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

Margarita Takou (1) , Tuomas Hämälä (2) , Evan M Koch (3) , Kim A Steige (1) , Hannes Dittberner (1) , Levi Yant , Mathieu Genete (4) , Shamil Sunyaev (5) , Vincent Castric (4) , Xavier Vekemans (4) , Outi Savolainen (6) , Juliette De Meaux (1)

1 University of Cologne
2 Departments of Ecology, Evolution and Behavior and Plant and Microbial Biology, University of Minnesota
3 DBMI - Department of Biomedical Informatics [Harvard]
4 Evo-Eco-Paléo (EEP) - Évolution, Écologie et Paléontologie (Evo-Eco-Paleo) - UMR 8198
5 UON - University of Nottingham, UK
6 Ecology and Genetics Research Unit, University of Oulu, 90014 Oulu

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 rangeedge 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.

Mots clés: range expansion; adaptation; deleterious mutations; self-incompatibility locus; negative frequencydependent selection; selective sweeps

Domaines: Génétique des populations [q-bio.PE]

Margarita Takou, Tuomas Hämälä, Evan M Koch, Kim A Steige, Hannes Dittberner, et al.. Maintenance of Adaptive Dynamics and No Detectable Load in a Range-Edge Outcrossing Plant Population. Molecular Biology and Evolution, 2021, 38, pp.1820 - 1836. ⟨10.1093/molbev/msaa322⟩. ⟨hal-03260407⟩