Evolutionary footprints of a cold relic in a rapidly warming world

With accelerating global warming, understanding the evolutionary dynamics of plant adaptation to environmental change is increasingly urgent. Here we reveal the enigmatic history of the genus Cochlearia (Brassicaceae), a Pleistocene relic that originated from a drought-adapted Mediterranean sister genus during the Miocene. Cochlearia rapidly diversified and adapted to circum-Arctic regions and other cold-characterized habitat types during the Pleistocene. This sudden change in ecological preferences was accompanied by a highly complex, reticulate polyploid evolution, which was apparently triggered by the impact of repeated Pleistocene glaciation cycles. Our results illustrate that two early diversified arctic-alpine diploid gene pools contributed differently to the evolution of this young polyploid genus now captured in a cold-adapted niche. Metabolomics revealed central carbon metabolism responses to cold in diverse species and ecotypes, likely due to continuous connections to cold habitats that may have facilitated widespread adaptation to alpine and subalpine habitats, and which we speculate were coopted from existing drought adaptations. Given the growing scientific interest in adaptive evolution of temperature-related traits, our results provide much-needed taxonomic and phylogenomic resolution of a model system as well as first insights into the origins of its adaptation to cold.

Methods
The data supplements contain:

a) Supplementary Data Set 1

SupplementaryDataSet1_CytogeneticDataSurvey.xlsx

This file contains 575 georeferenced chromosome counts and/or genome sizes across the Cochlearia genus.

b) Supplementary Data Set 2

SupplementaryDataSet2_AccessionDetailsNGSdata.xlsx

This file contains detailed information on 65 Cochlearia samples and 3 Ionopsidium samples included in NGS data generation and analysis.

c) Supplementary Data Set 3

SupplementaryDataSet3_MetabolicCompoundMatrix.xlsx

This file contains raw and normalized tables of 40 metabolic compounds consistently detected in all analyzed samples.

d) Supplementary Data Set 4

SupplementaryDataSet4_FlowCytometrySummaryTable.xlsx

This file contains detailed flow cytometry results.

d) Supplementary Data Set 5

SupplementaryDataSet5_PlastomeAlignment.txt

This file provides the plastome alignment as used for RAxML and BEAST analyses.

e) Supplementary Data Set 6

SupplementaryDataSet6_PlastomePartitionfileRaxmlBEAST.txt

This file contains data partitioning schemes for plastome RAxML and BEAST analyses.

f) Supplementary Data Set 7

SupplementaryDataSet7_MitochondrialContigs.zip

This folder contains annotated mitochondrial de novo consensus sequences of sample Cmica_0979 (in Genbank Flat File Format (*.gb)), as used as reference sequences in reference-based mappings and named as follows:

SupplementaryDataSet7a.gb
SupplementaryDataSet7b.gb
SupplementaryDataSet7c.gb
SupplementaryDataSet7d.gb
SupplementaryDataSet7e.gb
SupplementaryDataSet7f.gb
SupplementaryDataSet7g.gb
SupplementaryDataSet7h.gb

g) Supplementary Data Set 8

SupplementaryDataSet8_MitochondrialGenomeAlignment.txt

This file provides the alignment of mitochondrial genome sequences as inputted into RAxML analysis.

h) Supplementary Data Set 9

SupplementaryDataSet9_nrSNPalignmentRAxML.phy

This file provides the alignment of transcriptome-wide nuclear SNPs in phylip format as inputted into RAxML analysis.

i) Supplementary Data Set 10

SupplementaryDataSet10_nrSNPsSplitstreeTreemix.vcf.zip

This file provides hard-filtered biallelic transcriptome-wide nuclear SNPs in VCF format as used for SplitsTree and TreeMix analyses.

j) Supplementary Data Set 11

SupplementaryDataSet11_nrSNPsStructure.txt

This file provides the input for the STRUCTURE analysis of 62 Cochlearia samples.

k) Supplementary Data Set 12

SupplementaryDataSet12_nrSNPsStructureBavarica.txt

This file provides the input for the STRUCTURE analysis of Cochlearia bavarica.

l) Supplementary Data Set 13

SupplementaryDataSet13_nrSNPsABC.vcf.gz

This file provides the input for the ABC modelling in VCF format.