The Genome-Wide Effect of Drift and Selection over a Single Generation

Abstract

The relative importance of genetic drift versus selection to evolutionary change has long been debated. This debate has mainly focused over long-time-scales (e.g. hundreds of thousands of generations), leaving the question of short-term evolutionary change relatively unaddressed. Our knowledge about the effects of selection on genetic change over short time scales is often based on identifying major allele frequency changes at few loci with large selective advantage. Yet selection often acts on polygenic traits where the short-term response is shaped by small shifts in allele frequency at many loci that will be difficult to distinguish from genetic drift. Here, we quantify the genome-wide effects of polygenic selection over a single generation, using the idea that alleles in stronger genetic correlation (LD) with selected alleles are expected to show greater variance in allele frequency change than expected under genetic drift. We derive expressions relating variation in LD among loci to the variance in allele frequency change due to linked selection and genetic drift and leverage this theory to quantify the contribution of linked selection to a single generation of allele frequency change. To demonstrate our approach, we decompose the genome-wide allele frequency change in the UK Biobank using fitness proxy phenotypes. We show that selection makes a small, but significant, contribution, with genetic drift making up the large majority of the change in allele frequencies. Our framework could be applied to other organisms for which data on number of offspring or allele frequencies over consecutive generations are available, enabling investigations of the short-term, genome-wide effects of polygenic selection across a wide range of species.