DNA sequence polymorphism and divergence at the erect wing and suppressor of sable loci of Drosophila melanogaster and D. simulans

Abstract

Several evolutionary models of linked selection (e.g., genetic hitchhiking, background selection, and random environment) predict a reduction in polymorphism relative to divergence in genomic regions where the rate of crossing over per physical distance is restricted. We tested this prediction near the telomere of the Drosophila melanogaster and D. simulans X chromosome at two loci, erect wing (ewg) and suppressor of sable [su(s)]. Consistent with this prediction, polymorphism is reduced at both loci, while divergence is normal. The reduction is greater at ewg, the more distal of the two regions. Two models can be discriminated by comparing the observed site frequency spectra with those predicted by the models. The hitchhiking model predicts a skew toward rare variants in a sample, while the spectra under the background-selection model are similar to those of the neutral model of molecular evolution. Statistical tests of the fit to the predictions of these models require many sampled alleles and segregating sites. Thus we used SSCP and stratified DNA sequencing to cover a large number of randomly sampled alleles (approximately 50) from each of three populations. The result is a clear trend toward negative values of Tajima's D, indicating an excess of rare variants at ewg, the more distal of the two loci. One fixed difference among the populations and high FST values indicate strong population subdivision among the three populations at ewg. These results indicate genetic hitchhiking at ewg, in particular, geographically localized hitchhiking events within Africa. The reduction of polymorphism at su(s) combined with the excess of high-frequency variants in D. simulans is inconsistent with the hitchhiking and background-selection models.

Figure 1.—

The SSCP fragments of ewg, shown as small horizontal lines below the gene. Only part of the entire gene is shown, and it is oriented with the 3′-end on the left in contrast to the standard orientation to illustrate the fragment positions relative to the physical location of the su(s) fragments. The solid boxes are exons, the shaded boxes are alternatively spliced exons, and the thin lines connecting the solid boxes are the introns. The scale is indicated with a bar 200 nucleotides long.

Figure 2.—

The SSCP fragments of su(s). These are similar but not identical to fragments in Langley et al. (2000). The open box is the 5′-UTR. See the Figure 1 legend for more information.