A subset of octopaminergic neurons are important for Drosophila aggression

Aggression is an innate behavior that is important for animal survival and evolution. We examined the molecular and cellular mechanisms underlying aggression in Drosophila. Reduction of the neurotransmitter octopamine, the insect equivalent of norepinephrine, decreased aggression in both males and females. Mutants lacking octopamine did not initiate fighting and did not fight other flies, although they still provoked other flies to fight themselves. Mutant males lost to the wild-type males in fighting and in competing for copulation with females. Enhanced octopaminergic signaling increased aggression in socially grouped flies, but not in socially isolated flies. We carried out genetic rescue experiments that revealed the functional importance of neuronal octopamine and identified a small subset of octopaminergic neurons in the suboesophageal ganglion as being important for aggression.

[1]  C. Darwin The Descent of Man and Selection in Relation to Sex: INDEX , 1871 .

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

[3]  J. P. Scott GENETIC DIFFERENCES IN THE SOCIAL BEHAVIOR OF INBRED STRAINS OF MICE , 1942 .

[4]  M. E. Jacobs Influence of Light on Mating of Drosophila Melanogaster , 1960 .

[5]  M. Dow,et al.  Aggression and mating success in Drosophila melanogaster , 1975, Nature.

[6]  M. E. Jacobs Influence of beta-alanine on mating and territorialism in Drosophila melanogaster. , 1978, Behavior genetics.

[7]  M. E. Jacobs Influence ofβ-alanine on mating and territorialism inDrosophila melanogaster , 1978 .

[8]  R. Harris-Warrick,et al.  Serotonin and Octopamine Produce Opposite Postures in Lobsters , 1980, Science.

[9]  A. Hoffmann Territorial encounters between Drosophila males of different sizes , 1987, Animal Behaviour.

[10]  J. C. Hall,et al.  Behavioral and cytogenetic analysis of the cacophony courtship song mutant and interacting genetic variants in Drosophila melanogaster. , 1987, Genetics.

[11]  Ary A. Hoffmann,et al.  A laboratory study of male territoriality in the sibling species Drosophila melanogaster and D. simulans , 1987, Animal Behaviour.

[12]  E. Kravitz Hormonal control of behavior: amines and the biasing of behavioral output in lobsters. , 1988, Science.

[13]  A. Hoffmann,et al.  Selection for territoriality in Drosophila melanogaster: correlated responses in mating success and other fitness components , 1989, Animal Behaviour.

[14]  A. Hoffmann Geographic variation in the territorial success ofDrosophila melanogaster males , 1989, Behavior Genetics.

[15]  A. Hoffmann,et al.  Territoriality in Drosophila melanogaster as a conditional strategy , 1990, Animal Behaviour.

[16]  M. Nelen,et al.  Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. , 1993, Science.

[17]  R R Hoy,et al.  The role of neurohormonal octopamine during 'fight or flight' behaviour in the field cricket Gryllus bimaculatus. , 1995, The Journal of experimental biology.

[18]  T. Mackay,et al.  Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster. , 1996, Genetics.

[19]  P T Barnes,et al.  Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. , 1997, Genetics.

[20]  D. H. Edwards,et al.  Serotonin, social status and aggression , 1997, Current Opinion in Neurobiology.

[21]  M. Scheinin,et al.  Adrenergic α2C-Receptors Modulate the Acoustic Startle Reflex, Prepulse Inhibition, and Aggression in Mice , 1998, The Journal of Neuroscience.

[22]  K. Schildberger,et al.  The fight and flight responses of crickets depleted of biogenic amines. , 2000, Journal of neurobiology.

[23]  T. Kitamoto Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. , 2001, Journal of neurobiology.

[24]  Y. Kidokoro,et al.  Aggressive behaviours of female Drosophila melanogaster are influenced by their social experience and food resources , 2002 .

[25]  T. Kitamoto Conditional disruption of synaptic transmission induces male–male courtship behavior in Drosophila , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[26]  B. Brembs,et al.  Drosophila as a new model organism for the neurobiology of aggression? , 2002, The Journal of experimental biology.

[27]  E. Kravitz,et al.  Fighting fruit flies: A model system for the study of aggression , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[28]  H. Amrein,et al.  A Putative Drosophila Pheromone Receptor Expressed in Male-Specific Taste Neurons Is Required for Efficient Courtship , 2003, Neuron.

[29]  M. Heisenberg,et al.  Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila , 2003, The Journal of Neuroscience.

[30]  M. Monastirioti Distinct octopamine cell population residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogaster. , 2003, Developmental biology.

[31]  E. Kravitz,et al.  Gender-selective patterns of aggressive behavior in Drosophila melanogaster. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Ferveur,et al.  Social experience and pheromonal perception can change male–male interactions in Drosophila melanogaster , 2005, Journal of Experimental Biology.

[33]  A. Hoffmann The influence of age and experience with conspecifics on territorial behavior inDrosophila melanogaster , 2005, Journal of Insect Behavior.

[34]  T. Roeder Tyramine and octopamine: ruling behavior and metabolism. , 2005, Annual review of entomology.

[35]  J. Hirsh,et al.  Two Functional but Noncomplementing Drosophila Tyrosine Decarboxylase Genes , 2005, Journal of Biological Chemistry.

[36]  J. Rillich,et al.  Octopamine and Experience-Dependent Modulation of Aggression in Crickets , 2005, The Journal of Neuroscience.

[37]  Brooke N. Bourdélat-Parks,et al.  Genetic reduction of noradrenergic function alters social memory and reduces aggression in mice , 2005, Behavioural Brain Research.

[38]  M. Nitabach,et al.  Functional Dissection of a Neuronal Network Required for Cuticle Tanning and Wing Expansion in Drosophila , 2006, The Journal of Neuroscience.

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

[40]  R. Greenspan,et al.  Molecular analysis of flies selected for aggressive behavior , 2006, Nature Genetics.

[41]  T. Mackay,et al.  Quantitative Genomics of Aggressive Behavior in Drosophila melanogaster , 2006, PLoS genetics.

[42]  Paul J Shaw,et al.  Waking Experience Affects Sleep Need in Drosophila , 2006, Science.

[43]  Ralph J Greenspan,et al.  Serotonin and neuropeptide F have opposite modulatory effects on fly aggression , 2007, Nature Genetics.

[44]  E. Kravitz,et al.  Modulation of Drosophila male behavioral choice , 2007, Proceedings of the National Academy of Sciences.

[45]  Pietro Perona,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A common genetic target for environmental and heritable influences on aggressiveness in Drosophila , 2008 .

[46]  M. Heisenberg,et al.  Octopamine in Male Aggression of Drosophila , 2008, Current Biology.