Maintenance of Adaptive Dynamics and No Detectable Load in a Range-Edge Outcrossing Plant Population

Takou, Margarita; H�m�l�, Tuomas; Koch, Evan M.; Steige, Kim A.; Dittberner, Hannes; Yant, Levi; Genete, Mathieu; Sunyaev, Shamil; Castric, Vincent; Vekemans, Xavier; Savolainen, Outi; Meaux, Juliette de

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.

• Journal Article Type: Article
• Acceptance Date: Nov 30, 2020
• Online Publication Date: Jan 22, 2021
• Publication Date: 2021-05
• Deposit Date: Sep 24, 2021
• Publicly Available Date: Sep 29, 2021
• Journal: Molecular biology and evolution
• Print ISSN: 0737-4038
• Electronic ISSN: 1537-1719
• Publisher: Oxford University Press (OUP)
• Peer Reviewed: Peer Reviewed
• Volume: 38
• Issue: 5
• Pages: 1820-1836
• DOI: https://doi.org/10.1093/molbev/msaa322
• Public URL: https://nottingham-repository.worktribe.com/output/5619401
• Publisher URL: https://academic.oup.com/mbe/article/38/5/1820/6108107