TY - JOUR
T1 - Evolutionary dynamics of quantitative variation in an adaptive trait at the regional scale
T2 - The case of zinc hyperaccumulation in Arabidopsis halleri
AU - Babst-Kostecka, Alicja
AU - Schat, Henk
AU - Saumitou-Laprade, Pierre
AU - Grodzińska, Krystyna
AU - Bourceaux, Angélique
AU - Pauwels, Maxime
AU - Frérot, Hélène
N1 - Funding Information:
We thank Patrik Waldmann for input with the INLA methodology; Flurin Babst and Gregory King for editorial comments; Ophélie Ronce for fruitful discussion; and Cécile Godé, Anna Szczerbińska and Zbigniew Kostecki for technical assistance. The authorities of the town of Bolesław and ZGH Bolesław S.A. supported this research by permitting and facilitating the sampling and monitoring of metalliferous sites. The Tatra National Park granted permits to collect samples within the park boundaries. The research was supported by the POWROTY/REINTEGRATION programme of the Foundation for Polish Science cofinanced by the European Union under the European Regional Development Fund (POWROTY/2016-1/1), statutory fund and Programme for Young Scientists from the W. Szafer Institute of Botany PAS (4604/E-37/M/2014/1/2014), and GDRI-LOCOMET network (CNRS).
Funding Information:
The POWROTY/REINTEGRATION programme of the Foundation for Polish Science co-financed by the European Union under the European Regional Development Fund, Grant/Award Number: POWROTY/ 2016-1/1; Statutory fund and Program for Young Scientists from the W. Szafer Institute of Botany, PAS, Grant/Award Number: 4604/E-37/M/2014/1/2014; GDRI-LOCOMET network (CNRS)
Funding Information:
We thank Patrik Waldmann for input with the INLA methodology; Flurin Babst and Gregory King for editorial comments; Ophélie Ronce for fruitful discussion; and Cécile Godé, Anna Szczerbińska and Zbigniew Kostecki for technical assistance. The authorities of the town of Bolesław and ZGH Bolesław S.A. supported this research by permitting and facilitating the sampling and monitoring of metalliferous sites. The Tatra National Park granted permits to collect samples within the park boundaries. The research was supported by the POWROTY/REINTEGRATION programme of the Foundation for Polish Science cofinanced by the European Union under the European Regional Development Fund (POWROTY/2016‐ 1/1), statutory fund and Programme for Young Scientists from the W. Szafer Institute of Botany PAS (4604/E‐37/M/2014/1/2014), and GDRI‐LOCOMET network (CNRS).
Publisher Copyright:
© 2018 John Wiley & Sons Ltd
PY - 2018/8
Y1 - 2018/8
N2 - 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.
AB - 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.
KW - local adaptation
KW - metal trace elements
KW - population divergence
KW - pseudometallophyte
KW - relic
KW - selection
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U2 - 10.1111/mec.14800
DO - 10.1111/mec.14800
M3 - Article
AN - SCOPUS:85051737546
SN - 0962-1083
VL - 27
SP - 3257
EP - 3273
JO - Molecular Ecology
JF - Molecular Ecology
IS - 16
ER -