Reduced natural selection associated with low recombination in Drosophila melanogaster

Synonymous codons are not used equally in many organisms, and the extent ofcodon bias varies among loci. Earlier studies have suggested that morehighly expressed loci in Drosophila melanogaster are more biased,consistent with findings from several prokaryotes and unicellulareukaryotes that codon bias is partly due to natural selection fortranslational efficiency. We link this model of varying selection intensityto the population-genetics prediction that the effectiveness of naturalselection is decreased under reduced recombination. In analyses of 385 D.melanogaster loci, we find that codon bias is reduced in regions of lowrecombination (i.e., near centromeres and telomeres and on the fourthchromosome). The effect does not appear to be a linear function ofrecombination rate; rather, it seems limited to regions with the verylowest levels of recombination. The large majority of the genome apparentlyexperiences recombination at a sufficiently high rate for effective naturalselection against suboptimal codons. These findings support models of theHill-Robertson effect and genetic hitchhiking and are largely consistentwith multiple reports of low levels of DNA sequence variation in regions oflow recombination.