Originally published as Genetics Published Articles Ahead of Print on June 8, 2005.

Genetics, Vol. 170, 1153-1165, July 2005, Copyright © 2005
doi:10.1534/genetics.104.033456

DNA Sequence Polymorphism and Divergence at the erect wing and suppressor of sable Loci of Drosophila melanogaster and D. simulans

John M. Braverman^*,,,1, Brian P. Lazzaro^,, Montserrat Aguadé and Charles H. Langley

^* Department of Biology, Georgetown University, Washington, DC 20057-1229
Department of Entomology, Cornell University, Ithaca, New York 14853
Departament de Genètica, Facultat de Biologia, Universitat de Barcelona, 08071 Barcelona, Spain
Center for Population Biology and Section of Evolution and Ecology, University of California, Davis, California 95616

¹ Corresponding author: Department of Biology, Georgetown University, 3700 O St. NW, Washington, DC 20057-1229.
E-mail: jmb24{at}georgetown.edu

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 (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 F_ST 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.

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