Identification of quantitative trait loci function through analysis of multiple cuticular hydrocarbons differing between Drosophila simulans and Drosophila sechellia females

Abstract

The genetics of sexual isolation, behavioral differences between species that prevent mating, is understood poorly. Pheromonal differences between species can influence sexual isolation in many animals and in some cases a single locus can cause large functional changes in pheromonal mating signals. Drosophila cuticular hydrocarbons (CHCs) can function as pheromones and consequently affect mate recognition. In a previous study of the two major CHCs in females that affect mating discrimination between Drosophila simulans and D. sechellia, quantitative trait loci (QTL) were identified on the X and third chromosome, and a few candidate genes were potentially implicated. Here we specifically test candidate genes for CHC biosynthesis and determine the genetic architecture of four additional CHCs that differ in abundance between D. simulans and D. sechellia females. The same QTL, and new ones, were found for additional CHCs. By examining all these CHCs and exploring their covariance, we were able to ascribe putative function to the major QTL. Although desaturases have received considerable attention for their role in CHC biosynthesis, evidence here implies that elongases may be just as important. Sex determination genes do not seem to have a role in this species difference although D. sechellia is sexually dimorphic in CHCs, whereas D. simulans is not. Epistatic interactions, only detected for CHCs limited to D. sechellia, imply that complex interactions among loci may also be having a role in these compounds that affect mating isolation.

Sexual isolation between North American and Bogota strains of Drosophila pseudoobscura

“…Understanding the genetic architecture of a given behavior requires identifying and mapping genes which contribute to the trait and affect natural variation in the trait. Advances in molecular and statistical tools have identified QTLs for traits influencing sexual isolation between species (see Williams et al 2001;Gleason et al 2002;Huttunen et al 2004 for courtship song; Doi et al 2001;Shaw and Parsons 2002;Civetta and Cantor 2003;Moehring et al 2004 for mating behavior; Gleason et al 2005Gleason et al , 2009Etges et al 2007Etges et al , 2009 for cuticular hydrocarbons). Currently, we are analyzing QTLs affecting variation in courtship behavior and cuticular hydrocarbons conferring sexual isolation between the two D. pseudoobscura subspecies.…”

“…Courtship song and cuticular hydrocarbons have been identified as important elements in mating behavior (see Ferveur 2005;Gleason 2005;Hoikkala 2005 for review). Several studies estimated the number of loci that contribute to factors preventing gene exchange between species (Macdonald and Goldstein 1999;Williams et al 2001;Civetta et al 2002;Gleason et al 2002Gleason et al , 2005Gleason et al , 2009Civetta and Cantor 2003;Huttunen et al 2004;Moehring et al 2004;Etges et al 2007Etges et al , 2009. For example, in a study of differences between the sibling species Drosophila pseudoobscura and D. persimilis in courtship song, three quantitative trait loci (QTLs) for courtship song interpulse interval (IPI) were identified, all associated with inversions that differentiate these two species (Williams et al 2001).…”

Genetic dissection of a major polymorphism underlying population divergence in sexually selected pheromones in Drosophila serrata

“…Most of the CHCs mapped to QTLs on chromosome 3, a finding that is in accord with those of similar studies in Drosophila which find that CHC variation is largely driven by loci on chromosome 3 (FERVEUR et al 1996;COYNE et al 1999;DALLERAC et al 2000;WICKER-THOMAS and JALLON 2001;GLEASON et al 2009). By using several fine-mapping strategies I identified fatty-acyl-CoA reductase genes on chromosome 3R as underlying the CHC polymorphism in D. serrata.…”

“…The mapping of CHCs to many QTLs on chromosome 3 is in accord with findings of several similar studies in Drosophila (COYNE et al 1999;DALLERAC et al 2000;TAKAHASHI et al 2001;GLEASON et al 2009;SHIRANGI et al 2009). Hydrocarbon differences in Drosophila seem to be largely influenced by chromosome 3 loci (FERVEUR et al 1996;WICKER-THOMAS and JALLON 2001;MARCILLAC et al 2005a;WICKER-THOMAS et al 2009) …”

“…Pleiotropic and epistatic interactions as well as QTL x environment interactions also feature in the genetic architectures of these traits (GLEASON et al 2005;FOLEY et al 2007;ETGES et al 2009). Almost all of the four chromosomes of the Drosophila genome (X, 2, 3 and 4) have been implicated in CHC variation (RULE and ROELOFS 1989;ETGES et al 2009;GLEASON et al 2009) but the involvement of chromosome 3 is seemingly paramount.…”