University of Oulu

Margarita Takou, Tuomas Hämälä, Evan M Koch, Kim A Steige, Hannes Dittberner, Levi Yant, Mathieu Genete, Shamil Sunyaev, Vincent Castric, Xavier Vekemans, Outi Savolainen, Juliette de Meaux, Maintenance of Adaptive Dynamics and No Detectable Load in a Range-Edge Outcrossing Plant Population, Molecular Biology and Evolution, Volume 38, Issue 5, May 2021, Pages 1820–1836, https://doi.org/10.1093/molbev/msaa322

Maintenance of adaptive dynamics and no detectable load in a range-edge outcrossing plant population

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Author: Takou, Margarita1; Hämälä, Tuomas2; Koch, Evan M.3;
Organizations: 1Institute of Botany, University of Cologne, Cologne, Germany
2Department of Plant and Microbial Biology, University of Minnesota, St. Paul, MN, USA
3Department of Biomedical Informatics, Harvard Medical School, Boston, MA, USA
4School of Life Sciences, University of Nottingham, Nottingham, United Kingdom
5CNRS, UMR 8198 – Evo-Eco-Paleo, University of Lille, Lille, France
6Department of Ecology and Genetics, University of Oulu, Oulu, Finland
Format: article
Version: published version
Access: open
Online Access: PDF Full Text (PDF, 0.6 MB)
Persistent link: http://urn.fi/urn:nbn:fi-fe2021070240952
Language: English
Published: Oxford University Press, 2021
Publish Date: 2021-07-02
Description:

Abstract

During range expansion, edge populations are expected to face increased genetic drift, which in turn can alter and potentially compromise adaptive dynamics, preventing the removal of deleterious mutations and slowing down adaptation. Here, we contrast populations of the European subspecies Arabidopsis lyrata ssp. petraea, which expanded its Northern range after the last glaciation. We document a sharp decline in effective population size in the range-edge population and observe that nonsynonymous variants segregate at higher frequencies. We detect a 4.9% excess of derived nonsynonymous variants per individual in the range-edge population, suggesting an increase of the genomic burden of deleterious mutations. Inference of the fitness effects of mutations and modeling of allele frequencies under the explicit demographic history of each population predicts a depletion of rare deleterious variants in the range-edge population, but an enrichment for fixed ones, consistent with the bottleneck effect. However, the demographic history of the range-edge population predicts a small net decrease in per-individual fitness. Consistent with this prediction, the range-edge population is not impaired in its growth and survival measured in a common garden experiment. We further observe that the allelic diversity at the self-incompatibility locus, which ensures strict outcrossing and evolves under negative frequency-dependent selection, has remained unchanged. Genomic footprints indicative of selective sweeps are broader in the Northern population but not less frequent. We conclude that the outcrossing species A. lyrata ssp. petraea shows a strong resilience to the effect of range expansion.

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Series: Molecular biology and evolution
ISSN: 0737-4038
ISSN-E: 1537-1719
ISSN-L: 0737-4038
Volume: 38
Issue: 5
Pages: 1820 - 1836
DOI: 10.1093/molbev/msaa322
OADOI: https://oadoi.org/10.1093/molbev/msaa322
Type of Publication: A1 Journal article – refereed
Field of Science: 1184 Genetics, developmental biology, physiology
1181 Ecology, evolutionary biology
Subjects:
Funding: This project was funded by ERC projects No. 648617 Adaptoscope, No. 648321 (Novel) and Horizon 2020 research and innovation program (Grant No. ERC-StG 679056 HOTSPOT), via a grant to L.Y. The authors also thank the Région Hauts-de-France, the Ministère de l’Enseignement Supérieur et de la Recherche (CPER Climibio), the Biocenter Oulu and the European Fund for Regional Economic Development for their financial support.
Copyright information: © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com.
  https://creativecommons.org/licenses/by-nc/4.0/