Wired for Sex: The Neurobiology of Drosophila Mating Decisions

Decisions about whom to mate with can sometimes be difficult, but making the right choice is critical for an animal's reproductive success. The ubiquitous fruit fly, Drosophila, is clearly very good at making these decisions. Upon encountering another fly, a male may or may not choose to court. He estimates his chances of success primarily on the basis of pheromone signals and previous courtship experience. The female decides whether to accept or reject the male, depending on her perception of his pheromone and acoustic signals, as well as her own readiness to mate. This simple and genetically tractable system provides an excellent model to explore the neurobiology of decision making.

[1]  A. Sturtevant,et al.  Experiments on sex recognition and the problem of sexual selection in Drosoophilia. , 1915 .

[2]  H. H. Shorey,et al.  Nature of the Sound Produced by Drosophila melanogaster during Courtship , 1962, Science.

[3]  A. Manning,et al.  The control of sexual receptivity in female Drosophila. , 1962, Animal behaviour.

[4]  H. Bennet-Clark,et al.  Stimuli provided by Courtship of Male Drosophila melanogaster , 1967, Nature.

[5]  H. Bennet-Clark,et al.  THE COURTSHIP SONGS OF DROSOPHILA , 1968 .

[6]  F. M. Butterworth Lipids of Drosophila: A Newly Detected Lipid in the Male , 1969, Science.

[7]  H. C. Bennet-Clark,et al.  Pulse interval as a critical parameter in the courtship song of Drosophila melanogaster , 1969 .

[8]  F. Schilcher,et al.  The role of auditory stimuli in the courtship of Drosophila melanogaster , 1976, Animal Behaviour.

[9]  F. Schilcher The behavior of cacophony, a courtship song mutant in Drosophila melanogaster , 1976 .

[10]  F. Schilcher The function of pulse song and sine song in the courtship of Drosophila melanogaster , 1976, Animal Behaviour.

[11]  J. C. Hall Portions of the central nervous system controlling reproductive behavior inDrosophila melanogaster , 1977, Behavior genetics.

[12]  Jeffrey C. Hall,et al.  The function of courtship song rhythms in Drosophila , 1982, Animal Behaviour.

[13]  S. Mane,et al.  Male Esterase 6 Catalyzes the Synthesis of a Sex Pheromone in Drosophila melanogaster Females , 1983, Science.

[14]  C P Kyriacou,et al.  Interspecific genetic control of courtship song production and reception in Drosophila. , 1986, Science.

[15]  J. David,et al.  VARIATIONS IN CUTICULAR HYDROCARBONS AMONG THE EIGHT SPECIES OF THE DROSOPHILA MELANOGASTER SUBGROUP , 1987, Evolution; international journal of organic evolution.

[16]  T. Markow,et al.  Behavioral and sensory basis of courtship success in Drosophila melanogaster. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[17]  M. Bienz,et al.  A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster , 1988, Cell.

[18]  B. S. Baker,et al.  Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides , 1989, Cell.

[19]  J. Jallon,et al.  A new acoustic signal of the fruit-flies Drosophila simulans and D. melanogaster , 1991 .

[20]  C. Löfstedt,et al.  Functional specialization of olfactory glomeruli in a moth. , 1992, Science.

[21]  J. Truman,et al.  Commitment of abdominal neuroblasts in Drosophila to a male or female fate is dependent on genes of the sex-determining hierarchy. , 1992, Development.

[22]  K. Burtis,et al.  The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. , 1993, The EMBO journal.

[23]  B. S. Baker,et al.  Behavioral and neurobiological implications of sex-determining factors in Drosophila. , 1994, Developmental genetics.

[24]  H. Bennet-Clark,et al.  Courtship song components affect male and female Drosophila differently , 1995, Animal Behaviour.

[25]  Jeffrey C. Hall,et al.  Control of Male Sexual Behavior and Sexual Orientation in Drosophila by the fruitless Gene , 1996, Cell.

[26]  D. Yamamoto,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. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Y. Choffat,et al.  Sexual behaviour in Drosophila is irreversibly programmed during a critical period , 1998, Current Biology.

[28]  J. Weiner,et al.  Time, Love, Memory: A Great Biologist and His Quest for the Origins of Behavior , 1999 .

