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1.  Neural Circuitry Underlying Drosophila Female Postmating Behavioral Responses 
Current Biology  2012;22(13):1155-1165.
Summary
Background
After mating, Drosophila females undergo a remarkable phenotypic switch resulting in decreased sexual receptivity and increased egg laying. Transfer of male sex peptide (SP) during copulation mediates these postmating responses via sensory neurons that coexpress the sex-determination gene fruitless (fru) and the proprioceptive neuronal marker pickpocket (ppk) in the female reproductive system. Little is known about the neuronal pathways involved in relaying SP-sensory information to central circuits and how these inputs are processed to direct female-specific changes that occur in response to mating.
Results
We demonstrate an essential role played by neurons expressing the sex-determination gene doublesex (dsx) in regulating the female postmating response. We uncovered shared circuitry between dsx and a subset of the previously described SP-responsive fru+/ppk+-expressing neurons in the reproductive system. In addition, we identified sexually dimorphic dsx circuitry within the abdominal ganglion (Abg) critical for mediating postmating responses. Some of these dsx neurons target posterior regions of the brain while others project onto the uterus.
Conclusions
We propose that dsx-specified circuitry is required to induce female postmating behavioral responses, from sensing SP to conveying this signal to higher-order circuits for processing and through to the generation of postmating behavioral and physiological outputs.
Highlights
► dsx circuitry plays a pivotal role in the female postmating switch ► Peripheral dsx neurons detect and respond to sex peptide ► Central dsx neurons convey this signal to higher-order processing and direct postmating responses.
doi:10.1016/j.cub.2012.04.062
PMCID: PMC3396843  PMID: 22658598
2.  Sound production during agonistic behavior of male Drosophila melanogaster 
Fly  2011;5(1):29-38.
Male Drosophila fruit flies acquire and defend territories in order to attract females for reproduction. Both, male-directed agonistic behavior and female-directed courtship consist of series of recurrent stereotypical components. Various studies demonstrated the importance of species-specific sound patterns generated by wing vibration as being critical for male courtship success. In this study we analyzed the patterns and importance of sound signals generated during agonistic interactions of male Drosophila melanogaster. In contrast to acoustic courtship signals that consist of sine and pulse patterns and are generated by one extended wing, agonistic signals lack sine-like components and are generally produced by simultaneous movements of both wings. Though intra-pulse oscillation frequencies (carrier frequency) are identical, inter-pulse intervals are twice as long and more variable in aggression signals than in courtship songs, where their precise temporal pattern serves species recognition. Acoustic signals accompany male agonistic interactions over their entire course but occur particularly often after tapping behavior which is a major way to identify the gender of the interaction partner. Since similar wing movements may either be silent or generate sound and wing movements with sound have a greater impact on the subsequent behavior of a receiver, sound producing wing movements seem to be generated intentionally to serve as a specific signal during fruit fly agonistic encounters.
doi:10.4161/fly.5.1.13713
PMCID: PMC3052870  PMID: 20953152
acoustic signals; temporal patterns; frequency analysis; agonistic behavior; courtship; ethogram
3.  Correction: Pheromonal and Behavioral Cues Trigger Male-to-Female Aggression in Drosophila 
PLoS Biology  2010;8(12):10.1371/annotation/1c19d040-9f9f-4b9f-b678-70f1fe387192.
doi:10.1371/annotation/1c19d040-9f9f-4b9f-b678-70f1fe387192
PMCID: PMC2997046
4.  Pheromonal and Behavioral Cues Trigger Male-to-Female Aggression in Drosophila 
PLoS Biology  2010;8(11):e1000541.
