Genomic basis and phenotypic manifestation of (non-)parallel serpentine adaptation in Arabidopsis arenosa.

Parallel evolution is common in nature and provides one of the most compelling examples of rapid environmental adaptation. In contrast to the recent burst of studies addressing genomic basis of parallel evolution, integrative studies linking genomic and phenotypic parallelism are scarce. Edaphic islands of toxic serpentine soils provide ideal systems for studying rapid parallel adaptation in plants, imposing strong, spatially replicated selection on recently diverged populations. We leveraged threefold independent serpentine adaptation of Arabidopsis arenosa and combined reciprocal transplants, ion uptake phenotyping, and available genome-wide polymorphisms to test if parallelism is manifested to a similar extent at both genomic and phenotypic levels. We found pervasive phenotypic parallelism in functional traits yet with varying magnitude of fitness differences that was congruent with neutral genetic differentiation between populations. Limited costs of serpentine adaptation suggest absence of soil-driven trade-offs. On the other hand, the genomic parallelism at the gene level was significant, although relatively minor. Therefore, the similarly modified phenotypes, for example, of ion uptake arose possibly by selection on different loci in similar functional pathways. In summary, we bring evidence for the important role of genetic redundancy in rapid adaptation involving traits with polygenic architecture.

Parallel adaptation in autopolyploid Arabidopsis arenosa is dominated by repeated recruitment of shared alleles.

Relative contributions of pre-existing vs de novo genomic variation to adaptation are poorly understood, especially in polyploid organisms. We assess this in high resolution using autotetraploid Arabidopsis arenosa, which repeatedly adapted to toxic serpentine soils that exhibit skewed elemental profiles. Leveraging a fivefold replicated serpentine invasion, we assess selection on SNPs and structural variants (TEs) in 78 resequenced individuals and discover significant parallelism in candidate genes involved in ion homeostasis. We further model parallel selection and infer repeated sweeps on a shared pool of variants in nearly all these loci, supporting theoretical expectations. A single striking exception is represented by TWO PORE CHANNEL 1, which exhibits convergent evolution from independent de novo mutations at an identical, otherwise conserved site at the calcium channel selectivity gate. Taken together, this suggests that polyploid populations can rapidly adapt to environmental extremes, calling on both pre-existing variation and novel polymorphisms.

Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives.

Parallel adaptation provides valuable insight into the predictability of evolutionary change through replicated natural experiments. A steadily increasing number of studies have demonstrated genomic parallelism, yet the magnitude of this parallelism varies depending on whether populations, species, or genera are compared. This led us to hypothesize that the magnitude of genomic parallelism scales with genetic divergence between lineages, but whether this is the case and the underlying evolutionary processes remain unknown. Here, we resequenced seven parallel lineages of two Arabidopsis species, which repeatedly adapted to challenging alpine environments. By combining genome-wide divergence scans with model-based approaches, we detected a suite of 151 genes that show parallel signatures of positive selection associated with alpine colonization, involved in response to cold, high radiation, short season, herbivores, and pathogens. We complemented these parallel candidates with published gene lists from five additional alpine Brassicaceae and tested our hypothesis on a broad scale spanning ∼0.02 to 18 My of divergence. Indeed, we found quantitatively variable genomic parallelism whose extent significantly decreased with increasing divergence between the compared lineages. We further modeled parallel evolution over the Arabidopsis candidate genes and showed that a decreasing probability of repeated selection on the same standing or introgressed alleles drives the observed pattern of divergence-dependent parallelism. We therefore conclude that genetic divergence between populations, species, and genera, affecting the pool of shared variants, is an important factor in the predictability of genome evolution.

Parallel Alpine Differentiation in Arabidopsis arenosa.

Parallel evolution provides powerful natural experiments for studying repeatability of evolution and genomic basis of adaptation. Well-documented examples from plants are, however, still rare, as are inquiries of mechanisms driving convergence in some traits while divergence in others. Arabidopsis arenosa, a predominantly foothill species with scattered morphologically distinct alpine occurrences is a promising candidate. Yet, the hypothesis of parallelism remained untested. We sampled foothill and alpine populations in all regions known to harbor the alpine ecotype and used SNP genotyping to test for repeated alpine colonization. Then, we combined field surveys and a common garden experiment to quantify phenotypic parallelism. Genetic clustering by region but not elevation and coalescent simulations demonstrated parallel origin of alpine ecotype in four mountain regions. Alpine populations exhibited parallelism in height and floral traits which persisted after two generations in cultivation. In contrast, leaf traits were distinctive only in certain region(s), reflecting a mixture of plasticity and genetically determined non-parallelism. We demonstrate varying degrees and causes of parallelism and non-parallelism across populations and traits within a plant species. Parallel divergence along a sharp elevation gradient makes A. arenosa a promising candidate for studying genomic basis of adaptation.

The Evolutionary Genomics of Serpentine Adaptation.

Serpentine barrens are among the most challenging settings for plant life. Representing a perfect storm of hazards, serpentines consist of broadly skewed elemental profiles, including abundant toxic metals and low nutrient contents on drought-prone, patchily distributed substrates. Accordingly, plants that can tolerate the challenges of serpentine have fascinated biologists for decades, yielding important insights into adaptation to novel ecologies through physiological change. Here we highlight recent progress from studies which demonstrate the power of serpentine as a model for the genomics of adaptation. Given the moderate - but still tractable - complexity presented by the mix of hazards on serpentine, these venues are well-suited for the experimental inquiry of adaptation both in natural and manipulated conditions. Moreover, the island-like distribution of serpentines across landscapes provides abundant natural replicates, offering power to evolutionary genomic inference. Exciting recent insights into the genomic basis of serpentine adaptation point to a partly shared basis that involves sampling from common allele pools available from retained ancestral polymorphism or via gene flow. However, a lack of integrated studies deconstructing complex adaptations and linking candidate alleles with fitness consequences leaves room for much deeper exploration. Thus, we still seek the crucial direct link between the phenotypic effect of candidate alleles and their measured adaptive value - a prize that is exceedingly rare to achieve in any study of adaptation. We expect that closing this gap is not far off using the promising model systems described here.

Parallel colonization of subalpine habitats in the central European mountains by Primula elatior.

The island-like distribution of subalpine habitats across mountain ranges can trigger the parallel evolution of locally adapted ecotypes. Such naturally replicated scenarios allow testing hypotheses on how elevational differentiation structures genetic diversity within species. Nevertheless, the parallel colonization of subalpine habitats across different mountain ranges has only rarely been documented with molecular data. We chose Primula elatior (Primulaceae), naturally spanning entire elevation range in multiple mountain regions of central Europe, to test for the origin of its scattered subalpine populations. Nuclear microsatellite variation revealed three genetic groups corresponding with the distinct study regions. We found that genetic differentiation between foothill and subalpine populations within each region was relatively low, suggesting that the colonization of subalpine habitats occurred independently within each mountain range. Furthermore, the strongest differentiation was usually found between the subalpine populations suggesting that mountain ridges may act as migration barriers that can reduce gene flow more strongly than elevational differences between foothill and subalpine populations. Finally, we found that subalpine colonization did not result in a loss of genetic diversity relative to foothill populations in agreement with the high migration rates that we document here between the subalpine and the foothill populations. In summary, our study shows subalpine Primula elatior populations are genetically diverse and distinct results of parallel colonization events from multiple foothill gene pools.