Functional dissection of the neural substrates for sexual behaviors in Drosophila melanogaster

Genetics

Volumn 189, Issue 1, 2011, Pages 195-211

  Meissner, Geoffrey W ^a,b   Manoli, Devanand S ^a,c   Chavez, Jose F ^a,d   Knapp, Jon Michael ^a,b   Lin, Tasha L ^a,e   Stevens, Robin J ^a,f   Mellert, David J ^a,b   Tran, David H ^b,g   Baker, Bruce S ^a,b  

^a STANFORD UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^g SAN JOSE STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRUITLESS PROTEIN; PROTEIN; TRANSCRIPTION FACTOR GAL4; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL GENETICS; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; COURTSHIP; DROSOPHILA MELANOGASTER; FEMALE; FEMALE FERTILITY; HABITUATION; MALE; MALE FERTILITY; NERVE CELL; NEUROBIOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEXUAL BEHAVIOR;

ANIMALS; CHOLINERGIC NEURONS; COURTSHIP; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; FERTILITY; GENE EXPRESSION REGULATION; HIGH-THROUGHPUT SCREENING ASSAYS; MALE; NERVE TISSUE PROTEINS; PHENOTYPE; SEXUAL BEHAVIOR, ANIMAL; TRANSCRIPTION FACTORS;

DROSOPHILA MELANOGASTER;

EID: 80052667067     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.111.129940     Document Type: Article

References (87)

