Parallel local adaptation to an alpine environment in Arabidopsis arenosa

Parallel local adaptation, that is, when distinct genetic lineages independently adapt to the same selective environment, provides strong evidence for the action of natural selection. A few cases of parallel local adaptation were reported in plants but underlying mechanisms promoting or preventing the parallel response, such as the balance between migration and selection, were rarely quantified. Here, we conducted a transplant experiment to test whether distinct foothill-alpine population pairs of Arabidopsis arenosa exhibited similar adaptive responses to a contrasting alpine environment. We further investigated selection and migration patterns in these populations. Seedlings of 16 foothill and alpine populations of A. arenosa from four distinct mountain regions (one occupied by diploid and three by tetraploid populations) were transplanted into one low- and one high-elevation site. We recorded fitness proxies over two growing seasons to test whether the elevation-of-origin advantage was manifested in the same way across the four regions of origin. Then, we quantified the strength of selection on the traits at each transplantation site and used coalescent simulations to estimate past gene flow intensity between each pair of foothill and alpine populations in each region. We demonstrated that the four pairs of populations exhibited similar adaptive responses to elevation difference in terms of survival, number of flowering plants, stem height and accumulation of above-ground dry biomass; the other traits (rosette size, number of leaves, stems and flowers) exhibited rather regional-specific patterns. In addition, we found minor effects of ploidy level on the fitness proxies recorded. Our selection and migration analysis revealed that parallel local adaptation was probably achieved by differential selective pressure at low versus high elevation in combination with lack or limited gene flow between foothill and alpine populations. Synthesis. We show that the previously documented strong morphological and genetic distinctness of alpine A. arenosa compared to their foothill counterparts, which has been hypothesized to be driven by natural selection, is indeed mirrored in fitness differences consistent with parallel local adaptation. Our results provide experimental support for the repeatability of adaptive evolution and highlight the prominent role of divergent selection.

Automated summary

Parallel local adaptation, when different genetic lineages independently adapt to the same selective environment, was investigated in Arabidopsis arenosa populations from four distinct mountain regions. The study found that the populations exhibited similar adaptive responses to elevation difference, indicating parallel local adaptation. The results highlight the role of divergent selection and provide experimental support for the repeatability of adaptive evolution.