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

Abstract

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 nonmetalliferous 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 subregions, rather than to ecological types (i.e., metallicolous vs. nonmetallicolous). 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 nonmetallicolous lowland populations may have actually derived from metallicolous populations. Meanwhile, the distribution of quantitative variation in zinc hyperaccumulation did separate metallicolous and nonmetallicolous accessions, indicating more recent adaptive evolution and diversifying selection between metalliferous and nonmetalliferous habitats. This suggests that zinc hyperaccumulation evolves both ways-towards higher levels at nonmetalliferous 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.

Phylogenetic and geographic distribution of nickel hyperaccumulation in neotropical Psychotria

“…Regulation of elemental uptake, including processes of exclusion, accumulation, and hyperaccumulation, has broad implications for plant biochemistry, physiology, ecology, and evolution. The extreme elemental concentrations found in hyperaccumulators have made them useful systems for study of nutrient acquisition, transport, and homeostasis (van der Ent et al., ), plant–herbivore interactions (Boyd, ), plant–pathogen interactions (Hörger et al., ), and evolutionary dynamics (Babst‐Kostecka et al., ), to name a few examples. Hyperaccumulation may also have applied significance in the development of biotechnology such as phytoremediation (Chaney et al., ) and agromining (van der Ent et al., ; Chaney et al., ; Kidd et al., ).…”

Transmembrane transport and stress response genes play an important role in adaptation of Arabidopsis halleri to metalliferous soils

“…1 ). Arabidopsis halleri populations from these four locations hypertolerate and hyperaccumulate TMEs 9 , 21 . However, the history and soil composition of the four sites differ.…”

“…However, we think that this is counterbalanced by the categorical sampling design (replicated populations of M and NM sites) and the strong selection pressure that such TME-enriched soils exert on plants, complemented by the genome-wide perspective. Furthermore, the selected populations exhibit a wide range of TME concentrations in plant shoots and represent the genetic diversity and recently refined population genetic structure of A. halleri in southern Poland 21 .…”

“…3a,b ) – and one sub-alpine NM location in the northern foothills of the Tatra Mountains (NM_PL35). A recent study showed that plants from Olkusz and Niepołomice Forest regions belong to the same higher-level genetic cluster, while samples from the Tatra region were assigned to another cluster 21 . The latter cluster is considered to be the most ancestral and has the highest estimate of effective population size of all populations from southern Poland 21 .…”

“…A recent study showed that plants from Olkusz and Niepołomice Forest regions belong to the same higher-level genetic cluster, while samples from the Tatra region were assigned to another cluster 21 . The latter cluster is considered to be the most ancestral and has the highest estimate of effective population size of all populations from southern Poland 21 . At each site, we collected leaves of 30 A.halleri plants every 4 m along transects to avoid potential clones and dried them on silicagel.…”