1. Acebes, A., M. Cobb, and J.-F. Ferveur, 2003 Species-specific effects of single sensillum ablation on mating position in Drosophila. J. Exp. Biol. 206: 3095-3100.
2. Acebes, A., Y. Grosjean, C. Everaerts, and J.-F. Ferveur, 2004 Cholinergic control of synchronized seminal emissions in Drosophila. Curr. Biol. 14: 704-710.
3. Anand, A., A. Villella, L. C. Ryner, T. Carlo, S. F. Goodwin et al., 2001 Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics 158: 1569-1595.
4. Baker, B. S., B. J. Taylor, and J. C. Hall, 2001 Are complex behaviors specified by dedicated regulatory genes? Reasoning from Drosophila. Cell 105: 13-24.
5. Barolo, S., L. A. Carver, and J. W. Posakony, 2000 GFP and betagalactosidase transformation vectors for promoter/enhancer analysis in Drosophila. Biotechniques 29: 726, 728, 730, 732.
6. Barolo, S., B. Castro, and J. W. Posakony, 2004 New Drosophila transgenic reporters: insulated P-element vectors expressing fast-maturing RFP. Biotechniques 36: 436-440, 442.
7. Bray, S., and H. Amrein, 2003 A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39: 1019-1029.
8. Broughton, S. J., T. Kitamoto, and R. J. Greenspan, 2004 Excitatory and inhibitory switches for courtship in the brain of Drosophila melanogaster. Curr. Biol. 14: 538-547.
9. Cachero, S., A. D. Ostrovsky, J. Y. Yu, B. J. Dickson, and G. S. X. E. Jefferis, 2010 Sexual dimorphism in the fly brain. Curr. Biol. 20: 1589-1601.
10. Chan, Y.-B., and E. A. Kravitz, 2007 Specific subgroups of fruM neurons control sexually dimorphic patterns of aggression in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 104: 19577-19582.
11. Chen, S., A. Y. Lee, N. M. Bowens, R. Huber, and E. A. Kravitz, 2002 Fighting fruit flies: a model system for the study of aggression. Proc. Natl. Acad. Sci. USA 99: 5664-5668.
12. Clyne, J. D., and G. Miesenböck, 2008 Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133: 354-363.
13. Collett, T. S., and M. F. Land, 1975 Visual control of flight behaviour in the hoverfly, Syritta pipiens L. J. Comp. Physiol. A 99: 1-66.
14. Couto, A., M. Alenius, and B. J. Dickson, 2005 Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15: 1535-1547.
15. Datta, S. R., M. L. Vasconcelos, V. Ruta, S. Luo, A. Wong et al., 2008 The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452: 473-477.
16. Demir, E., and B. J. Dickson, 2005 Fruitless splicing specifies male courtship behavior in Drosophila. Cell 121: 785-794.
17. Dickson, B. J., 2008 Wired for sex: the neurobiology of Drosophila mating decisions. Science 322: 904-909.
18. Ejima, A., B. P. C. Smith, C. Lucas, J. D. Levine, and L. C. Griffith, 2005 Sequential learning of pheromonal cues modulates memory consolidation in trainer-specific associative courtship conditioning. Curr. Biol. 15: 194-206.
19. Ferveur, J. F., and R. J. Greenspan, 1998 Courtship behavior of brain mosaics in Drosophila. J. Neurogenet. 12: 205-226.
20. Ferveur, J. F., K. F. Störtkuhl, R. F. Stocker, and R. J. Greenspan, 1995 Genetic feminization of brain structures and changed sexual orientation in male Drosophila. Science 267: 902-905.
21. Fisher, S. E., and C. Scharff, 2009 FOXP2 as a molecular window into speech and language. Trends Genet. 25: 166-177.
22. Fishilevich, E., and L. B. Vosshall, 2005 Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15: 1548-1553.
23. Gailey, D. A., F. R. Jackson, and R. W. Siegel, 1982 Male courtship in Drosophila: the conditioned response to immature males and its genetic control. Genetics 102: 771-782.
24. Gailey, D. A., R. C. Lacaillade, and J. C. Hall, 1986 Chemosensory elements of courtship in normal and mutant, olfaction-deficient Drosophila melanogaster. Behav. Genet. 16: 375-405.
25. Goodwin, S. F., B. J. Taylor, A. Villella, M. Foss, L. C. Ryner et al., 2000 Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics 154: 725-745.
26. Greenspan, R. J., and J. F. Ferveur, 2000 Courtship in Drosophila. Annu. Rev. Genet. 34: 205-232.
27. Griffith, L. C., and A. Ejima, 2009 Courtship learning in Drosophila melanogaster: diverse plasticity of a reproductive behavior. Learn. Mem. 16: 743-750.
28. Hall, J. C., 1977 Portions of the central nervous system controlling reproductive behavior in Drosophila melanogaster. Behav. Genet. 7: 291-312.
29. Hall, J. C., 1978 Courtship among males due to a male-sterile mutation in Drosophila melanogaster. Behav. Genet. 8: 125-141.
