What does the fruitless gene tell us about nature vs. nurture in the sex life of Drosophila?

References

• Gill K. A mutation causing abnormal courtship and mating behavior in males of Drosophila melanogaster. Am Zool 1963; 3:507
   Google Scholar
• Villella A, Gailey DA, Berwald B, Ohsima S, Barnes PT, Hall JC. Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics 1997; 147:1107-30; PMID:9383056
   PubMed Web of Science ®Google Scholar
• Lee G, Hall JC. Abnormalities of male-specific FRU protein and serotonin expression in the CNS of fruitless mutants in Drosophila. J Neurosci 2001; 21:513-26; PMID:11160431
   PubMed Web of Science ®Google Scholar
• Pan Y, Baker BS. Genetic identification and separation of innate and experience-dependent courtship behaviors in Drosophila. Cell 2014; 156:236-48; PMID:24439379; http://dx.doi.org/10.1016/j.cell.2013.11.041
   PubMed Web of Science ®Google Scholar
• Baker BS, Taylor BJ, Hall JC. Are complex behaviors specified by dedicated regulatory genes? Reasoning from Drosophila. Cell 2001; 105:13-24; PMID:11300999; http://dx.doi.org/10.1016/S0092-8674(01)00293-8
   PubMed Web of Science ®Google Scholar
• Dickson BJ. Wired for sex: the neurobiology of Drosophila mating decisions. Science 2008; 322:904-9; PMID:18988843; http://dx.doi.org/10.1126/science.1159276
   PubMed Web of Science ®Google Scholar
• Pavlou HJ, Goodwin SF. Courtship behavior in Drosophila melanogaster: towards a ‘courtship connectome’. Curr Opin Neurobiol 2012; 23:1-8; PMID:23265962; http://dx.doi.org/10.1016/j.conb.2012.09.002
   PubMed Web of Science ®Google Scholar
• Yamamoto D, Koganezawa M. Genes and circuits of courtship behavior in Drosophila males. Nat Rev Neurosci 2013; 14:681-92; PMID:24052176; http://dx.doi.org/10.1038/nrn3567
   PubMed Web of Science ®Google Scholar
• Kohatsu S, Yamamoto D. Visually induced initiation of Drosophila innate courtship-like following pursuit is mediated by central excitatory state. Nat Com 2015; 6:6457; http://dx.doi.org/10.1038/ncomms7457
   PubMed Web of Science ®Google Scholar
• Dankert H, Wang L, Hoopfer ED, Anderson DJ, Perona P. Automated monitoring and analysis of social behavior in Drosophila. Nat Methods; 6:297-303; PMID:19270697; http://dx.doi.org/10.1038/nmeth.1310
   PubMed Web of Science ®Google Scholar
• 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; 59:759-69; PMID:18786359; http://dx.doi.org/10.1016/j.neuron.2008.06.007
   PubMed Web of Science ®Google Scholar
• Koganezawa M, Haba D, Matuo T, Yamamoto D. The shaping of male courtship posture by lateralized gustatory inputs to male-specific interneurons. Curr Biol 2010; 20:1-8; PMID:20036540; http://dx.doi.org/10.1016/j.cub.2009.11.038
   PubMed Web of Science ®Google Scholar
• Kohatsu S, Koganezawa M, Yamamoto D. Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 2011; 69:498-508; PMID:21315260; http://dx.doi.org/10.1016/j.neuron.2010.12.017
   PubMed Web of Science ®Google Scholar
• Inagaki HK, Jung Y, Hoopfer ED, Wong AM, Mishra N, Lin JY, Tsien RY, Anderson D. Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship. Nat Methods 2014; 11:325-32; PMID:24363022; http://dx.doi.org/10.1038/nmeth.2765
   PubMed Web of Science ®Google Scholar
• Lee G, Foss M, Goodwin SF, Carlo T, Taylor BJ, Hall JC. Spatial, temporal, and sexually dimorphic expressions patterns of the fruitless gene in the Drosophila central nervous system. J Neurobiol. 2000; 43:404-26; PMID:10861565; http://dx.doi.org/10.1002/1097-4695(20000615)43:4%3c404::AID-NEU8%3e3.0.CO;2-D
