The genome-wide signature of short-term temporal selection

Abstract

Despite evolutionary biology's obsession with natural selection, few studies have evaluated multigenerational series of patterns of selection on a genome-wide scale in natural populations. Here, we report on a 10-y population-genomic survey of the microcrustacean Daphnia pulex. The genome sequences of [Formula: see text]800 isolates provide insights into patterns of selection that cannot be obtained from long-term molecular-evolution studies, including the following: the pervasiveness of near quasi-neutrality across the genome (mean net selection coefficients near zero, but with significant temporal variance about the mean, and little evidence of positive covariance of selection across time intervals); the preponderance of weak positive selection operating on minor alleles; and a genome-wide distribution of numerous small linkage islands of observable selection influencing levels of nucleotide diversity. These results suggest that interannual fluctuating selection is a major determinant of standing levels of variation in natural populations, challenge the conventional paradigm for interpreting patterns of nucleotide diversity and divergence, and motivate the need for the further development of theoretical expressions for the interpretation of population-genomic data.

Keywords: Daphnia; fluctuating selection; molecular evolution; population genomics; temporal variation.

Fig. 1.

Features of site-specific selection coefficients across the entire genome. (A) Distribution of time-averaged (mean) selection coefficients, $\overline{s},$ for the full set of genomic sites, given for different ranges of minor-allele frequencies (MAFs). (B) Means of site-specific $\overline{s}$ (black points), variance of $\overline{s}$ among sites after removal of sampling variance (red points), and the average temporal variance of site-specific $s$, again after removing variance associated with sampling (blue points), as a function of MAF. Note that in all cases the SE of the estimates are on the order of the width of the plotted points or smaller. (C) Distributions of the site-specific estimates of temporal variances of $s$ (after removing the contribution from sampling error). (D) Correlations between $\overline{s}$ for pairs of sites separated by intrachromosomal distances of $0$ to ${10}^5$ bp, in increments of $10$ bp.

Fig. 2.

Genome-wide temporal covariance of allele-frequency changes (standardized by the allele-frequency variance) across time intervals with increasing length. With ten consecutive annual sampling points, there are eight ways to compute single-year changes in adjacent years, seven ways to compare single-year changes separated by 2 y, etc., and the plotted values denote the means of such sets. Results are given for windows of MAFs and as averages for the full set of polymorphic sites (denoted in the Inset). The analysis on the left envelopes the entire genome, whereas that on the right is restricted to islands of strong selection (ISSs).

Fig. 3.

Chromosome-wide scans of window-specific intensities of selection. (A) For the set of SNPs within each window, the average estimate of absolute values of selection coefficients was compared with the probability distribution based on samples of randomized sites, with $P$ denoting the probability of achieving the observed measure by chance. The dashed red lines denote the critical cutoff points for significance after correcting for multiple comparisons. Horizontal blue bars denote the approximate locations of centromeric regions based on multiple laboratory crosses (33). Yellow vertical bars denoting the positions of ISSs are often slightly wider than actual ISS spans (for visualization purposes). (B) Cumulative frequency distributions for the lengths of ISS blocks residing on chromosome arms vs. windows. (C) Decline of the correlation of window-specific selection strengths with increasing distance, where $x=1$ denotes adjacent (nonoverlapping) windows, and the curves are fitted quadratic regressions.

Fig. 4.

Response of expected within-population measures of nucleotide diversity as a function of the temporal SD of the selection coefficient (${\sigma }_s$) and the population size ($N$). (A) Nucleotide diversity at a linked silent site (${\pi }_S$) relative to the neutral expectation at drift-mutation equilibrium under free recombination. (B) Ratio of diversity at the selected site to that at a completely linked neutral site, ${\pi }_N/{\pi }_S.$ Color legend in the upper panel designates various levels of the temporal SD of the selection coefficient $s$; Inset in the Lower panel designates the symbol shapes used for three levels of the average selection coefficient $\overline{s}$.