Mutant studies of aggression in Drosophila

Summary

Principal Investigator: Edward Kravitz
Affiliation: Harvard University
Country: USA
Abstract: DESCRIPTION (provided by applicant): Aggression is a complex behavior expressed in many different social contexts. Often abused, yet essential for the survival of organisms, little is known of the biological roots of this behavior. While model systems may not duplicate aggression in all of its many human manifestations, they can be highly informative about: the relative importance of genes, hormones and experience in laying down patterns of aggression in nervous systems;detailing the neural circuitry involved;and addressing questions of how animals choose among the varied complex behaviors available within their behavioral repertoires. It is the last two matters that are the major focus of the present application. In recent years, the Kravitz laboratory has established a fruit fly model of aggression making this important behavior available for experimental analysis in an organism that is highly suitable for genetic analysis. With fruit flies aggression is complex and is shown by both males and females, the animals engage in many other inter-related behaviors, and the behaviors can be quantitatively analyzed. In addition, however, the genome has been sequenced and incredibly powerful methods are available that allow experimental manipulations to be performed with fruit flies that cannot yet even be approximated in most other animal model systems. Recently, it has been found that the same gene that determines who flies court also determines whether flies fight like males or females. The present application extends these studies and has the following Specific Aims: I. To explore decision-making between courtship and aggression, two sexually dimorphic patterns of behavior in flies, by mapping and manipulating the fruitless/doublesex-associated circuitry within the subesophageal ganglion (SOG), the taste center in fruit fly brains;II. To map the distribution of receptors for amines and peptides associated with the SOG circuitry;and III. To introduce genes into neurons that can alter the function of these nerve cells in behaving animals and to begin to address the question of how the same neurons differ in male and female animals. These studies use a wide variety of state-of-the-art genetic, behavioral and anatomical methods in exploring these Aims. For example, in collaborative studies with the Chiang laboratory in Taiwan, neuronal maps will be made that will allow examination in great detail of the possible connections between individual neurons involved in courtship and aggression. The focus will be to define the brain circuitry important in aggression and courtship at much higher levels of resolution than are now available, and then to ask how that circuitry gets established in fly brains and how animals choose between behavioral responses when conflict situations arise. PUBLIC HEALTH RELEVANCE: All organisms, including humans, must be capable of rapidly evaluating social situations and selecting proper responses from what may be a wide variety of possible behavioral choices. Such selections must be made correctly in order to allow the survival of organisms both as individuals and as species. How organisms make such choices and how patterns of innate behavior of great complexity get established in nervous systems are not well understood, and are the theme of this application.
Funding Period: 2009-09-30 - 2011-08-31
more information: NIH RePORT

Top Publications

  1. pmc Octopamine neuromodulation regulates Gr32a-linked aggression and courtship pathways in Drosophila males
    Jonathan C Andrews
    Center for Structural and Functional Neuroscience, University of Montana, Missoula, Montana, United States of America
    PLoS Genet 10:e1004356. 2014
  2. pmc Single dopaminergic neurons that modulate aggression in Drosophila
    Olga V Alekseyenko
    Department of Neurobiology, Harvard Medical School, Boston, MA 02115, USA
    Proc Natl Acad Sci U S A 110:6151-6. 2013
  3. pmc Neural circuitry underlying Drosophila female postmating behavioral responses
    Carolina Rezaval
    Department of Physiology, Anatomy and Genetics, University of Oxford, Sherrington Building, Parks Road, Oxford OX1 3PT, UK
    Curr Biol 22:1155-65. 2012
  4. pmc Octopamine neuromodulatory effects on a social behavior decision-making network in Drosophila males
    Sarah J Certel
    Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, United States of America
    PLoS ONE 5:e13248. 2010
  5. pmc Sound production during agonistic behavior of male Drosophila melanogaster
    Thorin Jonsson
    Institute for Zoology, University of Gottingen, Gottingen, Germany
    Fly (Austin) 5:29-38. 2011
  6. pmc A single social defeat reduces aggression in a highly aggressive strain of Drosophila
    Jill K M Penn
    Department of Neurobiology, Harvard Medical School, Boston, MA 02115, USA
    Proc Natl Acad Sci U S A 107:12682-6. 2010
  7. pmc Targeted manipulation of serotonergic neurotransmission affects the escalation of aggression in adult male Drosophila melanogaster
    Olga V Alekseyenko
    Neurobiology Department, Harvard Medical School, Boston, Massachusetts, USA
    PLoS ONE 5:e10806. 2010
  8. ncbi Field-based ion generation from microscale emitters on natural and artificial objects for atmospheric pressure mass spectrometry
    Alexander Pirkl
    Integrierte Funktionelle Genomik, Interdisziplinäres Zentrum für Klinische Forschung, Westfalische Wilhelms Universitat, Munster, Germany
    Anal Bioanal Chem 397:3311-6. 2010
  9. pmc A new male sex pheromone and novel cuticular cues for chemical communication in Drosophila
    Joanne Y Yew
    Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
    Curr Biol 19:1245-54. 2009
  10. pmc Feminizing cholinergic neurons in a male Drosophila nervous system enhances aggression
    Sibu Mundiyanapurath
    Medical Faculty Heidelberg, University of Heidelberg, Heidelberg, Germany
    Fly (Austin) 3:179-84. 2009