   PubMedGoogle 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. Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat Cell Biol 2000; 2:500-6; PMID:10934470; http://dx.doi.org/10.1038/35019537
   PubMed Web of Science ®Google Scholar
• Hueston CE, Olsen D, Li Q, Okuwa S, Peng B, Wu J, Volkan PC. Chromatin modulatory proteins and olfactory receptor signaling in the refinement and maintenance of fruitless expression in olfactory receptor neurons. PLoS Biol 2016; 14:e1002443; PMID:27093619; http://dx.doi.org/10.1371/journal.pbio.1002443
   PubMedGoogle Scholar
• Couto A, Alenius M, Dickson BJ. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 2005; 15:1535-47; PMID:16139208; http://dx.doi.org/10.1016/j.cub.2005.07.034
   PubMed Web of Science ®Google Scholar
• Grosjean Y, Rytz R, Farine JP, Abuin L, Cortot J, Jefferis GSXE, Benton R. An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 2011; 478:236-40; PMID:21964331; http://dx.doi.org/10.1038/nature10428
   PubMed Web of Science ®Google Scholar
• Stockinger P, Kvitsiani D, Rotkopf S, Tirián L, Dickson BJ. Neural circuitry that governs Drosophila male courtship behavior. Cell 2005; 121:795-807; PMID:15935765; http://dx.doi.org/10.1016/j.cell.2005.04.026
   PubMed Web of Science ®Google Scholar
• Kondoh Y, Kaneshiro KY, Kimura K-I, Yamamoto D. Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc Biol Sci 2003; 270:1005-13; PMID:12803889; http://dx.doi.org/10.1098/rspb.2003.2331
   PubMed Web of Science ®Google Scholar
• Dweck HKM, Ebrahim SAM, Thoma M, Mohamed AAM, Keesey IW, Trona F, Lavista-Llanos S, SvatoŠ A, Sachse S, Knaden M, Hansson BS. Pheromones mediating copulation and attraction in Drosophila. Proc Natl Acad Sci U S A 2015; 112:21:E2829-35; PMID:25964351; http://dx.doi.org/10.1073/pnas.1504527112
   PubMedGoogle Scholar
• Kurtovic A, Widmer A, Dickson BJ. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 2007; 446:542-6; PMID:17392786; http://dx.doi.org/10.1038/nature05672
   PubMed Web of Science ®Google Scholar
• Butterworth FM. Lipids of Drosophila: a newly detected lipid in the male. Science 1969; 163:1356-7; PMID:5765118; http://dx.doi.org/10.1126/science.163.3873.1356
   PubMed Web of Science ®Google Scholar
• Jallon JM. A few chemical words exchanged by Drosophila during courtship and mating. Behav Genet 1984; 14:441-78; PMID:6441563; http://dx.doi.org/10.1007/BF01065444
   PubMed Web of Science ®Google Scholar
• Kayser MS, Yue Z, Sehgal A. A critical period of sleep for development of courtship circuitry and behavior in Drosophila. Science 2014; 344:269-74; PMID:24744368; http://dx.doi.org/10.1126/science.1250553
   PubMed Web of Science ®Google Scholar
• Devaud JM, Acebes A, Ferrus A. Odor exposure causes central adaptation and morphological changes in selected olfactory glomeruli in Drosophila. J Neurosci 2001; 21:6274-82; PMID:11487650
   PubMed Web of Science ®Google Scholar
• van der Goes van Naters W, Carlson JR. Receptors and neurons for fly odors in Drosophila. Curr Biol; 2007; 17:606-12; PMID:17363256; http://dx.doi.org/10.1016/j.cub.2007.02.043
   PubMed Web of Science ®Google Scholar
• de Renobales M, Blomquist GJ. Biosynthesis of medium chain fatty acids in Drosophila melanogaster. Arch Biochem Biophys 1984; 228:407-14; PMID:6421238; http://dx.doi.org/10.1016/0003-9861(84)90004-3
   PubMed Web of Science ®Google Scholar
• Bonsquet F, Nojima T, Houot B, Chauvel I, Chaudy S, Dupas S, Yamamoto D, Ferveur J-F. Expression of desat1 in neural and nonneural tissues separately affects perception and emission of sex pheromones in Drosophila. Proc Natl Acad Sci U S A 2012; 109:249-54; PMID:22114190; http://dx.doi.org/10.1073/pnas.1109166108
