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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.

In plants, local adaptation across species range is frequent. Yet, much has to be discovered on its environmental drivers, the underlying functional traits and their molecular determinants. Genome scans are popular to uncover outlier loci potentially involved in the genetic architecture of local adaptation, however links between outliers and phenotypic variation are rarely addressed. Here we focused on adaptation of teosinte populations along two elevation gradients in Mexico that display continuous environmental changes at a short geographical scale. We used two common gardens, and phenotyped 18 traits in 1664 plants from 11 populations of annual teosintes. In parallel, we genotyped these plants for 38 microsatellite markers as well as for 171 outlier single nucleotide polymorphisms (SNPs) that displayed excess of allele differentiation between pairs of lowland and highland populations and/or correlation with environmental variables. Our results revealed that phenotypic differentiation at 10 out of the 18 traits was driven by local selection. Trait covariation along the elevation gradient indicated that adaptation to altitude results from the assembly of multiple co-adapted traits into a complex syndrome: as elevation increases, plants flower earlier, produce less tillers, display lower stomata density and carry larger, longer and heavier grains. The proportion of outlier SNPs associating with phenotypic variation, however, largely depended on whether we considered a neutral structure with 5 genetic groups (73.7%) or 11 populations (13.5%), indicating that population stratification greatly affected our results. Finally, chromosomal inversions were enriched for both SNPs whose allele frequencies shifted along elevation as well as phenotypically-associated SNPs. Altogether, our results are consistent with the establishment of an altitudinal syndrome promoted by local selective forces in teosinte populations in spite of detectable gene flow. Because elevation mimics climate change through space, SNPs that we found underlying phenotypic variation at adaptive traits may be relevant for future maize breeding., Author summary Across their native range species encounter a diversity of habitats promoting local adaptation of geographically distributed populations. While local adaptation is widespread, much has yet to be discovered about the conditions of its emergence, the targeted traits, their molecular determinants and the underlying ecological drivers. Here we employed a reverse ecology approach, combining phenotypes and genotypes, to mine the determinants of local adaptation of teosinte populations distributed along two steep altitudinal gradients in Mexico. Evaluation of 11 populations in two common gardens located at mid-elevation pointed to adaptation via an altitudinal multivariate syndrome, in spite of gene flow. We scanned genomes to identify loci with allele frequency shifts along elevation, a subset of which associated to trait variation. Because elevation mimics climate change through space, these polymorphisms may be relevant for future maize breeding.

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 foot-prints 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 .

In natural populations genetic variation is shaped by a complex interplay of evolutionary forces. For this thesis, I investigated patterns of natural variation in two selfing Brassicaceae species with contrasting demographic histories. I addressed the following questions: i) how do complex traits evolve in selfing populations when genetic drift is maximized and recombination strongly limited? ii) how can such populations be maintained when they are severely endangered? To answer the first question, I investigated natural variation in stomatal traits and water-use efficiency in 330 European accessions of the widely distributed human commensal Arabidopsis thaliana. A genome-wide association study (GWAS) revealed that natural variation in stomata density, stomata size and water-use efficiency has a complex largely polygenic genetic basis with few major effect loci at low frequency. Moreover, I found a significant correlation between stomata size and water-use efficiency, which has a genetic basis. All traits were significantly correlated with climatic variables and excessively differentiated among populations, suggesting a role of these traits in local adaptation. To answer the second question, I investigated the distribution of genetic diversity in Arabis nemorensis, a strongly endangered floodplain species. A. nemorensis is a target species in an ecological restoration project at the Upper Rhine. To assess whether genetic diversity was maintained in the restoration process I genotyped and compared individuals from four pristine and six restored sites. Genetic analysis revealed that, in these sites, A. nemorensis co-occurs with its morphologically highly similar but ecologically divergent sibling species Arabis sagittata and that they naturally hybridize. In both species, there was no difference in the level of genetic diversity between pristine and restored sites. In A. sagittata, restoration resulted in admixture of previously isolated genotypes, suggesting that restoration can increase the adaptive potential of populations, depending on the initial structure of the donor populations. Population genetic analysis of 15 additional pristine sites in Germany in Austria revealed that A. nemorensis is frequently confused with its sibling species, A. sagittata and Arabis hirsuta, in botanical surveys, indicating that the size of its total population might be overestimated. In three populations A. nemorensis co-occurs with A. hirsuta. However, the Rhine population is the only contact zone between A. nemorensis and A. sagittata I found. Intraspecific genetic diversity was low both in A. nemorensis and A. sagittata, likely due to habitat degradation. Thus, interspecific gene-flow through hybridization could be source of novel genetic variation for both species, which could be critical for their survival. Patterns of genomic ancestries of hybrids suggest that hybrids naturally back-cross with both parents, but preferentially with A. sagittata, which might have resulted in interspecific gene-flow. To test for interspecific gene-flow, I analyzed whole-genome sequences of 35 individuals from sympatric and allopatric populations of both species and an outgroup. In both sympatric and allopatric populations, I found signatures of substantial gene-flow among parental species, which was stronger from A. nemorensis into A. sagittata than vice versa and strongest into the sympatric A. sagittata population. Haplotype network analyses suggest that gene-flow in this population was both recent and ancestral. To assess the adaptive potential of interspecific gene-flow, I investigated the phenotypic divergence of the species. I found that they significantly differ in several potentially adaptive traits: phenology, morphology, defense and flooding tolerance, highlighting the adaptive potential of interspecific gene-flow. Yet, additional studies will be needed to assess whether gene-flow is indeed adaptive.