Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Jun 6;92(12):5525–5529. doi: 10.1073/pnas.92.12.5525

Misexpression of the white (w) gene triggers male-male courtship in Drosophila.

S D Zhang 1, W F Odenwald 1
PMCID: PMC41728  PMID: 7777542

Abstract

We report here that the general ectopic expression of a tryptophan/guanine transmembrane transporter gene, white (w), induces male-male courtship in Drosophila. Activation of a hsp-70/miniwhite (mini-w) transgene in mature males results in a marked change in their sexual behavior such that they begin to vigorously court other mature males. In transformant populations containing equal numbers of both sexes, most males participate, thus forming male-male courtship chains, circles, and lariats. Mutations that ablate the w transgene function also abolish this inducible behavior. Female sexual behavior does not appear to be altered by ectopic w expression. By contrast, when exposed to an active homosexual courtship environment, non-transformant males alter their behavior and actively participate in the male-male chaining. These findings demonstrate that, in Drosophila, both genetic and environmental factors play a role in male sexual behavior.

Full text

PDF
5525

Images in this article

5526Fig. 1
on p.5526
5527Fig. 2
on p.5527
5527Fig. 3
on p.5527
5528Fig. 4
on p.5528

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Basler K., Siegrist P., Hafen E. The spatial and temporal expression pattern of sevenless is exclusively controlled by gene-internal elements. EMBO J. 1989 Aug;8(8):2381–2386. doi: 10.1002/j.1460-2075.1989.tb08367.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Dreesen T. D., Johnson D. H., Henikoff S. The brown protein of Drosophila melanogaster is similar to the white protein and to components of active transport complexes. Mol Cell Biol. 1988 Dec;8(12):5206–5215. doi: 10.1128/mcb.8.12.5206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Edgar B. A., O'Farrell P. H. The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2 by string. Cell. 1990 Aug 10;62(3):469–480. doi: 10.1016/0092-8674(90)90012-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ewart G. D., Cannell D., Cox G. B., Howells A. J. Mutational analysis of the traffic ATPase (ABC) transporters involved in uptake of eye pigment precursors in Drosophila melanogaster. Implications for structure-function relationships. J Biol Chem. 1994 Apr 8;269(14):10370–10377. [PubMed] [Google Scholar]
  5. Ferguson J., Henriksen S., Cohen H., Mitchell G., Barchas J., Dement W. "Hypersexuality" and behavioral changes in cats caused by administration of p-chlorophenylalanine. Science. 1970 Apr 24;168(3930):499–501. doi: 10.1126/science.168.3930.499. [DOI] [PubMed] [Google Scholar]
  6. Fjose A., Polito L. C., Weber U., Gehring W. J. Developmental expression of the white locus of Drosophila melanogaster. EMBO J. 1984 Sep;3(9):2087–2094. doi: 10.1002/j.1460-2075.1984.tb02095.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fratta W., Biggio G., Gessa G. L. Homosexual mounting behavior induced in male rats and rabbits by a tryptophan-free diet. Life Sci. 1977 Aug 1;21(3):379–383. doi: 10.1016/0024-3205(77)90518-5. [DOI] [PubMed] [Google Scholar]
  8. Gailey D. A., Jackson F. R., Siegel R. W. Male courtship in Drosophila: the conditioned response to immature males and its genetic control. Genetics. 1982 Dec;102(4):771–782. doi: 10.1093/genetics/102.4.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hall J. C. Courtship among males due to a male-sterile mutation in Drosophila melanogaster. Behav Genet. 1978 Mar;8(2):125–141. doi: 10.1007/BF01066870. [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. Hoyland V. J., Shillito E. E., Vogt M. The effect of parachlorophenylalanine on the behaviour of cats. Br J Pharmacol. 1970 Dec;40(4):659–667. doi: 10.1111/j.1476-5381.1970.tb10645.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Klemenz R., Weber U., Gehring W. J. The white gene as a marker in a new P-element vector for gene transfer in Drosophila. Nucleic Acids Res. 1987 May 26;15(10):3947–3959. doi: 10.1093/nar/15.10.3947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kreitman M. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature. 1983 Aug 4;304(5925):412–417. doi: 10.1038/304412a0. [DOI] [PubMed] [Google Scholar]
