Impact of demography on linked selection in two outcrossing Brassicaceae species

Abstract

Genetic diversity is shaped by mutation, genetic drift, gene flow, recombination, and selection. The dynamics and interactions of these forces shape genetic diversity across different parts of the genome, between populations and species. Here, we have studied the effects of linked selection on nucleotide diversity in outcrossing populations of two Brassicaceae species, Arabidopsis lyrata and Capsella grandiflora, with contrasting demographic history. In agreement with previous estimates, we found evidence for a modest population size expansion thousands of generations ago, as well as efficient purifying selection in C. grandiflora. In contrast, the A. lyrata population exhibited evidence for very recent strong population size decline and weaker efficacy of purifying selection. Using multiple regression analyses with recombination rate and other genomic covariates as explanatory variables, we can explain 47% of the variance in neutral diversity in the C. grandiflora population, while in the A. lyrata population, only 11% of the variance was explained by the model. Recombination rate had a significant positive effect on neutral diversity in both species, suggesting that selection at linked sites has an effect on patterns of neutral variation. In line with this finding, we also found reduced neutral diversity in the vicinity of genes in the C. grandiflora population. However, in A. lyrata no such reduction in diversity was evident, a finding that is consistent with expectations of the impact of a recent bottleneck on patterns of neutral diversity near genes. This study thus empirically demonstrates how differences in demographic history modulate the impact of selection at linked sites in natural populations.

Selection on Accessible Chromatin Regions inCapsella grandiflora

“…In contrast, a for the 0-fold degenerate sites was 0.32 (95% CI: 0.31-0.33; supplementary fig. S3, Supplementary Material online), in line with previous estimates for C. grandiflora (Slotte et al 2010;Williamson et al 2014;Josephs et al 2017;Mattila et al 2019).…”

“…2 and supplementary fig. S2, Supplementary Material online) and the estimated DFE for 0-fold degenerate mutations in this study was similar to previous estimates for C. grandiflora (Williamson et al 2014;Mattila et al 2019).…”

“…An inferred constant population size is consistent with previous inference of demographic history in C. grandiflora (Foxe et al 2009;Slotte et al 2010;St. Onge et al 2011;Douglas et al 2015;Mattila et al 2019).…”

“…Indeed, natural selection was previously reported to be efficient in both coding and CNS in the C. grandiflora genome (Slotte et al 2010;Williamson et al 2014;Steige et al 2017). The rapid decay of linkage disequilibrium (within 0.004 cM, or $1 kb) in C. grandiflora (Foxe et al 2009;Mattila et al 2019), further minimizes interference from nearby coding sites and facilitates the study of selection patterns on candidate functional noncoding regions in the proximity of genes, such as cis-regulatory regions.…”

Genomic Signatures of Sexual Selection on Pollen-Expressed Genes in Arabis alpina

“…One potential complication when testing for an effect of diversity and inbreeding on sexual selection is that strong reductions in the effective population size, for example, due to demographic bottlenecks and/or linked selection, can result in reduced efficacy of selection genome-wide ( Wright et al 2013 ; Mattila et al 2019 ). In such populations, it can be difficult to specifically attribute relaxed purifying selection on gametophyte-expressed genes to relaxed sexual selection.…”