Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Identification of genes involved in Drosophila melanogaster geotaxis, a complex behavioral trait

Nature Genetics volume 31, pages 349–353 (2002)Cite this article

Abstract

Identifying the genes involved in polygenic traits has been difficult. In the 1950s and 1960s, laboratory selection experiments for extreme geotaxic behavior in fruit flies established for the first time that a complex behavioral trait has a genetic basis. But the specific genes responsible for the behavior have never been identified using this classical model. To identify the individual genes involved in geotaxic response, we used cDNA microarrays to identify candidate genes and assessed fly lines mutant in these genes for behavioral confirmation. We have thus determined the identities of several genes that contribute to the complex, polygenic behavior of geotaxis.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Comparisons of geotaxis scores of Hi5 and Lo geotaxic lines and wildtype CS lines in a nine-choice maze.
Figure 2: Difference in average geotaxis scores between a tested genotype and CS.

Similar content being viewed by others

References

  1. Erlenmeyer-Kimling, L. & Hirsch, J. Measurement of the relations between chromosomes and behavior. Science 134, 1068–1069 (1961).

    Article  CAS  Google Scholar 

  2. Hirsch, J. & Erlenmeyer-Kimling, L. Sign of taxis as a property of the genotype. Science 134, 835–836 (1961).

    Article  CAS  Google Scholar 

  3. Erlenmeyer-Kimling, L., Hirsch, J. & Weiss, J.M. Studies in experimental behavior genetics: III. Selection and hybridization analyses of individual differences in the sign of geotaxis. J. Comp. Physiol. Psychol. 55, 722–731 (1962).

    Article  Google Scholar 

  4. Hirsch, J. & Erlenmeyer-Kimling, L. Studies in experimental behavior genetics: IV. Chromosome analyses for geotaxis. J. Comp. Physiol. Psychol. 55, 732–739 (1962).

    Article  CAS  Google Scholar 

  5. Ricker, J.P. & Hirsch, J. Evolution of an instinct under long-term divergent selection for geotaxis in domesticated populations of Drosophila melanogaster. J. Comp. Psych. 99, 380–390 (1985).

    Article  CAS  Google Scholar 

  6. Dobzhansky, T. & Spassky, B. An experiment on migration and simultaneous selection for several traits in Drosophila pseudoobscura. Genetics 55, 723–734 (1966).

    Google Scholar 

  7. Dobzhansky, T., Spassky, B. & Sved, J. Effects of selection and migration on geotactic and phototactic behavior of Drosophila. II. Proc. R. Soc. Lond. B. 173, 191–207 (1968).

    Google Scholar 

  8. Dobzhansky, T., Levene, H. & Spassky, B. Effects of selection and migration on geotactic and phototactic behavior of Drosophila. III. Proc. R. Soc. Lond. B. 180, 21–41 (1972).

    Article  CAS  Google Scholar 

  9. Stoltenberg, S.F. & Hirsch, J. A gene correlate of geotaxis near Adh (2–50.1) in Drosophila melanogaster. J. Comp. Psych. 110, 252–259 (1996).

    Article  CAS  Google Scholar 

  10. Tully, T. Discovery of genes involved in learning and memory: an experimental synthesis of Hirschian and Benzerian perspectives. Proc. Natl Acad. Sci. USA 93, 13460–13467 (1996).

    Article  CAS  Google Scholar 

  11. White, K.P. Functional genomics and the study of development, variation, and evolution. Nature Rev. Genet. 2, 528–537 (2001).

    Article  CAS  Google Scholar 

  12. Ricker, J.P. & Hirsch, J. Reversal of genetic homeostasis in laboratory populations of Drosophila melanogaster under long-term selection for geotaxis and estimates of gene correlates: evolution of behavior-genetic systems. J. Comp. Psych. 102, 203–214 (1988).

    Article  CAS  Google Scholar 

  13. White, K.P., Rifkin, S.A., Hurban, P. & Hogness, D.S. Microarray analysis of Drosophila development during metamorphosis. Science 286, 2179–2184 (1999).

    Article  CAS  Google Scholar 

  14. Stanewsky, R. et al. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95, 681–692 (1998).

    Article  CAS  Google Scholar 

  15. Torok, I. et al. The overgrown hematopoietic organs-31 tumor suppressor gene of Drosophila encodes an Importin-like protein accumulating in the nucleus at the onset of mitosis. J. Cell Biol. 129, 1473–1489 (1995).

    Article  CAS  Google Scholar 

  16. Renn, S.C., Park, J.H., Rosbash, M., Hall, J.C. & Taghert, P.H. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99, 791–802 (1999).

