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Extensive epistasis for olfactory behaviour, sleep and waking activity in Drosophila melanogaster

  • SHILPA SWARUP (a1) (a2), SUSAN T. HARBISON (a1) (a2), LAUREN E. HAHN (a1), TATIANA V. MOROZOVA (a2) (a3), AKIHIKO YAMAMOTO (a2) (a3), TRUDY F. C. MACKAY (a1) (a2) and ROBERT R. H. ANHOLT (a1) (a2) (a3)...
Abstract
Summary

Epistasis is an important feature of the genetic architecture of quantitative traits, but the dynamics of epistatic interactions in natural populations and the relationship between epistasis and pleiotropy remain poorly understood. Here, we studied the effects of epistatic modifiers that segregate in a wild-derived Drosophila melanogaster population on the mutational effects of P-element insertions in Semaphorin-5C (Sema-5c) and Calreticulin (Crc), pleiotropic genes that affect olfactory behaviour and startle behaviour and, in the case of Crc, sleep phenotypes. We introduced Canton-S B (CSB) third chromosomes with or without a P-element insertion at the Crc or Sema-5c locus in multiple wild-derived inbred lines of the Drosophila melanogaster Genetic Reference Panel (DGRP) and assessed the effects of epistasis on the olfactory response to benzaldehyde and, for Crc, also on sleep. In each case, we found substantial epistasis and significant variation in the magnitude of epistasis. The predominant direction of epistatic effects was to suppress the mutant phenotype. These observations support a previous study on startle behaviour using the same D. melanogaster chromosome substitution lines, which concluded that suppressing epistasis may buffer the effects of new mutations. However, epistatic effects are not correlated among the different phenotypes. Thus, suppressing epistasis appears to be a pervasive general feature of natural populations to protect against the effects of new mutations, but different epistatic interactions modulate different phenotypes affected by mutations at the same pleiotropic gene.

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The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution-NonCommercial-ShareAlike licence <http://creativecommons.org/licenses/by-nc-sa/2.5/>. The written permission of Cambridge University Press must be obtained for commercial re-use.
Corresponding author
*Corresponding author: Robert R. H. Anholt, Department of Biology, Box 7617, North Carolina State University, Raleigh, NC 27695-7617, USA. Tel: (919) 515-1173. Fax: (919) 515-1801. E-mail: anholt@ncsu.edu
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