[29]  K. Siwicki,et al.  Mushroom Body Ablation Impairs Short-Term Memory and Long-Term Memory of Courtship Conditioning in Drosophila melanogaster , 1999, Neuron.

[30]  J. Ashby References and Notes , 1999 .

[31]  Richard Axel,et al.  An Olfactory Sensory Map in the Fly Brain , 2000, Cell.

[32]  J. C. Hall,et al.  Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. , 2000, Journal of neurobiology.

[33]  J. C. Hall,et al.  New reproductive anomalies in fruitless-mutant Drosophila males: extreme lengthening of mating durations and infertility correlated with defective serotonergic innervation of reproductive organs. , 2001, Journal of neurobiology.

[34]  L. Luo,et al.  Representation of the Glomerular Olfactory Map in the Drosophila Brain , 2002, Cell.

[35]  Richard Axel,et al.  Spatial Representation of the Glomerular Map in the Drosophila Protocerebrum , 2002, Cell.

[36]  S. Shen-Orr,et al.  Network motifs: simple building blocks of complex networks. , 2002, Science.

[37]  T Aubin,et al.  Functional coupling of acoustic and chemical signals in the courtship behaviour of the male Drosophila melanogaster , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  M. Göpfert,et al.  The mechanical basis of Drosophila audition. , 2002, The Journal of experimental biology.

[39]  M. Heisenberg,et al.  Evolutionary significance of courtship conditioning in Drosophila melanogaster , 2002, Animal Behaviour.

[40]  E. Kubli,et al.  Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[41]  M. Wolfner,et al.  The developments between gametogenesis and fertilization: ovulation and female sperm storage in Drosophila melanogaster. , 2003, Developmental biology.

[42]  L. Partridge,et al.  The sex peptide of Drosophila melanogaster: Female post-mating responses analyzed by using RNA interference , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[43]  U. Alon,et al.  Search for computational modules in the C. elegans brain , 2004, BMC Biology.

[44]  D. Yamamoto,et al.  Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[45]  M. Heisenberg Mushroom body memoir: from maps to models , 2003, Nature Reviews Neuroscience.

[46]  J. Ferveur,et al.  World-wide variation inDrosophila melanogaster sex pheromone: behavioural effects, genetic bases and potential evolutionary consequences , 2004, Genetica.

[47]  Peter Schlegel,et al.  Die Schwingungen der Antenne und ihre Bedeutung für die Flugsteuerung bei Calliphora erythrocephala , 1970, Zeitschrift für vergleichende Physiologie.

[48]  Jeffrey C. Hall,et al.  Neural topography of courtship song in sex mosaics ofDrosophila melanogaster , 1979, Journal of comparative physiology.

[49]  R. Dukas Male fruit flies learn to avoid interspecific courtship , 2004 .

[50]  G. Gisselmann,et al.  Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster , 2005, Nature Neuroscience.

[51]  Barry J. Dickson,et al.  fruitless Splicing Specifies Male Courtship Behavior in Drosophila , 2005, Cell.

[52]  Devanand S. Manoli,et al.  Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour , 2005, Nature.

[53]  R. Dukas Learning affects mate choice in female fruit flies , 2005 .

[54]  P. Xu,et al.  Drosophila OBP LUSH Is Required for Activity of Pheromone-Sensitive Neurons , 2005, Neuron.

[55]  T. Honegger,et al.  Gradual Release of Sperm Bound Sex-Peptide Controls Female Postmating Behavior in Drosophila , 2005, Current Biology.

[56]  D. Kvitsiani,et al.  Neural Circuitry that Governs Drosophila Male Courtship Behavior , 2005, Cell.

[57]  R. Dukas Experience improves courtship in male fruit flies , 2005, Animal Behaviour.

[58]  Leslie B. Vosshall,et al.  Genetic and Functional Subdivision of the Drosophila Antennal Lobe , 2005, Current Biology.

[59]  Richard S. Sutton,et al.  Reinforcement Learning: An Introduction , 1998, IEEE Trans. Neural Networks.

[60]  Daisuke Yamamoto,et al.  Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain , 2005, Nature.

[61]  J. Ferveur Cuticular Hydrocarbons: Their Evolution and Roles in Drosophila Pheromonal Communication , 2005, Behavior genetics.

[62]  Barry J. Dickson,et al.  Molecular, Anatomical, and Functional Organization of the Drosophila Olfactory System , 2005, Current Biology.

