Adaptive evolution is substantially impeded by Hill-Robertson interference in Drosophila

Abstract

It is known that rates of mutation and recombination vary across the genome in many species. Here we investigate whether these factors affect the rate at which genes undergo adaptive evolution both individually and in combination and quantify the degree to which Hill-Robertson interference (HRi) impedes the rate of adaptive evolution. To do this we compiled a dataset of 6,141 autosomal protein coding genes from Drosophila, for which we have polymorphism data from D. melanogaster and divergence out to D. yakuba. We estimated the rate of adaptive evolution using a derivative of the McDonald-Kreitman test that controls for the slightly deleterious mutations. We find that the rate of adaptive amino acid substitution is positively correlated to both the rates of recombination and mutation. We also find that these correlations are robust to controlling for each other, synonymous codon bias and gene functions related to immune response and testes. We estimate that HRi reduces the rate of adaptive evolution by [~]27%. We also show that this fraction depends on a genes mutation rate; genes with low mutation rates lose [~]11% of their adaptive substitutions while genes with high mutation rates lose [~]43%. In conclusion, we show that the mutation rate and the rate of recombination, are important modifiers of the rate of adaptive evolution in Drosophila.