By genetically manipulating both pheromonal profiles and behavioral patterns, we find that Drosophila males showed a complete reversal in their patterns of aggression towards other males and females
Appropriate displays of aggression rely on the ability to recognize potential competitors. As in most species, Drosophila males fight with other males and do not attack females. In insects, sex recognition is strongly dependent on chemosensory communication, mediated by cuticular hydrocarbons acting as pheromones. While the roles of chemical and other sensory cues in stimulating male to female courtship have been well characterized in Drosophila, the signals that elicit aggression remain unclear. Here we show that when female pheromones or behavior are masculinized, males recognize females as competitors and switch from courtship to aggression. To masculinize female pheromones, a transgene carrying dsRNA for the sex determination factor transformer (traIR) was targeted to the pheromone producing cells, the oenocytes. Shortly after copulation males attacked these females, indicating that pheromonal cues can override other sensory cues. Surprisingly, masculinization of female behavior by targeting traIR to the nervous system in an otherwise normal female also was sufficient to trigger male aggression. Simultaneous masculinization of both pheromones and behavior induced a complete switch in the normal male response to a female. Control males now fought rather than copulated with these females. In a reciprocal experiment, feminization of the oenocytes and nervous system in males by expression of transformer (traF) elicited high levels of courtship and little or no aggression from control males. Finally, when confronted with flies devoid of pheromones, control males attacked male but not female opponents, suggesting that aggression is not a default behavior in the absence of pheromonal cues. Thus, our results show that masculinization of either pheromones or behavior in females is sufficient to trigger male-to-female aggression. Moreover, by manipulating both the pheromonal profile and the fighting patterns displayed by the opponent, male behavioral responses towards males and females can be completely reversed. Therefore, both pheromonal and behavioral cues are used by Drosophila males in recognizing a conspecific as a competitor.
Author Summary
As in other species, the fruit fly Drosophila melanogaster uses chemical signals in the form of pheromones to recognize the species and sex of another individual. Males typically fight with other males and do not attack females. While the roles of pheromonal and other sensory cues in stimulating courtship towards females have been extensively studied, the signals that elicit aggression towards other males remain unclear. In this work, we use genetic tools to show that masculinization of female pheromones is sufficient to trigger aggression from wild type males towards females. Surprisingly, males also attacked females that displayed male patterns of aggression, even if they show normal female pheromonal profiles, indicating that pheromones are not the only cues important for identifying another animal as an opponent. By simultaneously manipulating pheromones and behavioral patterns of opponents, we can completely switch the behavioral response of males towards females and males. These results demonstrate that not only pheromonal but also behavioral cues can serve as triggers of aggression, underlining the importance of behavioral feedback in the manifestation of social behaviors.
doi:10.1371/journal.pbio.1000541
PMCID: PMC2990703  PMID: 21124886
5.  Octopamine Neuromodulatory Effects on a Social Behavior Decision-Making Network in Drosophila Males 
PLoS ONE  2010;5(10):e13248.
Situations requiring rapid decision-making in response to dynamic environmental demands occur repeatedly in natural environments. Neuromodulation can offer important flexibility to the output of neural networks in coping with changing conditions, but the contribution of individual neuromodulatory neurons in social behavior networks remains relatively unknown. Here we manipulate the Drosophila octopaminergic system and assay changes in adult male decision-making in courtship and aggression paradigms. When the functional state of OA neural circuits is enhanced, males exhibit elevated courtship behavior towards other males in both behavioral contexts. Eliminating the expression of the male form of the neural sex determination factor, Fruitless (FruM), in three OA suboesophageal ganglia (SOG) neurons also leads to increased male-male courtship behavior in these same contexts. We analyzed the fine anatomical structure through confocal examination of labeled single neurons to determine the arborization patterns of each of the three FruM-positive OA SOG neurons. These neurons send processes that display mirror symmetric, widely distributed arbors of endings within brain regions including the ventrolateral protocerebra, the SOG and the peri-esophageal complex. The results suggest that a small subset of OA neurons have the potential to provide male selective modulation of behavior at a single neuron level.
doi:10.1371/journal.pone.0013248
PMCID: PMC2953509  PMID: 20967276
6.  A new male sex-pheromone and novel cuticular cues for chemical communication in Drosophila 
Current biology : CB  2009;19(15):1245-1254.
Summary
Background
In many insect species, cuticular hydrocarbons serve as pheromones that can mediate complex social behaviors. In Drosophila melanogaster, several hydrocarbons including the male sex pheromone 11-cis-vaccenyl acetate (cVA) and female-specific 7,11-dienes influence courtship behavior and can function as cues for short-term memory associated with the mating experience. Behavioral and physiological studies suggest that other unidentified chemical communication cues are likely to exist. To more fully characterize the hydrocarbon profile of the D. melanogaster cuticle, we applied direct ultraviolet laser desorption/ionization orthogonal time-of-flight mass spectrometry (UV-LDI-o-TOF MS) and analyzed the surface of intact fruit flies at a spatial resolution of approximately 200 μm.
