Quantitative trait loci for cuticular hydrocarbons associated with sexual isolation between Drosophila simulans and D. sechellia.

The identification of genes with large effects on sexual isolation and speciation is an important link between classic evolutionary genetics and molecular biology. Few genes that affect sexual isolation and speciation have been identified, perhaps because many traits influencing sexual isolation are complex behaviors. Cuticular hydrocarbons (CHs) of species of the Drosophila melanogaster group play a large role in sexual isolation by functioning as contact pheromones influencing mate recognition. Some of the genes that play key roles in determining species-specific CHs have been identified. We have performed separate quantitative trait locus (QTL) analyses of 7-tricosene (7-T) and 7,11-heptacosadiene (7,11-HD), the two major female CHs differing between D. simulans and D. sechellia. We find that approximately 40% of the phenotypic variance in each CH is associated with two to four chromosomal regions. A region on the right arm of chromosome 3 contains QTL that affect both traits, but other QTL are in distinct chromosomal regions. Epistatic interactions were detected between two pairs of QTL for 7,11-HD such that if either were homozygous for the D. simulans allele, the fly was similar to D. simulans in phenotype, with a low level of 7,11-HD. We discuss the location of these regions with regard to candidate genes for CH production, including those for desaturases.

Gleason JM ，Jallon JM ，Rouault JD ，Ritchie MG ... -  《GENETICS》

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

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.

Gleason JM ，James RA ，Wicker-Thomas C ，Ritchie MG ... -  《-》

Genetics of differences in pheromonal hydrocarbons between Drosophila melanogaster and D. simulans.

Females of Drosophila melanogaster and its sibling species D. simulans have very different cuticular hydrocarbons, with the former bearing predominantly 7,11-heptacosadiene and the latter 7-tricosene. This difference contributes to reproductive isolation between the species. Genetic analysis shows that this difference maps to only the third chromosome, with the other three chromosomes having no apparent effect. The D. simulans alleles on the left arm of chromosome 3 are largely recessive, allowing us to search for the relevant regions using D. melanogaster deficiencies. At least four nonoverlapping regions of this arm have large effects on the hydrocarbon profile, implying that several genes on this arm are responsible for the species difference. Because the right arm of chromosome 3 also affects the hydrocarbon profile, a minimum of five genes appear to be involved. The large effect of the third chromosome on hydrocarbons has also been reported in the hybridization between D. simulans and its closer relative D. sechellia, implying either an evolutionary convergence or the retention in D. sechellia of an ancestral sexual dimorphism.

Coyne JA 《GENETICS》

Genetics of a pheromonal difference affecting sexual isolation between Drosophila mauritiana and D. sechellia.

Females of the sibling species Drosophila sechellia and D. mauritiana differ in their cuticular hydrocarbons: the predominant compound in D. sechellia is 7,11-heptacosadiene (7,11-HD), while that in D. mauritiana is 7-tricosene (7-T). We investigate the genetic basis of this difference and its involvement in reproductive isolation between the species. Behavioral studies involving hydrocarbon transfer suggest that these compounds play a large role in the sexual isolation between D. mauritiana males and D. sechellia females, while sexual isolation in the reciprocal hybridization results more from differences in female behavior than hydrocarbons. This interspecific difference in hydrocarbon profile is due to evolutionary change at a minimum of six loci, all on the third chromosome. The localization of evolutionary change to the third chromosome has been seen in very other genetic analysis of female hydrocarbon differences in the D. melanogaster group. We suggest that the high 7,11-HD phenotype seen in two species evolved twice independently from ancestors having the high 7-T phenotype and the recurrent third-chromosome effects are evolutionary convergences that may be due to a concentration of "hydrocarbon genes" on that chromosome.

Coyne JA ，Charlesworth B 《GENETICS》

Do quantitative trait loci (QTL) for a courtship song difference between Drosophila simulans and D. sechellia coincide with candidate genes and intraspecific QTL?

The genetic architecture of traits influencing sexual isolation can give insight into the evolution of reproductive isolation and hence speciation. Here we report a quantitative trait loci (QTL) analysis of the difference in mean interpulse interval (IPI), an important component of the male courtship song, between Drosophila simulans and D. sechellia. Using a backcross analysis, we find six QTL that explain a total of 40.7% of the phenotypic variance. Three candidate genes are located in the intervals bounded by two of the QTL and there are no significant QTL on the X chromosome. The values of mean IPI for hybrid individuals imply the presence of dominant alleles or epistasis. Because unisexual hybrid sterility prevents an F(2) analysis, we cannot distinguish dominant from additive genetic effects at the scale of QTL. A comparison with a study of QTL for intraspecific variation in D. melanogaster shows that, for these strains, the QTL we have identified for interspecific variation cannot be those that contribute to intraspecific variation. We find that the QTL have bidirectional effects, which indicates that the genetic architecture is compatible with divergence due to genetic drift, although other possibilities are discussed.

Gleason JM ，Ritchie MG 《GENETICS》