Natural Selection and Recombination Rate Variation Shape Nucleotide Polymorphism Across the Genomes of Three Related Populus Species

Abstract

A central aim of evolutionary genomics is to identify the relative roles that various evolutionary forces have played in generating and shaping genetic variation within and among species. Here we use whole-genome resequencing data to characterize and compare genome-wide patterns of nucleotide polymorphism, site frequency spectrum, and population-scaled recombination rates in three species of Populus: Populus tremula, P. tremuloides, and P. trichocarpa. We find that P. tremuloides has the highest level of genome-wide variation, skewed allele frequencies, and population-scaled recombination rates, whereas P. trichocarpa harbors the lowest. Our findings highlight multiple lines of evidence suggesting that natural selection, due to both purifying and positive selection, has widely shaped patterns of nucleotide polymorphism at linked neutral sites in all three species. Differences in effective population sizes and rates of recombination largely explain the disparate magnitudes and signatures of linked selection that we observe among species. The present work provides the first phylogenetic comparative study on a genome-wide scale in forest trees. This information will also improve our ability to understand how various evolutionary forces have interacted to influence genome evolution among related species.

Keywords: Populus; natural selection; nucleotide polymorphism; recombination; whole-genome resequencing.

Figure 1

Genome-wide patterns of polymorphism among three Populus species. Nucleotide diversity (Θ_π) was calculated over 100-kbp nonoverlapping windows in P. tremula (orange line), P. tremuloides (blue line), and P. trichocarpa (green line) along the 19 chromosomes.

Figure 2

Distribution and correlations of (A) polymorphism (Θ_π), (B) Tajima’s D, and (C) population-scaled recombination rate (ρ) between pairwise comparisons of P. tremula, P. tremuloides, and P. trichocarpa over 100-kbp nonoverlapping windows. The red-to-yellow-to-blue gradient indicates decreased density of observed events at a given location in the graph. Spearman’s rank correlation coefficient (rho) and the P-value are shown in each subplot. (***P < 2.2 × 10⁻¹⁶, **P < 0.001). The dashed gray line in each subplot indicates a simple linear regression line with intercept being zero and slope being one.

Figure 3

Estimates of purifying and positive selection at 0-fold nonsynonymous sites in three Populus species. (A) The distribution of fitness effects of new amino acid mutations, (B) the proportion of adaptive substitution (α), and (C) the rate of adaptive nonsynonymous-to-synonymous substitutions (ω) in P. tremula (orange bar), P. tremuloides (blue bar), and P. trichocarpa (green bar). Error bars represent 95% bootstrap confidence intervals.

Figure 4

Correlations of estimates between neutral genetic diversity (Θ_fourfold) (left), neutral genetic divergence (d_fourfold) (right), and population-scaled recombination rates (ρ) over 1-Mb nonoverlapping windows. Linear regression lines are colored according to species: (A) P. tremula (orange line), (B) P. tremuloides (blue line), and (C) P. trichocarpa (green line).

Figure 5

Correlations of estimates between (A) population-scaled recombination rates (ρ), (B) genic genetic diversity (Θ_fourfold), (C) intergenic genetic diversity (Θ_Intergenic), and gene density over 1-Mb nonoverlapping windows in P. tremula (left), P. tremuloides (middle), and P. trichocarpa (right). Gray points represent the statistics computed over 1-Mb nonoverlapping windows. Colored lines denote the lowess curves fit to the two analyzed variables in each species.