Skip to main content
SpringerLink
Log in

Neuroethology of male courtship in Drosophila: from the gene to behavior

  • Review
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Neurogenetic analyses in the fruit fly Drosophila melanogaster revealed that gendered behaviors, including courtship, are underpinned by sexually dimorphic neural circuitries, whose development is directed in a sex-specific manner by transcription factor genes, fruitless (fru) and doublesex (dsx), two core members composing the sex-determination cascade. Via chromatin modification the Fru proteins translated specifically in the male nervous system lead the fru-expressing neurons to take on the male fate, as manifested by their male-specific survival or male-specific neurite formations. One such male-specific neuron group, P1, was shown to be activated when the male taps the female abdomen. Moreover, when artificially activated, P1 neurons are sufficient to induce the entire repertoire of the male courtship ritual. These studies provide a conceptual framework for understanding how the genetic code for innate behavior can be embodied in the neuronal substrate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

7-T:

7-Tricosene

7,11-HD:

7,11-Heptacosadiene

bon :

bonus

cVA:

cis-Vaccenyl acetate

DEG/ENaC:

Degenerin/epithelial sodium channels

dsx :

doublesex

dTrpA1:

Drosophila transient receptor potential cation channel subfamily A1

EcR:

Ecdysone receptor

EPSPs:

Excitatory postsynaptic potentials

fru :

fruitless

Gr:

Gustatory receptor

HDAC1:

Histone deacetylase 1

HP1:

Heterochromatin protein 1

IR84a:

Ionotropic receptor 84a

mAL:

Medially located just above the antennal lobe

Or67d:

Olfactory receptor 67d

P2X2:

ATP-activated P2X purinoceptor 2

ppk :

pickpocket

SOG:

Suboesophageal ganglion

TIF1:

Transcription intermediary factor 1

TNT:

Tetanus toxin light chain

tra :

transformer

References

  • Anand A, Villella A, Ryner LC, Carlo T, Goodwin SF, Song HJ, Gailey DA, Morales A, Hall C, Baker BS, Taylor BJ (2001) Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics 158:1569–1595

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bastock M, Manning A (1955) The courtship of Drosophila melanogaster. Behaviour 8:85–111

    Google Scholar 

  • Bennet-Clark HC, Ewing AW (1968) The wing mechanism involved in the courtship of Drosophila. J Exp Biol 49:117–128

    Google Scholar 

  • Billeter JC, Villella A, Allendorfer JB, Dornan AJ, Richardson M, Gailey DA, Goodwin SF (2006) Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene. Curr Biol 16:1063–1076

    CAS  PubMed  Google Scholar 

  • Billeter JC, Atallah J, Krupp JJ, Millar JG, Levine JD (2009) Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461:987–991

    CAS  PubMed  Google Scholar 

  • Bocklandt S, Vilain E (2007) Sex differences in brain and behavior: hormones versus genes. Adv Genet 59:245–266

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Butterworth FM (1969) Lipids of Drosophila: a newly detected lipid in the male. Science 163:1356–1357

    CAS  PubMed  Google Scholar 

  • Cashero S, Ostrovsky AD, Yu JY, Dickson BJ, Jefferis GS (2010) Sexual dimorphism in the fly brain. Curr Biol 20:1589–1601

    Google Scholar 

  • Chiang AS, Lin CY, Chuang CC, Chang HM, Hsieh CH, Yeh CW, Shih CT, Wu JJ, Wang GT, Chen YC, Wu CC, Chen GY, Ching YT, Lee PC, Lin CY, Lin HH, Wu CC, Hsu HW, Huang YA, Chen JY, Chiang HJ, Lu CF, Ni RF, Yeh CY, Hwang JK (2011) Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr Biol 21:1–11

    CAS  PubMed  Google Scholar 

  • Clyne JD, Miesenböck G (2008) Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133:354–363

    CAS  PubMed  Google Scholar 

  • Currie DA, Bate M (1995) Innervation is essential for the development and differentiation of a sex-specific adult muscle in Drosophila melanogaster. Development 121:2549–2557