    Article  CAS  Google Scholar 

  17. Doe, C.Q., Chu-LaGraff, Q., Wright, D.M. & Scott, M.P., The prospero gene specifies cell fates in the Drosophila central nervous system. Cell 65, 451–464 (1991).

    Article  CAS  Google Scholar 

  18. Roch, F. et al. Screening of larval/pupal P-element induced lethals on the second chromosome in Drosophila melanogaster: clonal analysis and morphology of imaginal discs. Mol. Gen. Genet. 257, 103–112 (1998).

    CAS  PubMed  Google Scholar 

  19. Zinsmaier, K.E., Eberle, K.K., Buchner, E., Walter, N. & Benzer, S. Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263, 977–980 (1994).

    Article  CAS  Google Scholar 

  20. Osborne, K.A. et al. Natural behavioral polymorphism due to a cGMP-dependnet protein kinase of Drosophila. Science 277, 834–836 (1997).

    Article  CAS  Google Scholar 

  21. Lin, Y.J., Seroude, L. & Benzer, S. Extended life-span and stress resistance in the Drosophila mutant methuselah. Science 282, 943–946 (1998).

    Article  CAS  Google Scholar 

  22. Song, W. et al. Methuselah, a putative G protein-coupled receptor, regulates excitatory neurotransmitter exocytosis at the larval neuromuscular junction of Drosophila. A. Dros. Res. Conf. 42, 51 (2001).

  23. Choi, K.-W. & Benzer, S. Rotation of photoreceptor clusters in the developing Drosophila eye requires the nemo gene. Cell 78, 125–136 (1994).

    Article  CAS  Google Scholar 

  24. Konopka, R.J. & Benzer, S. Clock mutants of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 68, 2112–2116 (1971).

    Article  CAS  Google Scholar 

  25. Kussel, P. & Frasch, M. Pendulin, a Drosophila protein with cell cycle-dependent nuclear localization, is required for normal cell proliferation. J. Cell Biol. 129, 1491–1507 (1995).

    Article  CAS  Google Scholar 

  26. Emery, P., So, W.V., Kaneko, M., Hall, J.C. & Rosbash, M. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95, 669–679 (1998).

    Article  CAS  Google Scholar 

  27. Melzig, J., Burg, M., Gruhn, M., Pak, W.L. & Buchner, E. Selective histamine uptake rescues photo- and mechanoreceptor function of histidine decarboxylase-deficient Drosophila mutant. J. Neurosci. 18, 7160–7166 (1998).

    Article  CAS  Google Scholar 

  28. Claridge-Chang, A. et al. Circadian regulation of gene expression systems in the Drosophila head. Neuron 32, 657–671 (2001).

    Article  CAS  Google Scholar 

  29. McDonald, M.J. & Rosbash, M. Microarray analysis and organization of circadian gene expression in Drosophila. Cell 107, 567–578 (2001).

    Article  CAS  Google Scholar 

  30. Greenspan, R.J. A kinder, gentler genetic analysis of behavior: dissection gives way to modulation. Curr. Opin. Neurobiol. 7, 805–811 (1997).

    Article  CAS  Google Scholar 

  31. McMillan, P.A. & McGuire, T.R. The homeotic gene spineless-aristapedia affects geotaxis in Drosophila melanogaster. Behav. Genet. 22, 557–573 (1992).

    Article  CAS  Google Scholar 

  32. Shaw, P.J., Cirelli, C., Greenspan, R.J. & Tononi, G. Correlates of sleep and waking in Drosophila melanogaster. Science 287, 1834–1837 (2000).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank R.W. Cross for help with statistical analyses, S. Bekele and D. Robinson for technical assistance and H. Dierick, G. Robinson and B. van Swinderen for reviewing the manuscript. The work by K.P.W. was supported by the National Institutes of Health, and all work at the Neurosciences Institute was supported by the Neurosciences Research Foundation.

Author information

Authors and Affiliations

  1. The Neurosciences Institute, 10640 John Jay Hopkins Drive, San Diego, 92121, California, USA

    Daniel P. Toma & Ralph J. Greenspan

  2. Department of Genetics, Yale University School of Medicine, New Haven, Connecticut, USA

    Kevin P. White

  3. Department of Psychology and of Animal Biology, University of Illinois, Urbana, USA, Illinois

    Jerry Hirsch

Authors
  1. Daniel P. Toma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kevin P. White
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jerry Hirsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ralph J. Greenspan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Kevin P. White or Ralph J. Greenspan.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Toma, D., White, K., Hirsch, J. et al. Identification of genes involved in Drosophila melanogaster geotaxis, a complex behavioral trait. Nat Genet 31, 349–353 (2002). https://doi.org/10.1038/ng893

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng893

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing