Extensive epistasis for olfactory behaviour, sleep and waking activity inDrosophila melanogaster

Abstract

SummaryEpistasis 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-derivedDrosophila melanogasterpopulation on the mutational effects ofP-element insertions inSemaphorin-5C(Sema-5c) andCalreticulin(Crc), pleiotropic genes that affect olfactory behaviour and startle behaviour and, in the case ofCrc, sleep phenotypes. We introducedCanton-S B(CSB) third chromosomes with or without aP-element insertion at theCrcorSema-5clocus in multiple wild-derived inbred lines of theDrosophila melanogasterGenetic Reference Panel (DGRP) and assessed the effects of epistasis on the olfactory response to benzaldehyde and, forCrc, 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 sameD. melanogasterchromosome 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.