  14. Lefevre G., Jr, Wilkins M. D. Cytogenetic studies on the white locus in Drosophila melanogaster. Genetics. 1966 Jan;53(1):175–187. doi: 10.1093/genetics/53.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Levis R., O'Hare K., Rubin G. M. Effects of transposable element insertions on RNA encoded by the white gene of Drosophila. Cell. 1984 Sep;38(2):471–481. doi: 10.1016/0092-8674(84)90502-6. [DOI] [PubMed] [Google Scholar]
  16. Malicki J., Bogarad L. D., Martin M. M., Ruddle F. H., McGinnis W. Functional analysis of the mouse homeobox gene HoxB9 in Drosophila development. Mech Dev. 1993 Aug;42(3):139–150. doi: 10.1016/0925-4773(93)90003-g. [DOI] [PubMed] [Google Scholar]
  17. Mellerick D. M., Kassis J. A., Zhang S. D., Odenwald W. F. castor encodes a novel zinc finger protein required for the development of a subset of CNS neurons in Drosophila. Neuron. 1992 Nov;9(5):789–803. doi: 10.1016/0896-6273(92)90234-5. [DOI] [PubMed] [Google Scholar]
  18. Morgan T. H. SEX LIMITED INHERITANCE IN DROSOPHILA. Science. 1910 Jul 22;32(812):120–122. doi: 10.1126/science.32.812.120. [DOI] [PubMed] [Google Scholar]
  19. O'Connell P. O., Rosbash M. Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res. 1984 Jul 11;12(13):5495–5513. doi: 10.1093/nar/12.13.5495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. O'Hare K., Murphy C., Levis R., Rubin G. M. DNA sequence of the white locus of Drosophila melanogaster. J Mol Biol. 1984 Dec 15;180(3):437–455. doi: 10.1016/0022-2836(84)90021-4. [DOI] [PubMed] [Google Scholar]
  21. O'hare K., Levis R., Rubin G. M. Transcription of the white locus in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6917–6921. doi: 10.1073/pnas.80.22.6917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pepling M., Mount S. M. Sequence of a cDNA from the Drosophila melanogaster white gene. Nucleic Acids Res. 1990 Mar 25;18(6):1633–1633. doi: 10.1093/nar/18.6.1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pirrotta V., Bröckl C. Transcription of the Drosophila white locus and some of its mutants. EMBO J. 1984 Mar;3(3):563–568. doi: 10.1002/j.1460-2075.1984.tb01847.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pirrotta V., Steller H., Bozzetti M. P. Multiple upstream regulatory elements control the expression of the Drosophila white gene. EMBO J. 1985 Dec 16;4(13A):3501–3508. doi: 10.1002/j.1460-2075.1985.tb04109.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rubin G. M., Spradling A. C. Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res. 1983 Sep 24;11(18):6341–6351. doi: 10.1093/nar/11.18.6341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Spieth H. T. Courtship behavior in Drosophila. Annu Rev Entomol. 1974;19:385–405. doi: 10.1146/annurev.en.19.010174.002125. [DOI] [PubMed] [Google Scholar]
  27. Sullivan D. T., Bell L. A., Paton D. R., Sullivan M. C. Genetic and functional analysis of tryptophan transport in Malpighian tubules of Drosophila. Biochem Genet. 1980 Dec;18(11-12):1109–1130. doi: 10.1007/BF00484342. [DOI] [PubMed] [Google Scholar]
  28. Tearle R. G., Belote J. M., McKeown M., Baker B. S., Howells A. J. Cloning and characterization of the scarlet gene of Drosophila melanogaster. Genetics. 1989 Jul;122(3):595–606. doi: 10.1093/genetics/122.3.595. [DOI] [PMC free article] [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]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES