Abstract
It is a plausible hypothesis that parallel adaptation events to the same environmental challenge should result in genetic changes of similar or identical effects, depending on the underlying fitness landscapes. However, systematic testing of this is scarce. Here we examine this hypothesis in two closely related plant species, Arabidopsis halleri and Arabidopsis arenosa, which co-occur at two calamine metalliferous (M) sites harbouring toxic levels of the heavy metals zinc and cadmium. We conduct individual genome resequencing alongside soil elemental analysis for 64 plants from eight populations on M and non-metalliferous (NM) soils, and identify genomic footprints of selection and local adaptation. Selective sweep and environmental association analyses indicate a modest degree of gene as well as functional network convergence, whereby the proximal molecular factors mediating this convergence mostly differ between site pairs and species. Notably, we observe repeated selection on identical single nucleotide polymorphisms in several A. halleri genes at two independently colonized M sites. Our data suggest that species-specific metal handling and other biological features could explain a low degree of convergence between species. The parallel establishment of plant populations on calamine M soils involves convergent evolution, which will probably be more pervasive across sites purposely chosen for maximal similarity in soil composition.This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’.
Highlights
Most plants cannot rapidly escape hostile environments
The objective of this study was to probe for candidate genes that have undergone convergent selection on calamine M soils
We focused on genes with evidence for selection at two M sites, each of them in comparison to a geographically proximal NM site, in the two closely related and genetically tractable species A. halleri and A. arenosa
Summary
Most plants cannot rapidly escape hostile environments. they present powerful models for the study of adaptation. Metalliferous (M) soils are defined as rich in at least one class B and borderline trace metal element [1], are usually nutritionally imbalanced [2,3], and arise either through geological (e.g. ancient outcrop) or human (e.g. mining, metal smelter) activity Such soils are generally toxic to plants and host a sparse, species-poor characteristic vegetation of adapted, often endemic extremophiles, so-called metallophytes [4]. Experimental studies in synthetic hydroponic media have demonstrated species-wide hypertolerance to both metals in comparison to the closely related species A. lyrata and Arabidopsis thaliana [12,13] These same studies established that A. halleri accessions originating from calamine M soils exhibit enhanced Zn and/or Cd hypertolerance, which is probably the result of local adaptation. We show that this gene exhibits a series of convergent derived sequence variants in individuals originating from M sites, and appears to have undergone a loss of function in populations at NM sites
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