Results
We report the chemical and spatial characterization of 28 species of cuticular hydrocarbons, including a new major class of oxygen-containing compounds. Using UV-LDI MS, pheromones previously shown to be expressed exclusively by one sex, e.g. cVA, 7,11-heptacosadiene, and 7,11-nonacosadiene, appear to be found on both male and female flies. In males, cVA co-localizes at the tip of the ejaculatory bulb with a second acetylated hydrocarbon named CH503. We describe the chemical structure of CH503 as 3-O-acetyl-1,3-dihydroxy-octacosa-11,19-diene and show one behavioral role for this compound as a long-lived inhibitor of male courtship. Like cVA, CH503 is transferred from males to females during mating. Unlike cVA, CH503 remains on the surface of females for at least 10 days.
Conclusions
Oxygenated hydrocarbons comprise one major previously undescribed class of compounds on the Drosophila cuticular surface. In addition to cVA, a newly-discovered long chain acetate, CH503, serves as a mediator of courtship-related chemical communication.
doi:10.1016/j.cub.2009.06.037
PMCID: PMC2726907  PMID: 19615904
7.  Targeted Manipulation of Serotonergic Neurotransmission Affects the Escalation of Aggression in Adult Male Drosophila melanogaster 
PLoS ONE  2010;5(5):e10806.
Dopamine (DA) and serotonin (5HT) are reported to serve important roles in aggression in a wide variety of animals. Previous investigations of 5HT function in adult Drosophila behavior have relied on pharmacological manipulations, or on combinations of genetic tools that simultaneously target both DA and 5HT neurons. Here, we generated a transgenic line that allows selective, direct manipulation of serotonergic neurons and asked whether DA and 5HT have separable effects on aggression. Quantitative morphological examination demonstrated that our newly generated tryptophan hydroxylase (TRH)-Gal4 driver line was highly selective for 5HT-containing neurons. This line was used in conjunction with already available Gal4 driver lines that target DA or both DA and 5HT neurons to acutely alter the function of aminergic systems. First, we showed that acute impairment of DA and 5HT neurotransmission using expression of a temperature sensitive form of dynamin completely abolished mid- and high-level aggression. These flies did not escalate fights beyond brief low-intensity interactions and therefore did not yield dominance relationships. We showed next that manipulation of either 5HT or DA neurotransmission failed to duplicate this phenotype. Selective disruption of 5HT neurotransmission yielded flies that fought, but with reduced ability to escalate fights, leading to fewer dominance relationships. Acute activation of 5HT neurons using temperature sensitive dTrpA1 channel expression, in contrast, resulted in flies that escalated fights faster and that fought at higher intensities. Finally, acute disruption of DA neurotransmission produced hyperactive flies that moved faster than controls, and rarely engaged in any social interactions. By separately manipulating 5HT- and DA- neuron systems, we collected evidence demonstrating a direct role for 5HT in the escalation of aggression in Drosophila.
doi:10.1371/journal.pone.0010806
PMCID: PMC2875409  PMID: 20520823
8.  fruitless, doublesex and the genetics of social behavior in Drosophila melanogaster 
Current opinion in neurobiology  2009;19(2):200-206.
Summary
Two genes coding for transcription factors, fruitless and doublesex, have been suggested to play important roles in the regulation of sexually dimorphic patterns of social behavior in Drosophila melanogaster. The generalization that fruitless specified the development of the nervous system and doublesex specified non-neural tissues culminated with claims that fruitless was both necessary and sufficient to establish sex-specific patterns of behavior. Several recent articles refute this notion, however, demonstrating that at a minimum, both fruitless and doublesex are involved in establishing sexually dimorphic features of neural circuitry and behavior in fruit flies.
doi:10.1016/j.conb.2009.04.001
PMCID: PMC2716404  PMID: 19541474
9.  Feminizing cholinergic neurons in a male Drosophila nervous system enhances aggression 
Fly  2009;3(3):179-184.
