This review collects together evidence that phenotypic traits often evolve as syndromes in Arabidopsis thaliana populations, pointing to extensive levels of ecological diversification within species.

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 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.

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. In plants, range expansion is often concomitant with a shift in mating system. In the Northern American subspecies Arabidopsis lyrata ssp lyrata, range expansion has been associated with the evolution of a mixed mating system and the accumulation of a burden of deleterious mutations in individual genotypes. Here, we contrast populations of the European sister subspecies Arabidopsis lyrata ssp petraea, which expanded its European range without a shift in mating system. We document a sharp decline in effective population size in the range-edge population and observe that non-synonymous variants segregate at higher frequency. Yet, the time since the bottleneck was too short to allow the accumulation of a detectable per-individual genomic burden of deleterious mutations in the Northern population. 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, adaptive mutations were present in sufficient number and effect size to maintain adaptive dynamics at the range-edge of the strictly outcrossing species Arabidopsis lyrata ssp. petraea.

Balancing selection is a form of natural selection maintaining diversity at the sites it targets and at linked nucleotide sites. Due to selection favouring heterozygosity, it has the potential to facilitate the accumulation of a “sheltered” load of tightly linked recessive deleterious mutations. However, precisely evaluating the extent of these effects has remained challenging. Taking advantage of plant self-incompatibility as one of the best-understood examples of long-term balancing selection, we provide a highly resolved picture of the genomic extent of balancing selection on the sheltered genetic load. We used targeted genome resequencing to reveal polymorphism of the genomic region flanking the self-incompatibility locus in three sample sets in each of the two closely related plant species Arabidopsis halleri and A. lyrata, and used 100 control regions from throughout the genome to factor out differences in demographic histories and/or sample structure. Nucleotide polymorphism increased strongly around the S-locus in all sample sets, but only over a limited genomic region, as it became indistinguishable from the genomic background beyond the first 25-30 kb. Genes in this chromosomal interval exhibited no excess of mutations at 0-fold degenerated sites relative to putatively neutral sites, hence revealing no detectable weakening of the efficacy of purifying selection even for these most tightly linked genes. Overall, our results are consistent with the predictions of a narrow genomic influence of linkage to the S-locus, and clarify how natural selection in one genomic region affects the evolution of the adjacent genomic regions.