Data from: Evolutionary dynamics of quantitative variation in an adaptive trait at the regional scale: the case of zinc hyperaccumulation in Arabidopsis halleri

Metal hyperaccumulation in plants is an ecological trait whose biological significance remains debated, in particular because the selective pressures that govern its evolutionary dynamics are complex. One of the possible causes of quantitative variation in hyperaccumulation may be local adaptation to metalliferous soils. Here we explored the population genetic structure of Arabidopsis halleri at fourteen metalliferous and non-metalliferous sampling sites in Southern Poland. The results were integrated with a quantitative assessment of variation in zinc hyperaccumulation to trace local adaptation. We identified a clear hierarchical structure with two distinct genetic groups at the upper level of clustering. Interestingly, these groups corresponded to different geographic sub-regions, rather than to ecological types (i.e. metallicolous vs non-metallicolous). Also, approximate Bayesian computation analyses suggested that the current distribution of A. halleri in Southern Poland could be relictual as a result of habitat fragmentation caused by climatic shifts during the Holocene, rather than due to recent colonization of industrially polluted sites. In addition, we find evidence that some non-metallicolous lowland populations may have actually derived from metallicolous populations. Meanwhile, the distribution of quantitative variation in zinc hyperaccumulation did separate metallicolous and non-metallicolous accessions, indicating more recent adaptive evolution and diversifying selection between metalliferous and non-metalliferous habitats. This suggests that zinc hyperaccumulation evolves both ways – towards higher levels at non-metalliferous sites and lower levels at metalliferous sites. Our results open a new perspective on possible evolutionary relationships between A. halleri edaphic types that may inspire future genetic studies of quantitative variation in metal hyperaccumulation.

植物金属超富集（metal hyperaccumulation）是一类生态性状，其生物学意义迄今仍存争议，尤其因其进化动态所受选择压力较为复杂。导致超富集性状数量变异的潜在诱因之一，可能是植物对含金属土壤的本地适应。本研究针对波兰南部14个含金属与非含金属采样位点，对霍尔氏拟南芥（Arabidopsis halleri）的种群遗传结构展开探究，并将研究结果与锌超富集性状变异的定量评估相结合，以追踪本地适应的演化轨迹。分析结果显示，该物种的种群存在清晰的层级遗传结构，在聚类分析的最高层级可区分出两个独立的遗传类群。值得注意的是，这两个类群对应不同的地理亚区，而非预设的生态类型（即金属富集型与非金属富集型）。此外，近似贝叶斯计算（approximate Bayesian computation）分析表明，波兰南部霍尔氏拟南芥的当前分布可能属于孑遗分布，其成因是全新世时期气候变迁引发的生境破碎化，而非近期对工业污染位点的定植。本研究同时发现，部分非金属富集型低地种群实际起源于金属富集型种群。与此同时，锌超富集性状的数量变异分布确实能够有效区分金属富集型与非金属富集型种质株系，这提示两类生境间存在较近期的适应性进化与分化选择。研究结果表明，锌超富集性状可向两个方向演化：在非含金属生境中向更高富集水平演化，而在含金属生境中则向更低富集水平演化。本研究为霍尔氏拟南芥不同土壤生境型之间的进化关系提供了全新视角，可为未来针对金属超富集性状数量变异的遗传学研究提供重要借鉴。