  Recent studies have consistently inferred high rates of adaptive molecular
evolution between Drosophila species. At the same time, the Drosophila genome
evolves under different rates of recombination, which results in partial
genetic linkage between alleles at neighboring genomic loci. Here we analyze
how linkage correlations affect adaptive evolution. We develop a new inference
method for adaptation that takes into account the effect on an allele at a
focal site caused by neighboring deleterious alleles (background selection) and
by neighboring adaptive substitutions (hitchhiking). Using complete genome
sequence data and fine-scale recombination maps, we infer a highly
heterogeneous scenario of adaptation in Drosophila. In high-recombining
regions, about 50% of all amino acid substitutions are adaptive, together with
about 20% of all substitutions in proximal intergenic regions. In
low-recombining regions, only a small fraction of the amino acid substitutions
are adaptive, while hitchhiking accounts for the majority of these changes.
Hitchhiking of deleterious alleles generates a substantial collateral cost of
adaptation, leading to a fitness decline of about 30/2N per gene and per
million years in the lowest-recombining regions. Our results show how
recombination shapes rate and efficacy of the adaptive dynamics in eukaryotic
genomes.