    CAS  PubMed  Google Scholar 

  • Dalton JE, Lebo MS, Sanders LE, Sun F, Arbeitman MN (2009) Ecdysone receptor acts in fruitless-expressing neurons to mediate Drosophila courtship behaviors. Curr Biol 19:1447–1452

    CAS  PubMed Central  PubMed  Google Scholar 

  • Datta SR, Vasconcelos ML, Ruta V, Luo S, Wong A, Demir E, Flores J, Balonze K, Dickson BJ, Axel R (2008) The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452:473–477

    CAS  PubMed  Google Scholar 

  • Demir E, Dickson BJ (2005) fruitless splicing specifies male courtship behavior in Drosophila. Cell 121:785–794

    CAS  PubMed  Google Scholar 

  • Eberl DF, Duyk GM, Perrimon NA (1997) Genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. Proc Natl Acad Sci USA 94:14837–14842

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ejima A, Griffith LC (2008) Courtship initiation is stimulated by acoustic signals in Drosophila melanogaster. PLoS ONE 3:e3246

    PubMed Central  PubMed  Google Scholar 

  • Everaerts C, Farine J, Cobb M, Ferveur J (2010) Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PLoS ONE 5:e9607

    PubMed Central  PubMed  Google Scholar 

  • Ewing A (1978) The antenna of Drosophila as a ‘love song’ receptor. Physiol Entomol 3:33–36

    Google Scholar 

  • Fen P, Manoli DS, Ahmed OM, Chen Y, Agarwal N, Kwong S, Cai AG, Neitz J, Rsnsio A, Baker BS, Shah NM (2013) Genetic and neural mechanisms that inhibit Drosophila from mating with other species. Cell 154:89–102

    Google Scholar 

  • Gailey DA, Hall JC (1989) Behavior and cytogenetics of fruitless in Drosophila melanogaster: different courtship defects caused by separate, closely linked lesions. Genetics 121:773–785

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gailey DA, Taylor BJ, Hall JC (1991) Elements of the fruitless locus regulate development of the muscle of Lawrence, a male-specific structure in the abdomen of Drosophila melanogaster adults. Development 113:879–890

    CAS  PubMed  Google Scholar 

  • Gaj T, Gersbach CA, Barbas CF 3rd (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405

    CAS  PubMed  Google Scholar 

  • Gill KS (1963) A mutation causing abnormal courtship and mating behavior in males of Drosophila melanogaster. Am Zool 3:507

    Google Scholar 

  • Goodwin SF, Taylor BJ, Villella A, Foss M, Ryner LC, Baker BS, Hall JC (2000) Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics 154:725–745

    CAS  PubMed Central  PubMed  Google Scholar 

  • Goto J, Mikawa Y, Koganezawa M, Ito H, Yamamoto D (2011) Sexually dimorphic shaping of interneuron dendrites involves the Hunchback transcription factor. J Neurosci 31:5454–5459

    CAS  PubMed  Google Scholar 

  • Greenspan RJ, Ferveur J (2000) Courtship in Drosophila. Annu Rev Genet 34:205–232

    CAS  PubMed  Google Scholar 

  • Grosjean Y, Rytz R, Farine JP, Abuin L, Cortot J, Jefferis GS, Benton R (2011) An olfactory receptor for food-derived odors promotes male courtship in Drosophila. Nature 478:236–240

    CAS  PubMed  Google Scholar 

  • Hall JC (1977) Portions of the central nervous system controlling reproductive behavior in Drosophila melanogaster. Behav Genet 7:291–312

    CAS  PubMed  Google Scholar 

  • Hall JC (1982) Genetics of the nervous system in Drosophila. Q Rev Biophys 15:223–479

    CAS  PubMed  Google Scholar 

  • Heinrichs V, Ryner LC, Baker BS (1998) Regulation of sex-specific selection of fruitless 5′ splice sites by transformer and transformer-2. Mol Cell Biol 18:450–458