30. Hall, J. C., 1979 Control of male reproductive behavior by the central nervous system of Drosophila: dissection of a courtship pathway by genetic mosaics. Genetics 92: 437-457.
31. Hall, J. C., 1994 The mating of a fly. Science 264: 1702-1714.
32. Häsemeyer, M., N. Yapici, U. Heberlein, and B. J. Dickson, 2009 Sensory neurons in the Drosophila genital tract regulate female reproductive behavior. Neuron 61: 511-518.
33. Heinrichs, V., L. C. Ryner, and B. S. Baker, 1998 Regulation of sexspecific selection of fruitless 59 splice sites by transformer and transformer-2. Mol. Cell. Biol. 18: 450-458.
34. Hotta, Y., and S. Benzer, 1972 Mapping of behaviour in Drosophila mosaics. Nature 240: 527-535.
35. Ito, H., K. Fujitani, K. Usui, K. Shimizu-Nishikawa, S. Tanaka et al., 1996 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.
36. Juntti, S. A., J. K. Coats, and N. M. Shah, 2008 A genetic approach to dissect sexually dimorphic behaviors. Horm. Behav. 53: 627-637.
37. Juntti, S. A., J. Tollkuhn, M. V. Wu, E. J. Fraser, T. Soderborg et al., 2010 The androgen receptor governs the execution, but not programming, of male sexual and territorial behaviors. Neuron 66: 260-272.
38. Kankel, D. R., and J. C. Hall, 1976 Fate mapping of nervous system and other internal tissues in genetic mosaics of Drosophila melanogaster. Dev. Biol. 48: 1-24.
39. Kimchi, T., J. Xu, and C. Dulac, 2007 A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 448: 1009-1014.
40. Kimura, K.-I., T. Hachiya, M. Koganezawa, T. Tazawa, and D. Yamamoto, 2008 Fruitless and doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 59: 759-769.
41. Kimura, K.-I., M. Ote, T. Tazawa, and D. Yamamoto, 2005 Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Nature 438: 229-233.
42. Kitamoto, T., 2001 Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol. 47: 81-92.
43. Koganezawa, M., D. Haba, T. Matsuo, and D. Yamamoto, 2010 The shaping of male courtship posture by lateralized gustatory inputs to male-specific interneurons. Curr. Biol. 20: 1-8.
44. Kohatsu, S., M. Koganezawa, and D. Yamamoto, 2011 Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 69: 498-508.
45. Kowalski, S., T. Aubin, and J. R. Martin, 2004 Courtship song in Drosophila melanogaster: a differential effect on male-female locomotor activity. Can. J. Zool. 82: 1258-1266.
46. Krstic, D., W. Boll, and M. Noll, 2009 Sensory integration regulating male courtship behavior in Drosophila. PLoS One 4: e4457.
47. Kurtovic, A., A. Widmer, and B. J. Dickson, 2007 A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446: 542-546.
48. Kvitsiani, D., and B. J. Dickson, 2006 Shared neural circuitry for female and male sexual behaviours in Drosophila. Curr. Biol. 16: R355-R356.
49. Lacaille, F., C. Everaerts, and J.-F. Ferveur, 2009 Feminization and alteration of Drosophila taste neurons induce reciprocal effects on male avoidance behavior. Behav. Genet. 39: 554-563.
50. Lacaille, F., M. Hiroi, R. Twele, T. Inoshita, D. Umemoto et al., 2007 An inhibitory sex pheromone tastes bitter for Drosophila males. PLoS One 2: e661.
51. Lai, S.-L., and T. Lee, 2006 Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 9: 703-709.
52. Lee, G., M. Foss, S. F. Goodwin, T. Carlo, B. J. Taylor et al., 2000 Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. J. Neurobiol. 43: 404-426.
53. Lee, G., and J. C. Hall, 2001 Abnormalities of male-specific FRU protein and serotonin expression in the CNS of fruitless mutants in Drosophila. J. Neurosci. 21: 513-526.
54. Lee, G., A. Villella, B. J. Taylor, and J. C. Hall, 2001 New reproductive anomalies in fruitless-mutant Drosophila males: extreme lengthening of mating durations and infertility correlated with defective serotonergic innervation of reproductive organs. J. Neurobiol. 47: 121-149.
55. Luan, H., N. C. Peabody, C. R. Vinson, and B. H. White, 2006 Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 52: 425-436.
56. Luo, L., E. M. Callaway, and K. Svoboda, 2008 Genetic dissection of neural circuits. Neuron 57: 634-660.
57. Manoli, D. S., and B. S. Baker, 2004 Median bundle neurons coordinate behaviours during Drosophila male courtship. Nature 430: 564-569.
58. Manoli, D. S., M. Foss, A. Villella, B. J. Taylor, J. C. Hall et al., 2005 Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436: 395-400.