Previous studies in Drosophila have demonstrated that whether flies fight like males or females can be switched by selectively manipulating genes of the sex determination hierarchy in male and female nervous systems. Here we extend these studies by demonstrating that changing the sex of cholinergic neurons in male fruit fly nervous systems via expression of the transformer gene increases the levels of aggression shown by the flies without altering the way the flies fight. Transformer manipulation in this way does not change phototaxis, geotaxis, locomotion or odor avoidance of the mutant males compared to controls. Cholinergic neurons must be feminized via this route during the late larval/early pupal stages of development to show the enhanced aggression phenotype. Other investigators have shown that this is the same time period during which sexually dimorphic patterns of behavior are specified in flies. Neurons that co-express fruitless and choline acetyl transferase are found in varying numbers within different clusters of fruitless-expressing neurons: together they make up approximately 10% of the pool of fruitless-expressing neurons in the brain and nerve cord.
PMCID: PMC2831085  PMID: 19556850
Drosophila; aggression; cholinergic neurons; transformer; feminization
10.  Analysis of Neuropeptide Expression and Localization in Adult Drosophila melanogaster Central Nervous System by Affinity Cell-Capture Mass Spectrometry 
Journal of proteome research  2009;8(3):1271-1284.
A combined approach using mass spectrometry, a novel neuron affinity capture technique, and Drosophila melanogaster genetic manipulation has been developed to characterize the expression and localization of neuropeptides in the adult D. melanogaster brain. In extract from the whole adult brain, 42 neuropeptides from 18 peptide families were sequenced. Neuropeptide profiling also was performed on targeted populations of cells which were enriched with immunoaffinity purification using a genetically expressed marker.
doi:10.1021/pr800601x
PMCID: PMC2693453  PMID: 19199706
neuropeptide; Drosophila; mass spectrometry; MALDI-TOF; biogenic amine; dopamine; serotonin
11.  Neurobiology of Escalated Aggression and Violence 
Psychopathological violence in criminals and intense aggression in fruit flies and rodents are studied with novel behavioral, neurobiological, and genetic approaches that characterize the escalation from adaptive aggression to violence. One goal is to delineate the type of aggressive behavior and its escalation with greater precision; second, the prefrontal cortex (PFC) and brainstem structures emerge as pivotal nodes in the limbic circuitry mediating escalated aggressive behavior. The neurochemical and molecular work focuses on the genes that enable invertebrate aggression in males and females and genes that are expressed or suppressed as a result of aggressive experiences in mammals. The fruitless gene, immediate early genes in discrete serotonin neurons, or sex chromosome genes identify sexually differentiated mechanisms for escalated aggression. Male, but not female, fruit flies establish hierarchical relationships in fights and learn from previous fighting experiences. By manipulating either the fruitless or transformer genes in the brains of male or female flies, patterns of aggression can be switched with males using female patterns and vice versa. Work with Sts or Sry genes suggests so far that other genes on the X chromosomes may have a more critical role in female mouse aggression. New data from feral rats point to the regulatory influences on mesocortical serotonin circuits in highly aggressive animals via feedback to autoreceptors and via GABAergic and glutamatergic inputs. Imaging data lead to the hypothesis that antisocial, violent, and psychopathic behavior may in part be attributable to impairments in some of the brain structures (dorsal and ventral PFC, amygdala, and angular gyrus) subserving moral cognition and emotion.
doi:10.1523/JNEUROSCI.3500-07.2007
PMCID: PMC2667097  PMID: 17978016
aggression; alcohol; genetics; learning; prefrontal cortex; serotonergic 1A receptor; serotonin; sex difference
12.  LOCALIZATION OF THE SITES OF γ-AMINOBUTYRIC ACID (GABA) UPTAKE IN LOBSTER NERVE-MUSCLE PREPARATIONS 
The Journal of Cell Biology  1971;49(1):75-89.
The principal sites of γ-aminobutyric acid (GABA) uptake in lobster nerve-muscle preparations have been determined with radioautographic techniques after binding of the amino acid to proteins by aldehyde fixation. Semiquantitative studies showed that about 30% of the radioactive GABA taken into the tissue was bound to protein by fixation. Both light and electron micrographs showed dense accumulations of label over Schwann and connective tissue cell cytoplasm; muscle was lightly labeled, but axons and terminals were almost devoid of label. The possible role of Schwann and connective tissue cells in the inactivation of GABA released from inhibitory axons is discussed.
PMCID: PMC2108210  PMID: 5555581

Results 1-12 (12)