Evolutionary footprints of a cold relic in a rapidly warming world

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Abstract

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.

Data availability

All data has been submitted and uploaded to:GeneBank: Genomic data - https://www.ncbi.nlm.nih.gov/bioproject/PRJEB21320, and plastomes under LT629868 - LT629930 and LN866844 - LN866848Cytogenetic data: FlowRepository under identifier FR-FCM-Z3FYDRYAD: Mitochondrial consensus sequences as well as metabolite profiling data and input files for NGS data analyses are available at Dryad [doi:10.5061/dryad.fbg79cnsn]

The following data sets were generated

1. Koch MA
2. et al
(2020) The evolutionary history of the genus Cochlearia
NCBI BioProject, PRJEB21320.

https://www.ncbi.nlm.nih.gov/bioproject/PRJEB21320
1. Koch MA
2. et al
(2021) Data from: Evolutionary footprints of a cold relic in a rapidly warming world
Dryad Digital Repository, doi:10.5061/dryad.fbg79cnsn.

http://dx.doi.org/10.5061/dryad.fbg79cnsn

Article and author information

Author details

Eva M Wolf

Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany

For correspondence
eva.wolf@cos.uni-heidelberg.de

Competing interests
The authors declare that no competing interests exist.
Emmanuel Gaquerel

Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-0796-6417
Mathias Scharmann

Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8523-6888
Levi Yant

Future Food Beacon and School of Life Sciences, University of Nottingham, Nottingham, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Marcus A Koch

Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany

For correspondence
marcus.koch@cos.uni-heidelberg.de

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-1693-6829

Funding

Deutsche Forschungsgemeinschaft (KO2302/13)

Marcus A Koch

Deutsche Forschungsgemeinschaft (KO2302/16)

Marcus A Koch

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.