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hildebrand JG (1996) Olfactory control of behavior in moths: central processing of odor information and the functional significance of olfactory glomeruli. J Comp Physiol A 178:5–19

    CAS  PubMed  Google Scholar 

  • Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yamamoto D (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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ito H, Sato K, Koganezawa M, Ote M, Matsumoto K, Hama C, Yamamoto D (2012) Fruitless recruits two antagonistic chromatin factors to establish single-neuron sexual dimorphism. Cell 149:1327–1338

    CAS  PubMed  Google Scholar 

  • Jallon JM (1984) A few chemical words exchanged by Drosophila during courtship and mating. Behav Genet 14:441–478

    CAS  PubMed  Google Scholar 

  • Jefferis GS, Potter CJ, Chan AM, Marin EC, Rohlfing T, Maurer CR Jr, Luo L (2007) Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128:1187–1203

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kamikouchi A, Inagaki HK, Effertz T, Hendrich O, Fiala A, Gopfert MC, Ito K (2009) The neural basis of Drosophila gravity-sensing and hearing. Nature 458:165–171

    CAS  PubMed  Google Scholar 

  • Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, Ernst J, Sabo PJ, Larschan E, Gorchakov AA, Gu T, Linder-Basso D, Plachetka A, Shanower G, Tolstorukov MY, Luquette LJ, Xi R, Jung YL, Park RW, Bishop EP, Canfield TK, Sandstrom R, Thurman RE, MacAlpine DM, Stamatoyannopoulos JA, Kellis M, Elgin SC, Kuroda MI, Pirrotta V, Karpen GH, Park PJ (2010) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471(7339):480–485

    PubMed Central  PubMed  Google Scholar 

  • Kim WJ, Jan LY, Jan YN (2012) Contribution of visual and circadian neural circuits to memory for prolonged mating induced by rivals. Nat Neurosci 15:876–883

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kimura K (2011) Role of cell death in the formation of sexual dimorphism in the Drosophila central nervous system. Develop Growth Differ 53:236–244

    Google Scholar 

  • Kimura K, Ote M, Tazawa T, Yamamoto D (2005) Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Nature 438:229–233

    CAS  PubMed  Google Scholar 

  • Kimura K, Hachiya T, Koganezawa M, Tazawa T, Yamamoto D (2008) Fruitless and Doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 59:759–769

    CAS  PubMed  Google Scholar 

  • Koganezawa M, Haba D, Matsuo T, Yamamoto D (2010) The shaping of male courtship posture by lateralized gustatory inputs to male-specific interneurons. Curr Biol 20:1–8

    CAS  PubMed  Google Scholar 

  • Kohatsu S, Koganezawa M, Yamamoto D (2011) Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 69:498–508

    CAS  PubMed  Google Scholar 

  • Kohl J, Ostrovsky AD, Frechter S, Jefferis GSXE (2013) A bidirectional circuit switch reroutes pheromone signals in male and female brains. Cell 155:1610–1623

    Google Scholar 

  • Kondoh Y, Kaneshiro KY, Kimura K, Yamamoto D (2003) Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc R Soc Lond B 270:1005–1013

    Google Scholar 

  • Krstic D, Boll W, Noll M (2009) Sensory integration regulating male courtship behavior in Drosophila. PLoS ONE 4:e4457

    PubMed Central  PubMed  Google Scholar 

  • Kurtovic A, Widmer A, Dickson BJ (2007) A single class of olfactory neurons mediates behavioral responses to Drosophila sex pheromone. Nature 446:542–546

    CAS  PubMed  Google Scholar 

  • Lacaille F, Hiroi M, Twele R, Inoshita T, Umemoto D, Maniere G, Marion-Poll F, Ozaki M, Francke W, Cobb M, Everaerts C, Tanimura T, Ferveur JF (2007) An inhibitory sex pheromone tastes bitter for Drosophila males. PLoS ONE 8:e661

    Google Scholar 

  • Lam BJ, Bakshi A, Ekinci FY, Webb J, Graveley BR, Hertel KJ (2003) Enhancer-dependent 5′-splice site control of fruitless pre-mRNA splicing. J Biol Chem 278:22740–22747

