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. 1996 May;143(1):331–344. doi: 10.1093/genetics/143.1.331

Courtship Anomalies Caused by Doublesex Mutations in Drosophila Melanogaster

A Villella 1, J C Hall 1
PMCID: PMC1207265  PMID: 8722785

Abstract

The role played by the sex-determining gene doublesex (dsx) and its influence on Drosophila courtship were examined. Against a background of subnormal male-like behavior that is reported to be an attribute of haplo-X flies homozygous for the original dsx mutation, and given that a sex-specific muscle is unaffected by genetic variation at this locus, analyses of several reproductive behaviors and control for genetic background effects indicated that XY dsx mutants are impaired in their willingness to court females. When they did court, certain behavioral actions were normal, including components of courtship song. However, these mutants never produced courtship humming sounds. Mature XY dsx flies elicited anomalously high levels of courtship; that this occurs merely because of a delay in imaginal development was experimentally discounted. The current analysis reconciled two ostensibly conflicting reports involving the courtship-stimulating qualities of this mutant type. Such experiments also uncovered a new behavioral anomaly: dsx mutations caused chromosomal males to court other males at abnormally high levels. These results are discussed from the perspective of doublesex's influence on internal tissues of adult Drosophila involved in the triggering and neural control of male- and female-like elements of courtship, reproductive pheromone production, or a combination of such factors.