Scientific Experts

  • Sarah J Certel
  • Olga V Alekseyenko
  • Joanne Y Yew
  • Kathleen K Siwicki
  • Geoffrey K Ganter
  • Edward A Kravitz
  • Yick Bun Chan
  • Jonathan C Andrews
  • Carolina Rezaval
  • Adelaine K W Leung
  • Thorin Jonsson
  • Jill K M Penn
  • Alexander Pirkl
  • Sibu Mundiyanapurath
  • Eleftheria Vrontou
  • María Paz Fernández
  • Michael P Kavanaugh
  • Qin Yu
  • Greg P Leary
  • Hania J Pavlou
  • Stephen F Goodwin
  • Anthony J Dornan
  • Ralf Heinrich
  • Michael F Zito
  • Simone König
  • Klaus Dreisewerd
  • Steven P Nilsen
  • Barry J Dickson
  • Ebru Demir

Detail Information

Publications18

  1. pmc Octopamine neuromodulation regulates Gr32a-linked aggression and courtship pathways in Drosophila males
    Jonathan C Andrews
    Center for Structural and Functional Neuroscience, University of Montana, Missoula, Montana, United States of America
    PLoS Genet 10:e1004356. 2014
    ..Our findings demonstrate that octopaminergic neuromodulatory neurons function as early as a second-order step in this chemosensory-driven male social behavior pathway...
  2. pmc Single dopaminergic neurons that modulate aggression in Drosophila
    Olga V Alekseyenko
    Department of Neurobiology, Harvard Medical School, Boston, MA 02115, USA
    Proc Natl Acad Sci U S A 110:6151-6. 2013
    ..These data suggest that the two types of dopaminergic neurons may influence aggression through interactions in the central complex region of the brain involving two different DA receptor subtypes...
  3. pmc Neural circuitry underlying Drosophila female postmating behavioral responses
    Carolina Rezaval
    Department of Physiology, Anatomy and Genetics, University of Oxford, Sherrington Building, Parks Road, Oxford OX1 3PT, UK
    Curr Biol 22:1155-65. 2012
    ..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...
  4. pmc Octopamine neuromodulatory effects on a social behavior decision-making network in Drosophila males
    Sarah J Certel
    Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, United States of America
    PLoS ONE 5:e13248. 2010
    ..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...
  5. pmc Sound production during agonistic behavior of male Drosophila melanogaster
    Thorin Jonsson
    Institute for Zoology, University of Gottingen, Gottingen, Germany
    Fly (Austin) 5:29-38. 2011
    ....
  6. pmc A single social defeat reduces aggression in a highly aggressive strain of Drosophila
    Jill K M Penn
    Department of Neurobiology, Harvard Medical School, Boston, MA 02115, USA
    Proc Natl Acad Sci U S A 107:12682-6. 2010
    ..Lastly, females were more likely to copulate with males from the nonselected parent line than with the hyperaggressive strain...
  7. pmc Targeted manipulation of serotonergic neurotransmission affects the escalation of aggression in adult male Drosophila melanogaster
    Olga V Alekseyenko
    Neurobiology Department, Harvard Medical School, Boston, Massachusetts, USA
    PLoS ONE 5:e10806. 2010
    ..By separately manipulating 5HT- and DA- neuron systems, we collected evidence demonstrating a direct role for 5HT in the escalation of aggression in Drosophila...
  8. ncbi Field-based ion generation from microscale emitters on natural and artificial objects for atmospheric pressure mass spectrometry
    Alexander Pirkl
    Integrierte Funktionelle Genomik, Interdisziplinäres Zentrum für Klinische Forschung, Westfalische Wilhelms Universitat, Munster, Germany
