A Newly Uncovered Phenotype Associated with the fruitless Gene of Drosophila melanogaster: Aggression-like Head Interactions Between Mutant Males
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Male sexual behavior is regulated by the sex-determination hierarchy (SDH) in Drosophila melanogaster. The fruitless (fru) gene, one of the regulatory factors functioning downstream of other SDH factors, plays a prominent role in male sexual behavior. Here we demonstrate that fru mutations cause a previously unappreciated behavioral anomaly: high levels of head-to-head interactions between mutant males. These apparent confrontations between males are exhibited by all of the homozygous-viable fru mutants (expressing the effects of a given allele, among the four tested). Mutant dissatisfaction (dsf) males also exhibit this behavior at higher-than-normal levels, but it was barely displayed by doublesex or intersex mutants. For fru, a social component is involved in the head-interaction phenotype, while increasing age is a modifying factor for the behavior of dsf males. We suggest that head-to-head interactions, especially those performed by fru males, are instances of putative aggression analogous to those exhibited by wild-type males and that head interactions are, to an extent, operationally separable from courtship behavior.
- Boake, C. R. B., DeAngelis, M. P., and Andreadis, D. K. (1997). Is sexual selection and species recognition a continuum? Mating behavior of the stalk-eyed fly Drosophila heteroneura. Proc. Natl. Acad. Sci. USA 94:12442–12445.
- Boake, C. R. B., Price, D. K., and Andreadis, D. K. (1998). Inheritance of behavioural differences between two interfertile, sympatric species, Drosophila silvestris and D. heteroneura. Heredity 80: 642–650.
- Bredt, D. S., and Snyder, S. H. (1992). Nitric oxide, a novel neuronal messenger. Neuron 8:3–11.
- Burtis, K. C., and Baker, B. S. (1989). Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNA's encoding related sex-specific polypeptides. Cell 56: 997–1010.
- Chase, B. A., and Baker, B. S., (1995). A genetic analysis of intersex, a gene regulating sexual differentiation in Drosophila melanogaster females. Genetics 139:1649–1661.
- Demas, G. E., Eliasson, M. J., Dawson, T. M., Dawson, V. L., Kriegsfeld, L. J., Nelson, R. J., and Snyder, S. H. (1997). Inhibition of neuronal nitric oxide synthase increases aggressive behavior in mice. Mol. Med. 3:610–616.
- Dow, M. A., and Schilcher, F. v. (1975). Aggression and mating success in Drosophila melanogaster. Nature 254:511–512.
- Ferveur, J.-F., Störtkuhl, K. F., Stocker, R. F., and Greenspan, R. J. (1995). Genetic feminization of brain structures and changed sexual orientation in male Drosophila melanogaster. Science 267:902–905.
- Ferveur, J.-F., Savarit, F., O'Kane, C. J., Sureau, G., Greenspan, R. J., and Jallon, J.-M. (1997). Genetic feminization of pheromones and its behavioral consequences in Drosophila males. Science 276:1555–1558.
- Finley, K. D., Taylor, B. J., Milstein, M., and McKeown, M. (1997). dissatisfaction, a gene involved in sex-specific behavior and neural development of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 94:913–918.
- Finley, K. D., Edeen, P. T., Foss, M., Gross, E., Ghbeish, N., Palmer, R. H., Taylor, B. J., and McKeown, M. (1998). dissatisfaction encodes a Tailless-like nuclear receptor expressed in a subset of CNS neurons controlling Drosophila sexual behavior. Neuron 21:1363–1374.
- Gailey, D. A., and Hall, J. C. (1989). Behavior and cytogenetics of fruitless in Drosophila melanogaster: Different courtship defects caused by separate closely linked lesions. Genetics 121:773–785.
- Garthwaite, J., Charles, S. L., and Chess-Williams, R. (1988). Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336:385–388.
- Goodwin, S. F. (1999). Molecular neurogenetics of sexual differentiation and behaviour. Curr. Opin. Neurobiol. 9:759–765.
- Goodwin, S. F., Taylor, B. J., Villella, A., Foss, M., Ryner, L. C., Baker, B. S., and Hall, J. C. (2000). Mutations in the fruitless gene of Drosophila melanogaster causing aberrant splicing or altered spatial distribution of fru's sex-specific expression patterns. Genetics 154:725–745.
- Hall, J. C., (1978). Courtship among males due to a male-sterile mutation in Drosophila melanogaster. Behav. Genet. 8:125–141.
- Hall, J. C. (1994). The mating of a fly. Science 264:1702–1714.
- Hemmat, M., and Eggleston, P. (1988a). Competitive interactions in Drosophila melanogaster: Recurrent selection for aggression and response. J. Hered. 60:129–137.
- Hemmat, M., and Eggleston, P. (1988b). Competitive interactions in Drosophila melanogaster: Genetic variation for interference through media conditioning. J. Hered. 61:347–354.