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Selected References

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  1. An W., Wensink P. C. Integrating sex- and tissue-specific regulation within a single Drosophila enhancer. Genes Dev. 1995 Jan 15;9(2):256–266. doi: 10.1101/gad.9.2.256. [DOI] [PubMed] [Google Scholar]
  2. Baker B. S. Sex in flies: the splice of life. Nature. 1989 Aug 17;340(6234):521–524. doi: 10.1038/340521a0. [DOI] [PubMed] [Google Scholar]
  3. Burtis K. C., Baker B. S. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell. 1989 Mar 24;56(6):997–1010. doi: 10.1016/0092-8674(89)90633-8. [DOI] [PubMed] [Google Scholar]
  4. Burtis K. C. The regulation of sex determination and sexually dimorphic differentiation in Drosophila. Curr Opin Cell Biol. 1993 Dec;5(6):1006–1014. doi: 10.1016/0955-0674(93)90085-5. [DOI] [PubMed] [Google Scholar]
  5. Coschigano K. T., Wensink P. C. Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes Dev. 1993 Jan;7(1):42–54. doi: 10.1101/gad.7.1.42. [DOI] [PubMed] [Google Scholar]
  6. Currie D. A., Bate M. Innervation is essential for the development and differentiation of a sex-specific adult muscle in Drosophila melanogaster. Development. 1995 Aug;121(8):2549–2557. doi: 10.1242/dev.121.8.2549. [DOI] [PubMed] [Google Scholar]
  7. Duncan I. W., Kaufman T. C. Cytogenic analysis of chromosome 3 in Drosophila melanogaster: mapping of the proximal portion of the right arm. Genetics. 1975 Aug;80(4):733–752. doi: 10.1093/genetics/80.4.733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gailey D. A., Hall J. C. Behavior and cytogenetics of fruitless in Drosophila melanogaster: different courtship defects caused by separate, closely linked lesions. Genetics. 1989 Apr;121(4):773–785. doi: 10.1093/genetics/121.4.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gailey D. A., Taylor B. J., Hall J. C. Elements of the fruitless locus regulate development of the muscle of Lawrence, a male-specific structure in the abdomen of Drosophila melanogaster adults. Development. 1991 Nov;113(3):879–890. doi: 10.1242/dev.113.3.879. [DOI] [PubMed] [Google Scholar]
  10. Hall J. C. The mating of a fly. Science. 1994 Jun 17;264(5166):1702–1714. doi: 10.1126/science.8209251. [DOI] [PubMed] [Google Scholar]
  11. Heisenberg M., Heusipp M., Wanke C. Structural plasticity in the Drosophila brain. J Neurosci. 1995 Mar;15(3 Pt 1):1951–1960. doi: 10.1523/JNEUROSCI.15-03-01951.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hotta Y., Benzer S. Courtship in Drosophila mosaics: sex-specific foci for sequential action patterns. Proc Natl Acad Sci U S A. 1976 Nov;73(11):4154–4158. doi: 10.1073/pnas.73.11.4154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jallon J. M. A few chemical words exchanged by Drosophila during courtship and mating. Behav Genet. 1984 Sep;14(5):441–478. doi: 10.1007/BF01065444. [DOI] [PubMed] [Google Scholar]
  14. Jallon J. M., Hotta Y. Genetic and behavioral studies of female sex appeal in Drosophila. Behav Genet. 1979 Jul;9(4):257–275. doi: 10.1007/BF01068205. [DOI] [PubMed] [Google Scholar]
  15. Kulkarni S. J., Hall J. C. Behavioral and cytogenetic analysis of the cacophony courtship song mutant and interacting genetic variants in Drosophila melanogaster. Genetics. 1987 Mar;115(3):461–475. doi: 10.1093/genetics/115.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kyriacou C. P., van den Berg M. J., Hall J. C. Drosophila courtship song cycles in normal and period mutant males revisited. Behav Genet. 1990 Sep;20(5):617–644. doi: 10.1007/BF01065875. [DOI] [PubMed] [Google Scholar]
  17. Lawrence P. A., Johnston P. The muscle pattern of a segment of Drosophila may be determined by neurons and not by contributing myoblasts. Cell. 1986 May 23;45(4):505–513. doi: 10.1016/0092-8674(86)90282-5. [DOI] [PubMed] [Google Scholar]
  18. McKeown M., Madigan S. J. Sex determination and differentiation in invertebrates: Drosophila and Caenorhabditis elegans. Curr Opin Cell Biol. 1992 Dec;4(6):948–954. doi: 10.1016/0955-0674(92)90123-t. [DOI] [PubMed] [Google Scholar]
  19. McRobert S. P., Tompkins L. The effect of transformer, doublesex and intersex mutations on the sexual behavior of Drosophila melanogaster. Genetics. 1985 Sep;111(1):89–96. doi: 10.1093/genetics/111.1.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Neumann E. K., Wheeler D. A., Bernstein A. S., Burnside J. W., Hall J. C. Artificial neural network classification of Drosophila courtship song mutants. Biol Cybern. 1992;66(6):485–496. doi: 10.1007/BF00204113. [DOI] [PubMed] [Google Scholar]
  21. Shorey H. H., Bartell R. J. Role of a volatile female sex pheromone in stimulating male courtship behaviour in Drosophila melanogaster. Anim Behav. 1970 Feb;18(1):159–164. doi: 10.1016/0003-3472(70)90085-0. [DOI] [PubMed] [Google Scholar]
  22. Siegel R. W., Hall J. C., Gailey D. A., Kyriacou C. P. Genetic elements of courtship in Drosophila: mosaics and learning mutants. Behav Genet. 1984 Sep;14(5):383–410. doi: 10.1007/BF01065442. [DOI] [PubMed] [Google Scholar]
  23. Taylor B. J. Differentiation of a male-specific muscle in Drosophila melanogaster does not require the sex-determining genes doublesex or intersex. Genetics. 1992 Sep;132(1):179–191. doi: 10.1093/genetics/132.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Taylor B. J., Truman J. W. Commitment of abdominal neuroblasts in Drosophila to a male or female fate is dependent on genes of the sex-determining hierarchy. Development. 1992 Mar;114(3):625–642. doi: 10.1242/dev.114.3.625. [DOI] [PubMed] [Google Scholar]
  25. Taylor B. J., Villella A., Ryner L. C., Baker B. S., Hall J. C. Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev Genet. 1994;15(3):275–296. doi: 10.1002/dvg.1020150309. [DOI] [PubMed] [Google Scholar]
  26. Technau G. M. Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J Neurogenet. 1984 Apr;1(2):113–126. doi: 10.3109/01677068409107077. [DOI] [PubMed] [Google Scholar]
  27. Tompkins L., Hall J. C. Identification of Brain Sites Controlling Female Receptivity in Mosaics of DROSOPHILA MELANOGASTER. Genetics. 1983 Feb;103(2):179–195. doi: 10.1093/genetics/103.2.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wang X., Sun B., Yasuyama K., Salvaterra P. M. Biochemical analysis of proteins recognized by anti-HRP antibodies in Drosophila melanogaster: identification and characterization of neuron specific and male specific glycoproteins. Insect Biochem Mol Biol. 1994 Mar;24(3):233–242. doi: 10.1016/0965-1748(94)90002-7. [DOI] [PubMed] [Google Scholar]
  29. Wheeler D. A., Kulkarni S. J., Gailey D. A., Hall J. C. Spectral analysis of courtship songs in behavioral mutants of Drosophila melanogaster. Behav Genet. 1989 Jul;19(4):503–528. doi: 10.1007/BF01066251. [DOI] [PubMed] [Google Scholar]
  30. van Swinderen B., Hall J. C. Analysis of conditioned courtship in dusky-Andante rhythm mutants of Drosophila. Learn Mem. 1995 Mar-Apr;2(2):49–61. doi: 10.1101/lm.2.2.49. [DOI] [PubMed] [Google Scholar]
  31. von Schilcher F. A mutation which changes courtship song in Drosophila melanogaster. Behav Genet. 1977 May;7(3):251–259. doi: 10.1007/BF01066278. [DOI] [PubMed] [Google Scholar]

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