Adaptation to heavy-metal contaminated environments proceeds via selection on pre-existing genetic variation

Abstract

Across a species range, islands of stressful habitats impose similar selection pressures on isolated populations. It is as yet unclear, when populations respond to these selective pressures, the extent to which this results in convergent genetic evolution and whether convergence is due to independent mutations or shared ancestral variation. We address these questions investigating a classic example of adaptation by natural selection - the colonization of plant species to heavy metal contaminated soils. We use field-based reciprocal transplant experiments to demonstrate that mine alleles at a major copper tolerance QTL, Tol1, are strongly selected in the mine environment, but are neutral, or nearly so, in the off-mine environment. We assemble the genome of a mine adapted genotype and identify regions of this genome in tight genetic linkage to Tol1. We discover Tol1 candidate genes that exhibit significantly large differences in expression between tolerant and non-tolerant genotypes or in allele frequency between mine/off-mine population pairs. We identify a single gene, a multicopper oxidase, which exhibits both large differences in expression and allele frequency. Furthermore, patterns of genetic variation at the five loci with the greatest difference in allele frequency between populations, including the multicopper oxidase, are consistent with selection acting upon beneficial haplotypes that predates the existence of the copper mine habitat. We estimate the age of selected Tol1 haplotype to be at least 1700 years old and was at a frequency of 0.4-0.6% in the ancestral population when mining was initiated 150 years ago. These results suggest that adaptation to the mine habitat routinely occurs via selection on ancestral variation, rather than independent de-novo mutations or migration between populations.