- Hildreth, P. E. (1965). doublesex, a recessive gene that transforms both males and females of Drosophila into intersexes. Genetics 51:659–678.
- Hoffmann, A. A. (1989). Geographic variation in the territorial success of Drosophila melanogaster males. Behav. Genet. 19: 241–255.
- Huber, R., Smith, K., Delago, A., Isaksson, K., and Kravitz, E. A. (1997). Serotonin and aggressive motivation in crustaceans: Altering the decision to retreat. Proc. Natl. Acad. Sci. USA 94:5939–5942.
- Jacobs, M. E. (1978). Influence of β-alanine on mating and territorialism in Drosophila melanogaster. Behav. Genet. 8:487–502.
- Kravitz, E. A. (2000). Serotonin and aggression: Insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior. J. Comp. Physiol. A 186:221–238.
- Kriegsfeld, L. J., Dawson, T. M., Dawson, V. L., Nelson, R. J., and Snyder, S. H. (1997). Aggressive behavior in male mice lacking the gene for neuronal nitric oxide synthase requires testosterone. Brain Res. 769:66–70.
- Lande, R., and Kirkpatrick, M. (1988). Ecological speciation by sexual selection. J. Theoret. Biol. 133:85–98.
- Lee, G., and Hall, J. C. (2000). Abnormalities of male-specific FRU protein and serotonin expression in the central nervous system of fruitless mutants in Drosophila. J. Neurosci., in press.
- Lyons, W. E., Mamounas, L. A., Ricaurte, G. A., Coppola, V., Reid, S. W., Bora, S. H., Wihler, C., Koliatsos, V. E., and Tessarollo, L. (1999). Brain-derived neurotrophic factor-deficient mice develop aggressiveness and hyperphagia in conjunction with brain serotonergic abnormalities. Proc. Natl. Acad. Sci. USA 96:15239–15244.
- McRobert, S. P., and Tompkins, L. (1985). The effect of transformer, doublesex, and intersex mutations on the sexual behavior of Drosophila melanogaster. Genetics 111:89–96.
- Nelson, R. J., Demas, G. E., Huang, P. L., Fishman, M. C., Dawson, V. L., Dawson, T. M., and Snyder, S. H. (1995). Behavioural abnormalities in male mice lacking neuronal nitric oxide synthase. Nature 378:383–386.
- O'Dell, K. M. C., Armstrong, J. D., Yang, M. Y., and Kaiser, K. (1995). Functional dissection of the Drosophila mushroom bodies by selective feminization of genetically defined subcompartments. Neuron 15:55–61.
- O'Kane, C. J., and Asztalos, Z. (1999). Sexual behavior: Courting dissatisfaction. Curr. Biol. 9:R289-R292.
- Paillette, M., Ikeda, H., and Jallon, J.-M. (1991). A new acoustic signal of the fruit-flies Drosophila simulans and D. melanogaster. Bioacoustics 3:247–254.
- Ringo, J., Kananen, M. K., and Wood, D. (1983). Aggression and mating success in three species of Drosophila. Z. Tierpsychol. 61:341–350.
- Ryner, L. C., Goodwin, S. F., Castrillon, D. H., Anand, A., Villella, A., Baker, B. S., Hall, J. C., and Wasserman, S. A. (1996). Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87:1079–1089.
- Spieth, H. T. (1974). Courtship behavior in Drosophila. Annu. Rev. Entomol. 19:385–405.
- Spieth, H. T. (1981). Drosophila heteroneura and Drosophila silvestris: Head shapes, behavior, and evolution. Evolution 35:921–930.
- Tarchalska, B., Kostowski, W., Markowska, L., and Markiewicz, L. (1975). On the role of serotonin in aggressive behaviour of ants Genus formica. Pol. J. Pharmacol. Pharm. 27(Suppl.):237–239.
- Villella, A., and Hall, J. C. (1996). Courtship anomalies caused by doublesex mutations in Drosophila melanogaster. Genetics 143: 331–344.
- Villella, A., Gailey, D. A., Berwald, B., Ohshima, S., Barnes, P. T., and Hall, J. C. (1997). Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics 147:1107–1130
- Yamamoto, D., and Nakano, Y. (1998). Genes for sexual behavior. Biochem. Biophys. Res. Commun. 246:1–6.
- Yamamoto, D., Jallon, J.-M., and Komatsu, A. (1997). Genetic dissection of sexual behavior in Drosophila melanogaster. Annu. Rev. Entomol. 42:551–585.
- Yamamoto, D., Fujitani, K., Usui, K., Ito, H., and Nakano, Y. (1998). From behavior to development: Genes for sexual behavioral define the neuronal sexual switch in Drosophila. Mech. Dev. 73:135–146.
- A Newly Uncovered Phenotype Associated with the fruitless Gene of Drosophila melanogaster: Aggression-like Head Interactions Between Mutant Males
Volume 30, Issue 4 , pp 263-275
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- Intermale interactions
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- fruitless, dissatisfaction, doublesex, and intersex mutants