   PubMed Web of Science ®Google Scholar
• Billeter JC, Atallah J, Krupp JJ, Millar JG, Levine JD. Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 2009; 461:987-91; PMID:19829381; http://dx.doi.org/10.1038/nature08495
   PubMed Web of Science ®Google Scholar
• Agrawal S, Safarik S, Dickinson M. The relative roles of vision and chemosensation in mate recognition of Drosophila melanogaster. J Exp Biol 2014; 217:2796-805; PMID:24902744; http://dx.doi.org/10.1242/jeb.105817
   PubMed Web of Science ®Google Scholar
• Pan Y, Meissner GW, Baker BS. Joint control of Drosophila male courtship behavior by motion cues and activation of male-specific P1 neurons. Proc Natl Acad Sci U S A 2012; 109:10065-70; PMID:22645338; http://dx.doi.org/10.1073/pnas.1207107109
   PubMed Web of Science ®Google Scholar
• Bath DE, Stowers JR, Hörmann D, Poehlmann A, Dickson BJ, Straw AD. FlyMAD: rapid thermogenetic control of neuronal activity in freely walking Drosophila. Nat Methods 2014; 11:756-62; PMID:24859752; http://dx.doi.org/10.1038/nmeth.2973
   PubMed Web of Science ®Google Scholar
• Wang L, Han X, Mehren J, Hiroi M, Billeter JC, Miyamaoto T, Amrein H, Levine JD, Anderson JD. Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat Neurosci 2011; 14:757-62; PMID:21516101; http://dx.doi.org/10.1038/nn.2800
   PubMed Web of Science ®Google Scholar
• Clowney EJ, Iguchi S, Bussell JJ, Scheer E, Ruta V. Multimodal chemosensory circuits controlling male courtship in Drosophila. Neuron 2015; 87:1036-49; PMID:26279475; http://dx.doi.org/10.1016/j.neuron.2015.07.025
   PubMed Web of Science ®Google Scholar
• Lin HH, Cao DS, Sethi S, Zeng Z, Chin JSR, Chakraborty TS, Shepherd AK, Nguyen CA, Yew JY, Su C-Y, Wang JW. Hormonal modulation of pheromone detection enhances male courtship success. Neuron 2016; 90:1272-85; PMID:27263969; http://dx.doi.org/10.1016/j.neuron.2016.05.004
   PubMed Web of Science ®Google Scholar
• Saleem S, Ruggles PH, Abbott WK, Carney GE. Sexual experience enhances Drosophila melanogaster male mating behavior and success. PLoS One 2014; 9:e96639; PMID:24805129; http://dx.doi.org/10.1371/journal.pone.0096639
   PubMedGoogle Scholar
• Baxter CM, Barnett R, Dukas R. Effects of age and experience on male mate choosiness. Ethology 2014; 121:353-63; http://dx.doi.org/10.1111/eth.12344
   Web of Science ®Google Scholar
• Aigaki T, Fleischmann I, Chen PS, Kubli E. Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster. Neuron 1991; 7:557-63; PMID:1931051; http://dx.doi.org/10.1016/0896-6273(91)90368-A
   PubMed Web of Science ®Google Scholar
• Fricke C, Green D, Mills WE, Chapman T. Age-dependent female responses to a male ejaculate signal after demographic opportunities for selection. Proc Biol Sci 2013; 280:20130428; PMID:23843383; http://dx.doi.org/10.1098/rspb.2013.0428
   PubMed Web of Science ®Google Scholar
• Zhuang L, Sun Y, Hu M, Wu C, La X, Chen X, Feng Y, Wang X, Hu Y, Xue L. Or47b plays a role in Drosophila males preference for younger mates. Open Biol 2016; 6:160086; PMID:27278650; http://dx.doi.org/10.1098/rsob.160086
   PubMed Web of Science ®Google Scholar
• Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yamamoto D. 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 U S A. 1996; 93:9687-92; PMID:8790392; http://dx.doi.org/10.1073/pnas.93.18.9687
   PubMed Web of Science ®Google Scholar
• Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Taylor BJ, Wasserman SA. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 1996; 87:1079-89; PMID:8978612; http://dx.doi.org/10.1016/S0092-8674(00)81802-4
   PubMed Web of Science ®Google Scholar
• Ito H, Sato K, Koganezawa M, Ote M, Matsumoto K, Hama C, Yamamoto D. Fruitless recruits two antagonistic chromatin factors to establish single-neuron sexual dimorphism. Cell 2012; 149:1327-38; PMID:22682252; http://dx.doi.org/10.1016/j.cell.2012.04.025
   PubMed Web of Science ®Google Scholar
• Neville MC, Nojima T, Ashley E, Parker DJ, Walker J, Southhall T, Van de Sande B, Marques AC, Fischer B, Brand AH, et al. Male-specific Fruitless isoforms target neurodevelopmental genes to specify a sexually dimorphic nervous system. Curr Biol 2014; 24:229-41; PMID:24440396; http://dx.doi.org/10.1016/j.cub.2013.11.035
   PubMed Web of Science ®Google Scholar
• Vernes SC. Genome wide identification of fruitless targets suggests a role in upregulating genes important for neural circuit formation. Sci Rep 2014; 4:4412; PMID:24642956; http://dx.doi.org/10.1038/srep04412
   PubMed Web of Science ®Google Scholar
• Ito H, Sato K, Kondo S, Ueda R, Yamamoto D. Fruitless represses robo1 transcription to shape male-specific neural morphology and behavior in Drosophila. Curr Biol 2016; 26:1532-42; PMID:27265393; http://dx.doi.org/10.1016/j.cub.2016.04.067
   PubMed Web of Science ®Google Scholar
• Masuyama K, Zhang Y, Rao Y, Wang JW. Mapping neural circuits with activity-dependent nuclear import of a transcription factor. J Neurogenet 2012; 26:89-102; PMID:22236090; http://dx.doi.org/10.3109/01677063.2011.642910
   PubMed Web of Science ®Google Scholar
• Yang Y, Hill KK, Hemberg M, Reddy NC, Cho HY, Guthrie AN, Oldenborg A, Heiney SA, Ohmae S, Medina JF, et al. Chromatin remodeling inactivates activity genes and regulates neural coding. Science 2016; 353:300-5; PMID:27418512; http://dx.doi.org/10.1126/science.aad4225
   PubMed Web of Science ®Google Scholar
• Xu PS, Lee D, Holy TE. Experience-dependent plasticity drives individual differences in pheromone-sensing neurons. Neuron 2016; 91:878-92; PMID:27537487; http://dx.doi.org/10.1016/j.neuron.2016.07.034
   PubMed Web of Science ®Google Scholar
• Southall TD, Gold KS, Egger B, Davidson CM, Caygill EE, Marshall OJ, Brand AH. Cell-type-specific profiling of gene expression and chromatin binding without cell isolation: assaying RNA Pol II occupancy in neural stem cells. Dev Cell 2013; 26:101-12; PMID:23792147; http://dx.doi.org/10.1016/j.devcel.2013.05.020
   PubMed Web of Science ®Google Scholar
• Weaver ICG, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Secckl JR, Dymov S, Szyf M, Meaney MJ. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7:847-54; PMID:15220929; http://dx.doi.org/10.1038/nn1276
   PubMed Web of Science ®Google Scholar
• Meaney M. Environmental programming of phenotypic diversity in female reproductive strategies. Adv Genet 2007; 59:173-215; PMID:17888799; http://dx.doi.org/10.1016/S0065-2660(07)59007-3
   PubMed Web of Science ®Google Scholar
• Lüpold S, Manier MK, Ala-Honkola O, Belote JM, Pitnick S. Male Drosophila melanogaster adjust ejaculate size based on female mating stats, fecundity, and age. Behav Ecol 2011; 22:184-91; http://dx.doi.org/10.1093/beheco/arq193
   Web of Science ®Google Scholar
• Parker GA, Pizzari T. Sperm competition and ejaculate economics. Biol Rev Camb Philos Soc 2010; 85:897-934; PMID:20560928; http://dx.doi.org/10.1111/j.1469-185X.2010.00140.x
   PubMed Web of Science ®Google Scholar