Borrowed alleles and convergence in serpentine adaptation

Abstract

Serpentine barrens represent extreme hazards for plant colonists. These sites are characterized by high porosity leading to drought, lack of essential mineral nutrients, and phytotoxic levels of metals. Nevertheless, nature forged populations adapted to these challenges. Here, we use a population-based evolutionary genomic approach coupled with elemental profiling to assess how autotetraploid Arabidopsis arenosa adapted to a multichallenge serpentine habitat in the Austrian Alps. We first demonstrate that serpentine-adapted plants exhibit dramatically altered elemental accumulation levels in common conditions, and then resequence 24 autotetraploid individuals from three populations to perform a genome scan. We find evidence for highly localized selective sweeps that point to a polygenic, multitrait basis for serpentine adaptation. Comparing our results to a previous study of independent serpentine colonizations in the closely related diploid Arabidopsis lyrata in the United Kingdom and United States, we find the highest levels of differentiation in 11 of the same loci, providing candidate alleles for mediating convergent evolution. This overlap between independent colonizations in different species suggests that a limited number of evolutionary strategies are suited to overcome the multiple challenges of serpentine adaptation. Interestingly, we detect footprints of selection in A. arenosa in the context of substantial gene flow from nearby off-serpentine populations of A. arenosa, as well as from A. lyrata. In several cases, quantitative tests of introgression indicate that some alleles exhibiting strong selective sweep signatures appear to have been introgressed from A. lyrata. This finding suggests that migrant alleles may have facilitated adaptation of A. arenosa to this multihazard environment.adaptation | plant | gene flow | population genomics S erpentine barrens offer powerful venues for the study of multitrait adaptations. Soils at these sites feature dramatically skewed elemental contents, phytotoxic levels of heavy metals, drought risk, and very poor mineral nutrition (1-3). A defining characteristic of serpentine soils is a greatly reduced Ca:Mg ratio along with low K, N, and P, resulting in severe ion homeostasis challenges for plant colonists (4-6). Serpentine soils are also highly porous and thus chronically drought prone. As a result of these challenges, serpentine barrens are characterized by minimal ecosystem productivity and high rates of endemism (reviewed in refs. 2 and 3). Evolution has nevertheless repeatedly forged plant populations that overcome these hazards, making serpentine sites an important natural model for ecology, evolution, and physiology. Given the quantifiable challenges of serpentine adaptation presented by strongly skewed elemental levels and dehydration risk, adapted populations present a valuable opportunity to identify loci underlying adaptations important for understanding basic evolutionary processes, as well as candidate genes for rational crop design for tolerance of ...

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