REDUCED NATURAL-SELECTION ASSOCIATED WITH LOW RECOMBINATION IN DROSOPHILA-MELANOGASTER

Synonymous codons are not used equally in many organisms, and the exte nt of codon bias varies among loci. Earlier studies have suggested tha t more highly expressed loci in Drosophila melanogaster are more biase d, consistent with findings from several prokaryotes and unicellular e ukaryotes that codon bias is partly due to natural selection for trans lational efficiency. We link this model of varying selection intensity to the population-genetics prediction that the effectiveness of natur al selection is decreased under reduced recombination. In analyses of 385 D. melanogaster loci, we find that codon bias is reduced in region s of low recombination (i.e., near centromeres and telomeres and on th e fourth chromosome). The effect does not appear to be a linear functi on of recombination rate; rather, it seems limited to regions with the very lowest levels of recombination. The large majority of the genome apparently experiences recombination at a sufficiently high rate for effective natural selection against suboptimal codons. These findings support models of the Hill-Robertson effect and genetic hitchhiking an d are largely consistent with multiple reports of low levels of DNA se quence variation in regions of low recombination.