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Epigenetic mechanisms modulate differences in Drosophila foraging behavior

  1. Marla B. Sokolowskia,b,1
  1. aDepartment of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
  2. bChild and Brain Development Program, Canadian Institute for Advanced Research, Toronto, ON, Canada M5G 1M1;
  3. cDepartment of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada N6A 5C1;
  4. dDepartment of Biology, Faculty of Science, Western University, London, ON, Canada N6G 2M1
  1. Edited by Gene E. Robinson, University of Illinois at Urbana–Champaign, Urbana, IL, and approved September 26, 2017 (received for review June 14, 2017)

Significance

Individuals of the same species display remarkable variation in behavior even in identical contexts, but the molecular mechanisms that underlie this variation are still poorly understood. Here we present important findings on the regulation of behavioral variation. We show that epigenetic regulation interacts with genetic variation, and provide causal evidence that this mechanism underlies distinct foraging behavioral strategies. More globally, our findings show that individuals within a species may behave differently due to the epigenetic control of gene expression.

Abstract

Little is known about how genetic variation and epigenetic marks interact to shape differences in behavior. The foraging (for) gene regulates behavioral differences between the rover and sitter Drosophila melanogaster strains, but the molecular mechanisms through which it does so have remained elusive. We show that the epigenetic regulator G9a interacts with for to regulate strain-specific adult foraging behavior through allele-specific histone methylation of a for promoter (pr4). Rovers have higher pr4 H3K9me dimethylation, lower pr4 RNA expression, and higher foraging scores than sitters. The rover–sitter differences disappear in the presence of G9a null mutant alleles, showing that G9a is necessary for these differences. Furthermore, rover foraging scores can be phenocopied by transgenically reducing pr4 expression in sitters. This compelling evidence shows that genetic variation can interact with an epigenetic modifier to produce differences in gene expression, establishing a behavioral polymorphism in Drosophila.

Footnotes

  • ?1To whom correspondence should be addressed. Email: marla.sokolowski{at}utoronto.ca.
  • Author contributions: I.A., J.M.K., and M.B.S. designed research; I.A. performed research; J.M.K. and M.B.S. contributed new reagents/analytic tools; I.A. analyzed data; and I.A. and M.B.S. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database [accession nos. CP023329CP023334 (sitter) and CP023335CP023340 (rover)].

  • See Commentary on page 12365.

  • This article contains supporting information online at www.danielhellerman.com/lookup/suppl/doi:10.1073/pnas.1710770114/-/DCSupplemental.

Published under the PNAS license.

Online Impact

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