Rate and cost of adaptation in the Drosophila Genome

TL;DR

This study develops a new method to analyze how recombination influences adaptive evolution in the Drosophila genome, revealing high adaptation rates in high-recombining regions and significant costs in low-recombining regions.

Contribution

The paper introduces a novel inference method accounting for background selection and hitchhiking, providing detailed insights into adaptation heterogeneity across the Drosophila genome.

Findings

Approximately 50% of amino acid substitutions are adaptive in high-recombining regions.

Hitchhiking accounts for most substitutions in low-recombining regions.

Recombination influences the rate and effectiveness of adaptive evolution.

Abstract

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.