Genomic basis of parallel adaptation varies with divergence in<i>Arabidopsis</i>and its relatives

Bohutínská, Magdalena; Vlček, Jakub; Yair, Sivan; Laenen, Benjamin; Konečná, Veronika; Fracassetti, Marco; Slotte, Tanja; Kolář, Filip

doi:10.1101/2020.03.24.005397

Cited by 20 publications

(42 citation statements)

References 106 publications

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“…Replicated phenotypic shifts in response to similar environmental pressures that are stable over two generations in cultivation suggest the role of selection triggered by the stressful alpine environment. Our findings open new avenues for studying convergent genetic underpinnings of phenotypic parallelism currently being addressed by a follow-up study (Bohutínská et al, 2020). Indeed, alpine A. arenosa is a particularly well-suited model for following such questions due to negligible neutral divergence between ecotypes within each region and lack of strong bottleneck, both of which mitigate potentially confounding signals of past demographic events.…”

Section: Resultsmentioning

confidence: 88%

Parallel Alpine Differentiation in Arabidopsis arenosa

et al. 2020

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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.

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Section: Resultsmentioning

confidence: 88%

Parallel Alpine Differentiation in Arabidopsis arenosa

et al. 2020

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“…For example, Preite et al [51] demonstrated a moderate level of molecular parallelism in adaptation to calamine metalliferous soils within Arabidopsis species, but less parallelism between species. In addition, a recent study [52] discovered that the degree of molecular parallelism decreases with increasing divergence between lineages in Arabidopsis alpine species. Third, population genetic modeling predicts that traits with pleiotropic constraint are more likely to demonstrate molecular parallelism [53].…”

Section: Discussionmentioning

confidence: 99%

Molecular Parallelism Underlies Convergent Highland Adaptation of Maize Landraces

Wang

Josephs

Lee

et al. 2020

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Convergent phenotypic evolution provides some of the strongest evidence for adaptation. However, the extent to which recurrent phenotypic adaptation has arisen via parallelism at the molecular level remains unresolved, as does the evolutionary origin of alleles underlying such adaptation. Here, we investigate genetic mechanisms of convergent highland adaptation in maize landrace populations and evaluate the genetic sources of recurrently selected alleles. Population branch excess statistics reveal strong evidence of parallel adaptation at the level of individual SNPs, genes and pathways in four independent highland maize populations, even though most SNPs show unique patterns of local adaptation. The majority of selected SNPs originated via migration from a single population, most likely in the Mesoamerican highlands. Polygenic adaptation analyses of quantitative traits reveal that alleles affecting flowering time are significantly associated with elevation, indicating the flowering time pathway was targeted by highland adaptation. In addition, repeatedly selected genes were significantly enriched in the flowering time pathway, indicating their significance in adapting to highland conditions. Overall, our study system represents a promising model to study convergent evolution in plants with potential applications to crop adaptation across environmental gradients.

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“…We calculated pairwise FST 81 for nonoverlapping 1 kb windows along the genome with the minimum of 10 SNPs per window using the custom script (https://github.com/mbohutinska/ScanTools_ProtEvol) based on ScanTools pipeline that has been successfully applied in our previous analyses of autotetraploid A. arenosa 8 . The window size is larger than average genome-wide LD decay of genotypic correlations (150-800 bp) estimated in A. arenosa 82 . We identified the upper 99% quantile of all 1 kb windows in the empirical distribution of FST metric per each population pair.…”

Section: Window-based Scans For Directional Selectionmentioning

confidence: 95%

Parallel adaptation in autopolyploidArabidopsis arenosais dominated by repeated recruitment of shared alleles

Konečná

Bray

Vlček

et al. 2021

Preprint

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Relative contributions of pre-existing vs de novo genomic variation to adaptation are poorly understood, especially in polyploid organisms, which maintain increased variation. 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 discovered substantial parallelism in candidate genes involved in ion homeostasis. We further modelled parallel selection and inferred 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.

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Genomic basis of parallel adaptation varies with divergence inArabidopsisand its relatives

Cited by 20 publications

References 106 publications

Parallel Alpine Differentiation in Arabidopsis arenosa

Parallel Alpine Differentiation in Arabidopsis arenosa

Molecular Parallelism Underlies Convergent Highland Adaptation of Maize Landraces

Parallel adaptation in autopolyploidArabidopsis arenosais dominated by repeated recruitment of shared alleles

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