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Impact of demography on linked selection in two outcrossing Brassicaceae species
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).ORCID iD: 0000-0002-3221-8835
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Number of Authors: 62019 (English)In: Ecology and Evolution, E-ISSN 2045-7758, Vol. 9, no 17, p. 9532-9545Article in journal (Refereed) Published
Abstract [en]

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.

Place, publisher, year, edition, pages
2019. Vol. 9, no 17, p. 9532-9545
Keywords [en]
demography, distribution of fitness effects, linked selection, neutral genetic diversity, purifying selection, recombination
National Category
Biological Sciences
Research subject
Ecology and Evolution
Identifiers
URN: urn:nbn:se:su:diva-173157DOI: 10.1002/ece3.5463ISI: 000481053400001OAI: oai:DiVA.org:su-173157DiVA, id: diva2:1354003
Available from: 2019-09-24 Created: 2019-09-24 Last updated: 2024-01-17Bibliographically approved
In thesis
1. Population genomic analyses of regulatory variation and selection in Brassicaceae species
Open this publication in new window or tab >>Population genomic analyses of regulatory variation and selection in Brassicaceae species
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The impact of selection on regulatory variation and the contribution of regulatory changes to phenotypic variation has long been debated in evolutionary genetics. Because cis-regulatory elements such as promoters and enhancers can be difficult to identify, it has been more challenging to quantify the impact of selection on variation in cis-regulatory regions than in protein-coding regions. In this thesis, I use genomic tools to investigate gene expression variation and selection in Brassicaceae species. First, I investigated the genomic impact of selection on putative cis-regulatory regions in the genome of the crucifer species Capsella grandiflora (Brassicaceae) (Paper I). I used an assay for transposase-accessible chromatin with high throughput sequencing (ATAC-seq) to empirically identify putative cis-regulatory regions as those located in accessible chromatin regions (ACRs) in the genome of the crucifer species Capsella grandiflora. Based on whole-genome resequencing data from a natural population, I then showed that ACRs are under stronger purifying selection than other intergenic regions and that they are depleted for transposable element (TE) insertions and enriched for expression quantitative trait loci (eQTL), as would be expected if ACRs are enriched for functional elements affecting gene expression. Second, I explored how the location and silencing of transposable elements (TEs) affects selection against TEs (Paper II). Specifically, I tested a trade-off model on epigenetic TE silencing, according to which the positive effects of TE silencing on preventing TE movement conflict with negative effects of TE silencing on nearby gene expression. I found that TE silencing through the RNA-directed DNA methylation (RdDM) pathway affects selection against TEs close to genes in C. grandiflora, which is consistent with the trade-off model. Third, I used Arabidopsis thaliana single-cell expression data to investigate the relationship between gene body methylation (gbM) and transcriptional regulation (Paper III). I found that there was an indirect correlation between gbM and gene expression noise as well as a direct correlation between gbM and gene expression consistency and potentially intron retention in Arabidopsis thaliana. Fourth, I investigated the impact of demographic history on genomic signatures of selection at linked sites (linked selection) (Paper IV). This study revealed that neutral genetic diversity in C. grandiflora with a stable effective population size is influenced by linked selection whereas in Arabidopsis lyrata, which underwent a recent and strong bottleneck, neutral diversity is mainly affected by population size change. In summary, this thesis offers new insights into determinants of gene expression variation, selection on genomic features linked to gene expression alteration, as well as on the effect of demographic history on linked selection patterns in Brassicaceae.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, 2020. p. 48
Keywords
Capsella grandiflora, Arabidopsis thaliana, Arabidopsis lyrata, natural selection, gene expression variation, DNA and gene body methylation, transposable elements, DNA accessibility, gene expression noise, epigenetic silencing, linked selection
National Category
Genetics and Genomics
Research subject
Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-179151 (URN)978-91-7911-076-5 (ISBN)978-91-7911-077-2 (ISBN)
Public defence
2020-05-08, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
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Note

At the time of the doctoral defense, the following paper was unpublished and had a status as follows: Paper 1: Manuscript.

Available from: 2020-04-15 Created: 2020-03-11 Last updated: 2025-02-07Bibliographically approved

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Laenen, BenjaminHorvath, RobertSlotte, Tanja

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