Demography and mating system shape the genome-wide impact of purifying selection in Arabis alpina

Plant mating systems have profound effects on levels and structuring of genetic variation and can affect the impact of natural selection. Although theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 115; no. 4; pp. 816 - 821
Main Authors Laenen, Benjamin, Tedder, Andrew, Nowak, Michael D., Toräng, Per, Wunder, Jörg, Wötzel, Stefan, Steige, Kim A., Kourmpetis, Yiannis, Odong, Thomas, Drouzas, Andreas D., Bink, Marco C. A. M., Ågren, Jon, Coupland, George, Slotte, Tanja
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 23.01.2018
Subjects
Accumulation
Alleles
Alpine environments
Arabis alpina
Biological Sciences
Bottleneck
Colonization
Demographic history
Demographics
Demography
Evolution
Fertilization
Fitness effects
Genetic diversity
Genetic load
Genomes
Genomic analysis
Genomics
Natural selection
Plant reproduction
Polar environments
Population genetics
Populations
Self-fertilization
genetic load
self-fertilization
demographic history
fitness effects
bottleneck
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Summary:Plant mating systems have profound effects on levels and structuring of genetic variation and can affect the impact of natural selection. Although theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population-genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina. We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles, whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, mating system and demography shape the impact of purifying selection on genomic variation in A. alpina. These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixedmating strategies.
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Reviewers: P.I., Swedish University of Agricultural Sciences; and A.T., Technical University of Munich.
4Present address: Hendrix Genetics Research, Technology & Services, 5830 AC Boxmeer, The Netherlands.
Author contributions: M.C.A.M.B., J.Å., G.C., and T.S. designed research; B.L., A.T., P.T., J.W., S.W., and K.A.S. performed research; A.D.D. contributed new reagents/analytic tools; B.L., A.T., M.D.N., Y.K., and T.O. analyzed data; and B.L., A.T., J.Å., G.C., and T.S. wrote the paper.
1B.L. and A.T. contributed equally to this work.
2Present address: Institute of Botany, Biozentrum, University of Cologne, 50674 Cologne, Germany.
Contributed by George Coupland, December 7, 2017 (sent for review May 10, 2017; reviewed by Pär K. Ingvarsson and Aurélien Tellier)
3Present address: Nestlé Institute of Health Sciences, 1015 Lausanne, Switzerland.
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.1707492115