[63]  D. Kvitsiani,et al.  Shared neural circuitry for female and male sexual behaviours in Drosophila , 2006, Current Biology.

[64]  Kei Ito,et al.  Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster , 2006, The Journal of comparative neurology.

[65]  Z. Mainen,et al.  Early events in olfactory processing. , 2006, Annual review of neuroscience.

[66]  Silke Sachse,et al.  Atypical Membrane Topology and Heteromeric Function of Drosophila Odorant Receptors In Vivo , 2006, PLoS biology.

[67]  Dean P. Smith,et al.  A Pheromone Receptor Mediates 11-cis-Vaccenyl Acetate-Induced Responses in Drosophila , 2006, The Journal of Neuroscience.

[68]  Barry J Dickson,et al.  fruitless regulates aggression and dominance in Drosophila , 2006, Nature Neuroscience.

[69]  J. Allendorfer,et al.  Isoform-Specific Control of Male Neuronal Differentiation and Behavior in Drosophila by the fruitless Gene , 2006, Current Biology.

[70]  L. Vosshall,et al.  An essential role for a CD36-related receptor in pheromone detection in Drosophila , 2007, Nature.

[71]  J. Billeter,et al.  The Sex-Determination Genes fruitless and doublesex Specify a Neural Substrate Required for Courtship Song , 2007, Current Biology.

[72]  L. Luo,et al.  Comprehensive Maps of Drosophila Higher Olfactory Centers: Spatially Segregated Fruit and Pheromone Representation , 2007, Cell.

[73]  B. Dickson,et al.  A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone , 2007, Nature.

[74]  J. Levine,et al.  Generalization of Courtship Learning in Drosophila Is Mediated by cis-Vaccenyl Acetate , 2007, Current Biology.

[75]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[76]  Barry J Dickson,et al.  Function of the Drosophila CPEB protein Orb2 in long-term courtship memory , 2007, Nature Neuroscience.

[77]  Björn Nadrowski,et al.  Mechanical Signatures of Transducer Gating in the Drosophila Ear , 2007, Current Biology.

[78]  John R. Carlson,et al.  Receptors and Neurons for Fly Odors in Drosophila , 2007, Current Biology.

[79]  J. Armstrong,et al.  Functional dissection of the neural substrates for gravitaxic maze behavior in Drosophila melanogaster , 2007, The Journal of comparative neurology.

[80]  Rachel I. Wilson,et al.  Olfactory processing and behavior downstream from highly selective receptor neurons , 2007, Nature Neuroscience.

[81]  Regine Heller,et al.  Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels , 2008, Nature.

[82]  K. Svoboda,et al.  Genetic Dissection of Neural Circuits , 2008, Neuron.

[83]  Dean P. Smith,et al.  Activation of Pheromone-Sensitive Neurons Is Mediated by Conformational Activation of Pheromone-Binding Protein , 2008, Cell.

[84]  B. Dickson,et al.  A receptor that mediates the post-mating switch in Drosophila reproductive behaviour , 2008, Nature.

[85]  G. Miesenböck,et al.  Sex-Specific Control and Tuning of the Pattern Generator for Courtship Song in Drosophila , 2008, Cell.

[86]  Ruedi Stoop,et al.  Periodic orbit analysis demonstrates genetic constraints, variability, and switching in Drosophila courtship behavior. , 2008, Chaos.

[87]  M. Koganezawa,et al.  Fruitless and Doublesex Coordinate to Generate Male-Specific Neurons that Can Initiate Courtship , 2008, Neuron.

[88]  G. Rubin,et al.  Tools for neuroanatomy and neurogenetics in Drosophila , 2008, Proceedings of the National Academy of Sciences.

[89]  Barry J. Dickson,et al.  The Drosophila pheromone cVA activates a sexually dimorphic neural circuit , 2008, Nature.

[90]  Leslie B. Vosshall,et al.  Insect olfactory receptors are heteromeric ligand-gated ion channels , 2008, Nature.

[91]  Jing W. Wang,et al.  A Presynaptic Gain Control Mechanism Fine-Tunes Olfactory Behavior , 2008, Neuron.

[92]  T. Ha,et al.  SNMP is a signaling component required for pheromone sensitivity in Drosophila , 2008, Proceedings of the National Academy of Sciences.