59. Manoli, D. S., G. W. Meissner, and B. S. Baker, 2006 Blueprints for behavior: genetic specification of neural circuitry for innate behaviors. Trends Neurosci. 29: 444-451.
60. Mellert, D. J., J.-M. Knapp, D. S. Manoli, G. W. Meissner, and B. S. Baker, 2010 Midline crossing by gustatory receptor neuron axons is regulated by fruitless, doublesex and the Roundabout receptors. Development 137: 323-332.
61. Miyamoto, T., and H. Amrein, 2008 Suppression of male courtship by a Drosophila pheromone receptor. Nat. Neurosci. 11: 874-876.
62. Moon, S. J., Y. Lee, Y. Jiao, and C. Montell, 2009 A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr. Biol. 19: 1623-1627.
63. Nilsen, S. P., Y.-B. Chan, R. Huber, and E. A. Kravitz, 2004 Genderselective patterns of aggressive behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 101: 12342-12347.
64. O'Dell, K. M., J. D. Armstrong, M. Y. Yang, and K. Kaiser, 1995 Functional dissection of the Drosophila mushroom bodies by selective feminization of genetically defined subcompartments. Neuron 15: 55-61.
65. Pan, Y., C. C. Robinett, and B. S. Baker, 2011 Turning males on: activation of male courtship behavior in Drosophila melanogaster. PLoS ONE 6: e21144.
66. Portman, D. S., 2007 Genetic control of sex differences in C. elegans neurobiology and behavior. Adv. Genet. 59: 1-37.
67. Rideout, E. J., J.-C. Billeter, and S. F. Goodwin, 2007 The sexdetermination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr. Biol. 17: 1473-1478.
68. Rideout, E. J., A. J. Dornan, M. C. Neville, S. Eadie, and S. F. Goodwin, 2010 Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat. Neurosci. 13: 458-466.
69. Robinett, C. C., A. G. Vaughan, J.-M. Knapp, and B. S. Baker, 2010 Sex and the single cell. II. There is a time and place for sex. PLoS Biol. 8: e1000365.
70. Robinson, G. E., R. D. Fernald, and D. F. Clayton, 2008 Genes and social behavior. Science 322: 896-900.
71. Ryner, L. C., S. F. Goodwin, D. H. Castrillon, A. Anand, A. Villella et al., 1996 Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87: 1079-1089.
72. Salvaterra, P. M., and T. Kitamoto, 2001 Drosophila cholinergic neurons and processes visualized with Gal4/UAS-GFP. Gene Exp. Patterns 1: 73-82.
73. Sanders, L. E., and M. N. Arbeitman, 2008 Doublesex establishes sexual dimorphism in the Drosophila central nervous system in an isoform-dependent manner by directing cell number. Dev. Biol. 320: 378-390.
74. Siwicki, K. K., and E. A. Kravitz, 2009 Fruitless, doublesex and the genetics of social behavior in Drosophila melanogaster. Curr. Opin. Neurobiol. 19: 200-206.
75. Spieth, H. T., 1974 Courtship behavior in Drosophila. Annu. Rev. Entomol. 19: 385-405.
76. Stockinger, P., D. Kvitsiani, S. Rotkopf, L. Tirián, and B. J. Dickson, 2005 Neural circuitry that governs Drosophila male courtship behavior. Cell 121: 795-807.
77. Sturtevant, A., 1915 Experiments on sex recognition and the problem of sexual selection in Drosophila. J. Anim. Behav. 5: 351-366.
78. Usui-Aoki, K., H. Ito, K. Ui-Tei, K. Takahashi, T. Lukacsovich et al., 2000 Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat. Cell Biol. 2: 500-506.
79. Villella, A., D. A. Gailey, B. Berwald, S. Ohshima, P. T. Barnes et al., 1997 Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics 147: 1107-1130.
80. Villella, A., and J. C. Hall, 2008 Neurogenetics of courtship and mating in Drosophila. Adv. Genet. 62: 67-184.
81. von Philipsborn, A. C., T. Liu, J. Y. Yu, C. Masser, S. S. Bidaye et al., 2011 Neuronal control of Drosophila courtship song. Neuron 69: 509-522.
82. Vrontou, E., S. P. Nilsen, E. Demir, E. A. Kravitz, and B. J. Dickson, 2006 Fruitless regulates aggression and dominance in Drosophila. Nat. Neurosci. 9: 1469-1471.
83. Wu, M. V., D. S. Manoli, E. J. Fraser, J. K. Coats, J. Tollkuhn et al., 2009 Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 139: 61-72.
84. Yamamoto, D., 2008 Brain sex differences and function of the fruitless gene in Drosophila. J. Neurogenet. 22: 309-322.
85. Yang, C.-H., S. Rumpf, Y. Xiang, M. D. Gordon, W. Song et al., 2009 Control of the postmating behavioral switch in Drosophila females by internal sensory neurons. Neuron 61: 519-526.
86. Yapici, N., Y.-J. Kim, C. Ribeiro, and B. J. Dickson, 2008 A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451: 33-37.
87. Yu, J. Y., M. I. Kanai, E. Demir, G. S. X. E. Jefferis, and B. J. Dickson, 2010 Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr. Biol. 20: 1602-1614.