    Anal Bioanal Chem 397:3311-6. 2010
    ..Cuticular hairs serve as electric field-enhancing structures and play a key role in ion generation. Artificial emitters such as graphite whiskers or sharp metal tips replicate this effect...
  9. pmc A new male sex pheromone and novel cuticular cues for chemical communication in Drosophila
    Joanne Y Yew
    Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
    Curr Biol 19:1245-54. 2009
    ....
  10. pmc Feminizing cholinergic neurons in a male Drosophila nervous system enhances aggression
    Sibu Mundiyanapurath
    Medical Faculty Heidelberg, University of Heidelberg, Heidelberg, Germany
    Fly (Austin) 3:179-84. 2009
    ....
  11. pmc Fruitless, doublesex and the genetics of social behavior in Drosophila melanogaster
    Kathleen K Siwicki
    Department of Biology, Swarthmore College, 500 College Aveune, Swarthmore, PA 19081, USA
    Curr Opin Neurobiol 19:200-6. 2009
    ..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...
  12. pmc Analysis of neuropeptide expression and localization in adult drosophila melanogaster central nervous system by affinity cell-capture mass spectrometry
    Joanne Y Yew
    Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115, USA
    J Proteome Res 8:1271-84. 2009
    ..Neuropeptide profiling also was performed on targeted populations of cells which were enriched with immunoaffinity purification using a genetically expressed marker...
  13. pmc Cuticular hydrocarbon analysis of an awake behaving fly using direct analysis in real-time time-of-flight mass spectrometry
    Joanne Y Yew
    Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
    Proc Natl Acad Sci U S A 105:7135-40. 2008
    ..This method provides near-instantaneous analysis of an individual animal's chemical profile in parallel with behavioral studies and could be extended to other models of pheromone-mediated behavior...
  14. pmc Specific subgroups of FruM neurons control sexually dimorphic patterns of aggression in Drosophila melanogaster
    Yick Bun Chan
    Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
    Proc Natl Acad Sci U S A 104:19577-82. 2007
    ....
  15. pmc Modulation of Drosophila male behavioral choice
    Sarah J Certel
    Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
    Proc Natl Acad Sci U S A 104:4706-11. 2007
    ..These results provide insight into how complex social behaviors are coordinated in the nervous system and suggest a role for neuromodulators in the functioning of male-specific circuitry relating to behavioral choice...
  16. ncbi Increased male-male courtship in ecdysone receptor deficient adult flies
    Geoffrey K Ganter
    Department of Biological Sciences, University of New England, 11 Hills Beach Road, Biddeford, ME 04005, USA
    Behav Genet 37:507-12. 2007
    ..EcR-deficient males courted wildtype males and females, but were not courted by wildtype males. These results suggest that the ecdysone steroid hormone system may have a role in courtship initiation by adult male fruit flies...
  17. ncbi fruitless regulates aggression and dominance in Drosophila
    Eleftheria Vrontou
    Research Institute of Molecular Pathology, Dr Bohr Gasse 7, A 1030 Vienna, Austria
    Nat Neurosci 9:1469-71. 2006
    ..Here we show that sex-specific splicing of the fruitless gene plays a critical role in determining who and how a fly fights, and whether a dominance relationship forms...