Behavior Genetics

, Volume 30, Issue 4, pp 263–275

A Newly Uncovered Phenotype Associated with the fruitless Gene of Drosophila melanogaster: Aggression-like Head Interactions Between Mutant Males

  • Gyunghee Lee
  • Jeffrey C. Hall
Article

Abstract

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.

Intermale interactions aggression sexual behavior fruitless, dissatisfaction, doublesex, and intersex mutants 

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REFERENCES

  1. 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.Google Scholar
  2. 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.Google Scholar
  3. Bredt, D. S., and Snyder, S. H. (1992). Nitric oxide, a novel neuronal messenger. Neuron 8:3–11.PubMedGoogle Scholar
  4. 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.PubMedGoogle Scholar
  5. 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.PubMedGoogle Scholar
  6. 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.PubMedGoogle Scholar
  7. Dow, M. A., and Schilcher, F. v. (1975). Aggression and mating success in Drosophila melanogaster. Nature 254:511–512.PubMedGoogle Scholar
  8. 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.PubMedGoogle Scholar
  9. 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.PubMedGoogle Scholar
  10. 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.PubMedGoogle Scholar
  11. 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.PubMedGoogle Scholar
  12. 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.PubMedGoogle Scholar
  13. 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.PubMedGoogle Scholar
  14. Goodwin, S. F. (1999). Molecular neurogenetics of sexual differentiation and behaviour. Curr. Opin. Neurobiol. 9:759–765.PubMedGoogle Scholar
  15. 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.PubMedGoogle Scholar
  16. Hall, J. C., (1978). Courtship among males due to a male-sterile mutation in Drosophila melanogaster. Behav. Genet. 8:125–141.PubMedGoogle Scholar
  17. Hall, J. C. (1994). The mating of a fly. Science 264:1702–1714.PubMedGoogle Scholar
  18. Hemmat, M., and Eggleston, P. (1988a). Competitive interactions in Drosophila melanogaster: Recurrent selection for aggression and response. J. Hered. 60:129–137.Google Scholar
  19. Hemmat, M., and Eggleston, P. (1988b). Competitive interactions in Drosophila melanogaster: Genetic variation for interference through media conditioning. J. Hered. 61:347–354.Google Scholar
  20. Hildreth, P. E. (1965). doublesex, a recessive gene that transforms both males and females of Drosophila into intersexes. Genetics 51:659–678.PubMedGoogle Scholar
  21. Hoffmann, A. A. (1989). Geographic variation in the territorial success of Drosophila melanogaster males. Behav. Genet. 19: 241–255.PubMedGoogle Scholar
  22. 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.PubMedGoogle Scholar
  23. Jacobs, M. E. (1978). Influence of β-alanine on mating and territorialism in Drosophila melanogaster. Behav. Genet. 8:487–502.PubMedGoogle Scholar
  24. 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.PubMedGoogle Scholar
  25. 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.PubMedGoogle Scholar
  26. Lande, R., and Kirkpatrick, M. (1988). Ecological speciation by sexual selection. J. Theoret. Biol. 133:85–98.Google Scholar
  27. 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.Google Scholar
  28. 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.PubMedGoogle Scholar
  29. 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.PubMedGoogle Scholar
  30. 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.PubMedGoogle Scholar
  31. 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.PubMedGoogle Scholar
  32. O'Kane, C. J., and Asztalos, Z. (1999). Sexual behavior: Courting dissatisfaction. Curr. Biol. 9:R289-R292.PubMedGoogle Scholar
  33. 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.Google Scholar
  34. Ringo, J., Kananen, M. K., and Wood, D. (1983). Aggression and mating success in three species of Drosophila. Z. Tierpsychol. 61:341–350.Google Scholar
  35. 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.PubMedGoogle Scholar
  36. Spieth, H. T. (1974). Courtship behavior in Drosophila. Annu. Rev. Entomol. 19:385–405.PubMedGoogle Scholar
  37. Spieth, H. T. (1981). Drosophila heteroneura and Drosophila silvestris: Head shapes, behavior, and evolution. Evolution 35:921–930.Google Scholar
  38. 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.PubMedGoogle Scholar
  39. Villella, A., and Hall, J. C. (1996). Courtship anomalies caused by doublesex mutations in Drosophila melanogaster. Genetics 143: 331–344.PubMedGoogle Scholar
  40. 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 147:1107–1130PubMedGoogle Scholar
  41. Yamamoto, D., and Nakano, Y. (1998). Genes for sexual behavior. Biochem. Biophys. Res. Commun. 246:1–6.Google Scholar
  42. Yamamoto, D., Jallon, J.-M., and Komatsu, A. (1997). Genetic dissection of sexual behavior in Drosophila melanogaster. Annu. Rev. Entomol. 42:551–585.PubMedGoogle Scholar
  43. 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.PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 2000

Authors and Affiliations

  • Gyunghee Lee
    • 1
  • Jeffrey C. Hall
    • 2
  1. 1.Department of BiologyBrandeis UniversityWaltham
  2. 2.Department of BiologyBrandeis UniversityWaltham

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