Natural polymorphism affecting learning and memory in Drosophila

Edited by Gene E. Robinson, University of Illinois at Urbana–Champaign, Urbana, IL, and approved June 11, 2007
August 7, 2007
104 (32) 13051-13055
Commentary
Memory flies sooner from flies that learn faster
Daniel R. Papaj, Emilie C. Snell-Rood

Abstract

Knowing which genes contribute to natural variation in learning and memory would help us understand how differences in these cognitive traits evolve among populations and species. We show that a natural polymorphism at the foraging (for) locus, which encodes a cGMP-dependent protein kinase (PKG), affects associative olfactory learning in Drosophila melanogaster. In an assay that tests the ability to associate an odor with mechanical shock, flies homozygous for one natural allelic variant of this gene (forR) showed better short-term but poorer long-term memory than flies homozygous for another natural allele (fors). The fors allele is characterized by reduced PKG activity. We showed that forR-like levels of both short-term learning and long-term memory can be induced in fors flies by selectively increasing the level of PKG in the mushroom bodies, which are centers of olfactory learning in the fly brain. Thus, the natural polymorphism at for may mediate an evolutionary tradeoff between short- and long-term memory. The respective strengths of learning performance of the two genotypes seem coadapted with their effects on foraging behavior: forR flies move more between food patches and so could particularly benefit from fast learning, whereas fors flies are more sedentary, which should favor good long-term memory.

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Acknowledgments

This work was supported by grants from Swiss National Science Foundation and Roche Research Foundation (T.J.K.); an Assistive Technology Infusion Project Grant from the Centre National de la Recherche Scientifique (to F.M.); grants from the Canadian Institutes of Health Research; and the Canada Research Chair Program (to M.B.S.). We thank L. Sygnarski for assistance with the experiments; J. D. Levine for the GAL4 lines (University of Toronto); K. R. Kaun for crossing the GAL4 drivers into sitter genetic backgrounds; and J. D. Levine, R. Stocker, A. Thum, C. J. Reaume, L. Rowe, and three referees for comments.

Supporting Information

Adobe PDF - 02923Fig4.pdf
Adobe PDF - 02923Fig4.pdf

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 104 | No. 32
August 7, 2007
PubMed: 17640898

Classifications

Submission history

Received: March 29, 2007
Published online: August 7, 2007
Published in issue: August 7, 2007

Keywords

  1. behavior
  2. evolution
  3. genetics
  4. rover-sitter
  5. cGMP-dependent protein kinase

Acknowledgments

This work was supported by grants from Swiss National Science Foundation and Roche Research Foundation (T.J.K.); an Assistive Technology Infusion Project Grant from the Centre National de la Recherche Scientifique (to F.M.); grants from the Canadian Institutes of Health Research; and the Canada Research Chair Program (to M.B.S.). We thank L. Sygnarski for assistance with the experiments; J. D. Levine for the GAL4 lines (University of Toronto); K. R. Kaun for crossing the GAL4 drivers into sitter genetic backgrounds; and J. D. Levine, R. Stocker, A. Thum, C. J. Reaume, L. Rowe, and three referees for comments.

Notes

This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0702923104/DC1.

Authors

Affiliations

Frederic Mery
Department of Biology, University of Fribourg, Chemin du Musée 10, CH 1700 Fribourg, Switzerland;
Laboratory for Evolution, Genome and Speciation, Centre National de la Recherche Scientifique, Avenue de la Terrasse, F 91198 Gif sur Yvette, France; and
Amsale T. Belay
Department of Biology, University of Toronto, 3359 Mississauga Road, Mississauga, ON, Canada L5L 1C6
Anthony K.-C. So
Department of Biology, University of Toronto, 3359 Mississauga Road, Mississauga, ON, Canada L5L 1C6
Marla B. Sokolowski
Department of Biology, University of Toronto, 3359 Mississauga Road, Mississauga, ON, Canada L5L 1C6
Tadeusz J. Kawecki§ [email protected]
Department of Biology, University of Fribourg, Chemin du Musée 10, CH 1700 Fribourg, Switzerland;

Notes

§
To whom correspondence should be sent at the present address: Department of Ecology and Evolution, University of Lausanne, Le Biophore, CH 1015 Lausanne, Switzerland. E-mail: [email protected]
Author contributions: F.M., M.B.S., and T.J.K. designed research; F.M. and A.T.B. performed research; A.K.-C.S. contributed new reagents/analytic tools; T.J.K. analyzed data; and F.M., A.T.B., M.B.S., and T.J.K. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Natural polymorphism affecting learning and memory in Drosophila
    Proceedings of the National Academy of Sciences
    • Vol. 104
    • No. 32
    • pp. 12951-13209

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