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lawrence PA, Johnson P (1984) The genetic specification of pattern in a Drosophila muscle. Cell 36:775–782

    CAS  PubMed  Google Scholar 

  • Lawrence PA, Johnson P (1986) The muscle pattern of a segment of Drosophila may be determined by neurons and not by contribution myoblasts. Cell 45:505–513

    CAS  PubMed  Google Scholar 

  • Lee T, Luo L (1999) Mosaic analysis with a repressible neurotechnique cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:45–461

    Google Scholar 

  • Lee G, Foss M, Goodwin SF, Carlo T, Taylor BJ, Hall JC (2000) Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. J Neurobiol 15:404–426

    Google Scholar 

  • Lee G, Hall JC, Park JH (2002) doublesex gene expression in the central nervous system of Drosophila melanogaster. J Neurogenet 16:229–248

    CAS  PubMed  Google Scholar 

  • Lin H, Mann KJ, Starostina E, Kinser RD, Pikilny CW (2005) A Drosophila DEG/ENaC channel subunit is required for male response to female pheromones. Proc Natl Acad Sci USA 102:12831–12836

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu L, Ni JQ, Shi YD, Oakeley EJ, Sun FL (2005) Sex-specific role of Drosophila melanogaster HP1 regulating chromatin structure and gene transcription. Nat Genet 37:1361–1366

    CAS  PubMed  Google Scholar 

  • Liu T, Starostina E, Vijayan V, Pikielny CW (2012) Two Drosophila DEG/ENaC channel subunits have distinct functions in gustatory that active male courtship. J Neurosci 32:11879–11889

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lu B, LaMora A, Sun Y, Welsh MJ, Ben-Shahar Y (2012) ppk23-Dependent chemosensory functions contribute to courtship behavior in Drosophila melanogaster. PLoS Genet 8:e1002587

    CAS  PubMed Central  PubMed  Google Scholar 

  • Luo L, Callaway EM, Svoboda K (2008) Genetic dissection of neural circuits. Neuron 57:634–660

    CAS  PubMed Central  PubMed  Google Scholar 

  • Manoli DS, Foss M, Villella A, Taylor BJ, Hall JC, Baker BS (2005) Male-specific fruitless specifies the neural substrates of Drosophila courtship behavior. Nature 436:395–400

    CAS  PubMed  Google Scholar 

  • Mellert DJ, Knapp J, Manoli DS, Meissner GW, Baker BS (2010) Midline crossing by gustatory receptor neuron axons is regulated by Fruitless, Doublesex and Roundabout receptors. Development 137:323–332

    CAS  PubMed Central  PubMed  Google Scholar 

  • Miyamoto T, Amrein H (2008) Suppression of male courtship by a Drosophila pheromone receptor. Nat Neurosci 11:874–876

    CAS  PubMed  Google Scholar 

  • Moon SJ, Lee Y, Jiao Y, Montell CA (2009) Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr Biol 19:1623–1627

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nagoshi RN, McKeown M, Burtis KC, Belote JM, Baker BS (1988) The control of alternative splicing at genes regulating sexual differentiation in D. melanogaster. Cell 53:229–236

    CAS  PubMed  Google Scholar 

  • Nielsen AL, Ortiz JA, You J, Oulad-Abdelghani M, Khechumian R, Gansmuller A, Chambon P, Losson R (1999) Interaction with members of the heterochromatin protein 1 (HP1) family and histone deacetylation are differentially involved in transcriptional silencing by members of the TLF1 family. EMBO J 18:6385–6395

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nojima T, Kimura K, Koganezawa M, Yamamoto D (2010) Neuronal synaptic outputs determine the sexual fate of postsynaptic targets. Curr Biol 20:836–840

    CAS  PubMed  Google Scholar 

  • Pan Y, Robinett CC, Baker BS (2011) Turning males on: activation of male courtship behavior in Drosophila melanogaster. PLoS ONE 6:e21144

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pan Y, Messner GW, Baker BS (2012) 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Piacentini L, Fanti L, Berloco M, Perrini B, Pimpinelli S (2003) Heterochromatin protein (HP1) is associated with induced gene expression in Drosophila euchromatin. J Cell Biol 161:707–714

    CAS  PubMed Central  PubMed  Google Scholar 

  • Possidente DR, Murphey RK (1989) Genetic control of sexually dimorphic axon morphology in Drosophila sensory neurons. Dev Biol 132:448–457

    CAS  PubMed  Google Scholar 

  • Rideout EJ, Billeter J, Goodwin SF (2007) The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr Biol 17:1473–1478

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rideout EJ, Dornan AJ, Neville MC, Eadie S, Goodwin SF (2010) Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat Neurosci 13:458–466

    CAS  PubMed Central  PubMed  Google Scholar 

  • Robinett CC, Vaughan AG, Knapp J, Baker BS (2010) Sex and the single cell. II. There is a time and place for sex. PLoS ONE 8:e1000365

    Google Scholar 

  • Rubinstein CD, Rivlin PK, Hoy RR (2010) Genetic feminization of the thoracic nervous system disrupts courtship song in male Drosophila melanogaster. J Neurogenet 24:234–245

    CAS  PubMed  Google Scholar 

  • Ruta V, Datta SR, Vasconcelos ML, Freeland J, Looger LL, Axel R (2010) A dimorphic pheromone circuit in Drosophila from sensory input descending output. Nature 468:686–690

    CAS  PubMed  Google Scholar 

  • Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Taylor BJ, Wasserman SA (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87:1079–1089

    CAS  PubMed  Google Scholar 

  • Sakai T, Isono K, Tomaru M, Oguma Y (1997) Light-affected male following behavior is involved in light-dependent mating in Drosophila melanogaster. Genes Genet Syst 72:275–281

    Google Scholar 

  • Salz HK (2011) Sex determination in insects: a binary decision based on alternative splicing. Curr Opin Genet Dev 21:395–400

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sanders LE, Arbeitman MN (2008) Doublesex establishes sexual dimorphism in the Drosophila central nervous system in an isoform-dependent manner by directing cell number. Dev Biol 132:448–457

    Google Scholar 

  • Schreiber SL, Bernstein BE (2002) Signaling network model of chromatin. Cell 111:771–778

    CAS  PubMed  Google Scholar 

  • Sekido R, Lovell-Badge R (2009) Sex determination and SRY: down to a wink and a nudge? Trends Genet 25:19–29

    CAS  PubMed  Google Scholar 

  • Shirangi TR, Taylor BJ, McKeown M (2006) A double-switch system regulates male courtship behavior in male and female Drosophila melanogaster. Nat Genet 38:1435–1439

    CAS  PubMed  Google Scholar 

  • Song HJ, Billeter JC, Reynaud E, Carlo T, Spana EP, Perrimon N, Goodwin SF, Baker BS, Taylor BJ (2002) The fruitless gene is required for the proper formation of axonal tracts in the embryonic central nervous system of Drosophila. Genetics 162:1703–1724

    CAS  PubMed Central  PubMed  Google Scholar 

  • Starostina E, Liu T, Vijayan V, Zheng Z, Siwicki KK, Pikielny CW (2012) A Drosophila DEG/ENaC subunit functions specifically in gustatory neurons required for male courtship behavior. J Neurosci 32:4665–4674

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stockinger P, Kvitsiani D, Rotkopf S, Tirián L, Dickson BJ (2005) Neural circuitry that governs Drosophila male courtship behavior. Cell 121:795–807

    CAS  PubMed  Google Scholar 

  • Taylor BJ (1992) Differentiation of a male-specific muscle in Drosophila melanogaster does not require the sex-determining genes doublesex or intersex. Genetics 132:179–191

    CAS  PubMed Central  PubMed  Google Scholar 

  • Taylor BJ, Knittel LM (1995) Sex-specific differentiation of a male-specific abdominal muscle, the Muscle of Lawrence, is abnormal in hydroxyurea-treated and in fruitless male flies. Development 121:3079–3088

