Using Hitchhiking Genes to Study Adaptation and Divergence During Speciation Within the Drosophila melanogaster Species Complex

Abstract

Several studies of intraspecific and interspecific DNA sequence variation from Drosophila loci have revealed a pattern of low intraspecific variation from genomic regions of low recombination. The mechanisms consistently invoked to explain these patterns are the selective sweep of advantageous mutations together with genetic hitchhiking of linked loci. To examine the effect of selective sweeps on genetic divergence during speciation, we studied two loci in different genomic regions thought to be subject to selective sweeps. We obtained DNA sequences from 1.1-kb pair portions of the fourth chromosome locus cubitus interruptus Dominant (ciD) and from the asense locus near the telomere of the X chromosome. At ciD, we found very low variation among multiple lines of Drosophila mauritiana and D. sechellia. This finding is consistent with an earlier report of very low variation in D. melanogaster and D. simulans at ciD and supports the conclusion of selective sweeps and genetic hitchhiking on the nonrecombining fourth chromosome. The pattern of variation found at asense suggests that a selective sweep has occurred recently at the tip of the X chromosome in D. simulans, but not in D. melanogaster or D. mauritiana. The data from ciD and asense are compared with data from three X chromosome loci (period, zeste, and yolk protein 2) that experience normal levels of recombination. By examining estimated genealogies and the rates at which different classes of mutations have accumulated, we conclude that selective sweeps are common occurrences on the fourth chromosome but less common near the tip of the X chromosome. An interesting pattern of low variation at ciD among D. simulans, D. mauritiana, and D. sechellia suggests that a selective sweep may have occurred among these forms even after divergence into separate species had begun.