Maintenance of adaptive dynamics in a bottlenecked population that retained strict outcrossing

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 sub-species 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 non-synonymous variants segregate at higher frequencies. We detect a 4.9% excess of derived non-synonymous variants per individual, suggesting an increase of the genomic burden of deleterious mutations in the range-edge population. Inference of fitness effects under the explicit demographic history of each population shows that the range-edge population is depleted in rare deleterious variants, but enriched for fixed ones, resulting in a small net difference in per-individual burden between the range-edge and –core populations. Consistent with this prediction, the range-edge population was 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, has remained unchanged. Genomic footprints indicative of selective sweeps were broader in the Northern population but not less frequent. This indicates that, despite a dramatic bottleneck and a mild expansion load, adaptive mutations were present in sufficient number to maintain adaptive dynamics at the range-edge of the strictly outcrossing species Arabidopsis lyrata ssp. petraea. indicative of selective sweeps were broader in the Northern population but not less frequent. The joint modeling of the distribution of fitness effects of the two populations indicates that most adaptive mutations have small effects on fitness, but their proportion is similar in the two populations. In addition, we detected no significant increase in deleterious mutations, the accumulated genetic load at the whole genome level in the northern population. These results suggest that adaptive dynamics were maintained at the range-edge of the strictly outcrossing species Arabidopsis lyrata spp petraea despite a dramatic bottleneck.