Courtship behavior in Drosophila melanogaster: Towards a 'courtship connectome'

Current Opinion in Neurobiology

Volumn 23, Issue 1, 2013, Pages 76-83

  Pavlou, Hania J ^a   Goodwin, Stephen F ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DEGENERIN SODIUM CHANNEL; INSECT PROTEIN; PROTEIN DSX; PROTEIN FRU; RECOMBINASE; SEX PHEROMONE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ATTITUDE; BEHAVIOR CONTROL; BRAIN FUNCTION; BRAIN MAPPING; BRAIN REGION; CELL ACTIVATION; CELL COMPONENT; CELL COUNT; CELL FUNCTION; CELL STRUCTURE; CONNECTOME; COPULATION; COURTSHIP; DECISION MAKING; DROSOPHILA MELANOGASTER; EGG LAYING; INTERNEURON; MOTONEURON; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NERVE CONDUCTION; NERVE FUNCTION; NONHUMAN; OLFACTORY RECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRODUCTIVE SUCCESS; REVIEW; SENSILLUM; SENSORIMOTOR INTEGRATION; SENSORY NERVE CELL; SENSORY STIMULATION; SEX DIFFERENCE; SMELLING; SYNAPTIC TRANSMISSION; VENTRAL ROOT;

ANIMALS; BRAIN; CONNECTOME; COURTSHIP; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MALE; SEXUAL BEHAVIOR, ANIMAL;

EID: 84872860756     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2012.09.002     Document Type: Review

References (61)

