Estimating the genome-wide contribution of selection to temporal allele frequency change

Abstract

<jats:title>Abstract</jats:title><jats:p>Rapid phenotypic adaptation is often observed in natural populations and selection experiments. However, detecting the genome-wide impact of this selection is difficult, since adaptation often proceeds from standing variation and selection on polygenic traits, both of which may leave faint genomic signals indistinguishable from a noisy background of genetic drift. One promising signal comes from the genome-wide covariance between allele frequency changes observable from temporal genomic data, e.g. evolve-and-resequence studies. These temporal covariances reflect how heritable fitness variation in the population leads changes in allele frequencies at one timepoint to be predictive of the changes at later timepoints, as alleles are indirectly selected due to remaining associations with selected alleles. Since genetic drift does not lead to temporal covariance, we can use these covariances to estimate what fraction of the variation in allele frequency change through time is driven by linked selection. Here, we reanalyze three selection experiments to quantify the effects of linked selection over short timescales using covariance among time-points and across replicates. We estimate that at least 17% to 37% of allele frequency change is driven by selection in these experiments. Against this background of positive genome-wide temporal covariances we also identify signals of negative temporal covariance corresponding to reversals in the direction of selection for a reasonable proportion of loci over the time course of a selection experiment. Overall, we find that in the three studies we analyzed, linked selection has a large impact on short-term allele frequency dynamics that is readily distinguishable from genetic drift.</jats:p><jats:sec><jats:title>Significance Statement</jats:title><jats:p>A long-standing problem in evolutionary biology is to understand the processes that shape the genetic composition of populations. In a population without migration, the two processes that change allele frequencies are selection, which increases beneficial alleles and removes deleterious ones, and genetic drift which randomly changes frequencies as some parents contribute more or less alleles to the next generation. Previous efforts to disentangle these processes have used genomic samples from a single timepoint and models of how selection affects neighboring sites (linked selection). Here, we use genomic data taken through time to quantify the contributions of selection and drift to genome-wide frequency changes. We show selection acts over short timescales in three evolve-and-resequence studies and has a sizable genome-wide impact.</jats:p></jats:sec>

Polygenic adaptation after a sudden change in environment

“…As polygenic adaptation in quantitative traits is likely ubiquitous, our conclusions have potentially important implications. One is that, contrary to adaptation mediated by selective sweeps of initially rare, large effect, beneficial alleles (Smith and Haigh, 1974; Kaplan et al, 1989; Braverman et al, 1995; Hermisson and Pennings, 2005; Coop and Ralph, 2012; Berg and Coop, 2015), polygenic adaptation might have minor effects on patterns of neutral diversity at any given point in time (but may affect temporal diversity patterns (Buffalo and Coop, 2019, 2020). The effects of selected alleles on neutral diversity at linked loci follow from their trajectories (Barton, 2000).…”

Inference of natural selection from ancient DNA

“…However, this approach is subject to many of the caveats discussed below in that it assumes a constant population size and the model would be violated by migration or other temporal variation in population composition. Therefore, although this approach is supported by simulations, and has been demonstrated to be effective at estimating temporal covariance in allele frequencies associated with linked selection in lab‐based experimental evolution (Buffalo and Coop 2019a, b), it may be limited in its application to real‐life aDNA data. The effect of population stratification on polygenic signals from modern samples has recently been highlighted, when two studies found that the signal for height selection in Europe was less pronounced in the U.K. Biobank dataset, which is less confounded by population structure than the GIANT consortium dataset (Berg et al.…”

Clinal and seasonal change are correlated inDrosophila melanogasternatural populations

“…Genome-wide analyses have identified polymorphisms and inversions that oscillate in seasonal timescales in several localities in the United States and Europe (Bergland et al 2014; Kapun et al 2016; Machado et al 2018). However, a recent analysis suggested seasonal fluctuations in allele frequencies seems small and temporal structure independent of seasons may be more important in this system (Buffalo and Coop 2019).…”

“…Identifying polymorphisms that fluctuate seasonally is challenging, because effect sizes are small and populations are subject to stochastic environmental events that are not tied to seasonality (Machado et al 2018). Indeed, a recent study put in question the interpretation that a set of previously identified seasonal SNPs in D. melanogaster is due to seasonally varying selection (Buffalo and Coop 2019).…”