C. et al. Substrate-borne vibratory communication during courtship in Drosophila melanogaster. Curr. Biol. 22, 2180-2185 (2012).
89. Ewing, A. W. The neuromuscular basis of courtship song in Drosophila: the role of the direct and axillary wing muscles. J. Comp. Physiol. 130, 87-93 (1979).