1. Bullmore E., Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 2009, 10:186-198.
2. Dauwalder B. The roles of fruitless and doublesex in the control of male courtship. Int Rev Neurobiol 2011, 99:87-105.
3. Villella A., Hall J.C. Neurogenetics of courtship and mating in Drosophila. Adv Genet 2008, 62:67-184.
4. Connolly K., Cook R.M. Rejection responses by female Drosophila melanogaster: their ontogeny, causality and effects upon the behavior of the courting male. Behavior 1973, 44:142-167.
5. Spieth H.T., Ringo J.M. Mating behavior and sexual isolation in Drosophila. The Genetics and Biology of Drosophila 1983, vol 3c:223-284. Academic Press.
6. Ejima A., Nakayama S., Aigaki T. Phenotypic association of spontaneous ovulation and sexual receptivity in virgin females of Drosophila melanogaster mutants. Behav Genet 2001, 31:437-444.
7. Kubli E. Sex-peptides: seminal peptides of the Drosophila male. Cell Mol Life Sci 2003, 60:1689-1704.
8. Billeter J.-C., Rideout E.J., Dornan A.J., Goodwin S.F. Control of male sexual behavior in Drosophila by the sex determination pathway. Curr Biol 2006, 16:R766-R776.
9. Rideout E.J., Billeter J.-C., Goodwin S.F. The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr Biol 2007, 17:1473-1478.
10. 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 2008, 320:378-390.
11. Kimura K.-I., Hachiya T., Koganezawa M., Tazawa T., Yamamoto D. Fruitless and doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 2008, 59:759-769.
12. 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. Nat Neurosci 2010, 13:458-466.
13. Billeter J.-C., Goodwin S.F. Characterization of Drosophila fruitless-gal4 transgenes reveals expression in male-specific fruitless neurons and innervation of male reproductive structures. J Comp Neurol 2004, 475:270-287.
14. Manoli D.S., Foss M., Villella A., Taylor B.J., Hall J.C., Baker B.S. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 2005, 436:395-400.
15. Stockinger P., Kvitsiani D., Rotkopf S., Tirián L., Dickson B.J. Neural circuitry that governs Drosophila male courtship behavior. Cell 2005, 121:795-807.
16. Kimura K., Ote M., Tazawa T., Yamamoto D. Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Nature 2005, 438:229-233.
17. Mellert D.J., Knapp J.-M., Manoli D.S., Meissner G.W., Baker B.S. Midline crossing by gustatory receptor neuron axons is regulated by fruitless, doublesex and the Roundabout receptors. Development 2010, 137:323-332.
18. Cachero S., Ostrovsky A.D., Yu J.Y., Dickson B.J., Jefferis G.S.X.E. Sexual dimorphism in the fly brain. Curr Biol 2010, 20:1589-1601.
19. Yu J.Y., Kanai M.I., Demir E., Jefferis G.S.X.E., Dickson B.J. Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol 2010, 20:1602-1614.
20. Robinett C.C., Vaughan A.G., Knapp J.-M., Baker B.S. Sex and the single cell. II. There is a time and place for sex. PLoS Biol 2010, 8:e1000365.
21. Rezaval C., Pavlou H.J., Dornan A.J., Chan Y.B., Kravitz E.A., Goodwin S.F. Neural circuitry underlying Drosophila female postmating behavioral responses. Curr Biol 2012, 22:1155-1165.
22. Lee T., Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999, 22:451-461.
23. Liu W., Hou S.X. Genetic tools used for cell lineage tracing and gene manipulation in Drosophila germline stem cells. Methods Mol Biol 2008, 450:61-70.
24. Datta S.R., Vasconcelos M.L., Ruta V., Luo S., Wong A., Demir E., Flores J., Balonze K., Dickson B.J., Axel R. The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 2008, 452:473-477.
25. Ruta V., Datta S.R., Vasconcelos M.L., Freeland J., Looger L.L., Axel R. A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 2010, 468:686-690.
26. von Philipsborn A.C., Liu T., Yu J.Y., Masser C., Bidaye S.S., Dickson B.J. Neuronal control of Drosophila courtship song. Neuron 2011, 69:509-522.
27. Kondoh Y., Kaneshiro K.Y., Kimura K.-I., Yamamoto D. Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc Biol Sci 2003, 270:1005-1013.
28. Jefferis G.S., Potter C.J., Chan A.M., Marin E.C., Rohlfing T., Maurer C.R., Luo L. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 2007, 128:1187-1203.
29. Butterworth F.M. Lipids of Drosophila: a newly detected lipid in the male. Science 1969, 163:1356-1357.
30. Ha T.S., Smith D.P. A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J Neurosci 2006, 26:8727-8733.
31. Kurtovic A., Widmer A., Dickson B.J. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 2007, 446:542-546.
32. Wang L., Anderson D.J. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 2010, 463:227-231.
33. Ejima A., Smith B.P., Lucas C., van der Goes van Naters W., Miller C.J., Carlson J.R., Levine J.D., Griffith L.C. Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr Biol 2007, 17:599-605.
34. Grosjean Y., Rytz R., Farine J.P., Abuin L., Cortot J., Jefferis G.S., Benton R. An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 2011, 478:236-240.
35. Benton R., Vannice K.S., Gomez-Diaz C., Vosshall L.B. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 2009, 136:149-162.
36. Spieth H.T. Courtship behavior in Drosophila. Annu Rev Entomol 1974, 19:385-405.
37. Ferveur J.F., Cobb M. Behavioral and Evolutionary Roles of Cuticular Hydrocarbons in Drosophila 2010, Cambridge University Press, Cambridge. A.G. Bagnères, G.J. Blomquist (Eds.).
38. Watanabe K., Toba G., Koganezawa M., Yamamoto D. Gr39a, a highly diversified gustatory receptor in Drosophila, has a role in sexual behavior. Behav Genet 2011, 41:746-753.
39. Lacaille F., Hiroi M., Twele R., Inoshita T., Umemoto D., Manière G., Marion-Poll F., Ozaki M., Francke W., Cobb M., et al. An inhibitory sex pheromone tastes bitter for Drosophila males. PLoS ONE 2007, 2:e661.
40. Miyamoto T., Amrein H. Suppression of male courtship by a Drosophila pheromone receptor. Nat Neurosci 2008, 11:874-876.
41. 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 2009, 19:1623-1627.
42. Koganezawa M., Haba D., Matsuo T., Yamamoto D. The shaping of male courtship posture by lateralized gustatory inputs to male-specific interneurons. Curr Biol 2010, 20:1-8.
43. 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 2012, 8:e1002587.
44. Thistle R., Cameron P., Ghorayshi A., Dennison L., Scott K. Contact chemoreceptors mediate male-male repulsion and male-female attraction during Drosophila courtship. Cell 2012, 149:1140-1151.
45. Toda H., Zhao X., Dickson B.J. The Drosophila female aphrodisiac pheromone activates ppk23(+) sensory neurons to elicit male courtship behavior. Cell Rep 2012, 1:599-607.
46. Possidente D.R., Murphey R.K. Genetic control of sexually dimorphic axon morphology in Drosophila sensory neurons. Dev Biol 1989, 132:448-457.
47. 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 2005, 102:12831-12836.
48. Starostina E., Liu T., Vijayan V., Zheng Z., Siwicki K.K., Pikielny C.W. A Drosophila DEG/ENaC subunit functions specifically in gustatory neurons required for male courtship behavior. J Neurosci 2012, 32:4665-4674.
49. Häsemeyer M., Yapici N., Heberlein U., Dickson B.J. Sensory neurons in the Drosophila genital tract regulate female reproductive behavior. Neuron 2009, 61:511-518.
50. Yang C.-H., Rumpf S., Xiang Y., Gordon M.D., Song W., Jan L.Y., Jan Y.-N. Control of the postmating behavioral switch in Drosophila females by internal sensory neurons. Neuron 2009, 61:519-526.
51. Yapici N., Kim Y.-J., Ribeiro C., Dickson B.J. A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 2008, 451:33-37.
52. Clyne J.D., Miesenböck G. Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 2008, 133:354-363.
53. Kohatsu S., Koganezawa M., Yamamoto D. Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 2011, 69:498-508.
54. Pan Y., Meissner 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 2012, 109:10065-10070.
55. Bernstein J.G., Garrity P.A., Boyden E.S. Optogenetics and thermogenetics: technologies for controlling the activity of targeted cells within intact neural circuits. Curr Opin Neurobiol 2012, 22:61-71.
56. Yao Z., Macara A.M., Lelito K.R., Minosyan T.Y., Shafer O.T. Analysis of functional neuronal connectivity in the Drosophila brain. J Neurophysiol 2012, 108:684-696.
57. Olsen S.R., Wilson R.I. Cracking neural circuits in a tiny brain: new approaches for understanding the neural circuitry of Drosophila. Trends Neurosci 2008, 31:512-520.
58. van der Goes van Naters W., Carlson J.R. Receptors and neurons for fly odors in Drosophila. Curr Biol 2007, 17:606-612.
59. Vosshall L.B., Wong A.M., Axel R. An olfactory sensory map in the fly brain. Cell 2000, 102:147-159.
60. Rezaval C., Fabre C.C., Goodwin S.F. Invertebrate neuroethology: food play and sex. Curr Biol 2011, 21:R960-R962.
61. Benton R. Decision making: singin' in the brain. Neuron 2011, 69:399-401.