    CAS  PubMed  Google Scholar 

  • Taylor BJ, Villella A, Ryner LC, Baker BS, Hall JC (1994) Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev Genet 15:275–296

    CAS  PubMed  Google Scholar 

  • The modENCODE Consortium (2010) Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330:1787–1796

    PubMed Central  Google Scholar 

  • Thistle R, Cameron P, Ghorayshi A, Dennison L, Scott K (2012) Contact chemoreceptors mediate male–male repulsion male–female attraction during Drosophila courtship. Cell 149:1140–1151

    CAS  PubMed Central  PubMed  Google Scholar 

  • Toda H, Zhao X, Dickson BJ (2012) The Drosophila female aphrodisiac pheromone actives ppk23 + sensory neurons to elicit male courtship behavior. Cell Rep 1:599–607

    CAS  PubMed  Google Scholar 

  • Tootoonian S, Coen P, Kawai R, Murthy M (2012) Neural representations of courtship song in the Drosophila brain. J Neurosci 32:787–798

    CAS  PubMed Central  PubMed  Google Scholar 

  • Usui-Aoki K, Ito H, Ui-Tei K, Takahashi K, Lukacsovich T, Awano W, Nakata H, Piao ZF, Nilsson EE, Tomida J, Yamamoto D (2000) Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat Cell Biol 2:500–506

    CAS  PubMed  Google Scholar 

  • Venken KJT, Simpson JH, Bellen HJ (2011) Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron 72:202–230

    CAS  PubMed Central  PubMed  Google Scholar 

  • von Philipsborn AC, Liu T, Yu JY, Masser C, Bidaye SS, Dickson BJ (2011) Neuronal control of Drosophila courtship song. Neuron 69:509–522

    Google Scholar 

  • von Schilcher F (1976a) The function of pulse song and sine song in the courtship of Drosophila melanogaster. Anim Behav 24:622–625

    Google Scholar 

  • von Schilcher F (1976b) The role of auditory stimuli in the courtship of Drosophila melanogaster. Anim Behav 24:18–26

    Google Scholar 

  • Watanabe K, Toba G, Koganezawa M, Yamamoto D (2011) Gr39a, a highly diversified gustatory receptor in Drosophila, has a role in sexual behavior. Behav Genet 41:746–753

    PubMed  Google Scholar 

  • Yamamoto D, Ishikawa Y (2013) Genetic and neural bases for species-specific behavior in Drosophila species. J Neurogenet. doi:10.3109/01677063.2013.800060

    Google Scholar 

  • Yew JY, Dreisewerd K, Luftmann H, Muthing J, Pohlentz G, Kravitz EA (2009) A new male sex pheromone and cuticular cues for chemical communication in Drosophila. Curr Biol 19:1245–1254

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yu JY, Kanai MI, Demir E, Jefferis GS, Dickson BJ (2010) Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol 20:1602–1614

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors’ work is funded by Grants-in-Aid for Scientific Research (24113502, 23220007, 1802012 to D.Y., 25132702 and 24700309 to K.S. and 24570082 and 23115702 to M.K.) from MEXT, the Strategic Japanese-French Cooperative Program from JST (D.Y.) and a Life Science Grant from the Takeda Science Foundation (D.Y. and K.S.). The authors thank M. Suyama and S. Abe for secretarial assistance.

Author information

Authors and Affiliations

  1. Division of Neurogenetics, Tohoku University Graduate School of Life Sciences, 2-1-1 Katahira, Aoba-ku, Sendai, 980-8577, Japan

    Daisuke Yamamoto, Kosei Sato & Masayuki Koganezawa

Authors
  1. Daisuke Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kosei Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masayuki Koganezawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daisuke Yamamoto.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yamamoto, D., Sato, K. & Koganezawa, M. Neuroethology of male courtship in Drosophila: from the gene to behavior. J Comp Physiol A 200, 251–264 (2014). https://doi.org/10.1007/s00359-014-0891-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-014-0891-5

Keywords

Search

Navigation