Evolutionary footprints of a cold relic in a rapidly warming world

  1. Eva M Wolf  Is a corresponding author
  2. Emmanuel Gaquerel
  3. Mathias Scharmann
  4. Levi Yant
  5. Marcus A Koch  Is a corresponding author
  1. Heidelberg University, Germany
  2. University of Lausanne, Switzerland
  3. University of Nottingham, United Kingdom

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

Article and author information

Author details

  1. 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.
  2. Emmanuel Gaquerel

    Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0796-6417
  3. Mathias Scharmann

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8523-6888
  4. 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.
  5. 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.
    ORCID icon "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.

Reviewing Editor

  1. Daniel J Kliebenstein, University of California, Davis, United States

Publication history

  1. Received: June 23, 2021
  2. Preprint posted: July 12, 2021 (view preprint)
  3. Accepted: November 24, 2021
  4. Accepted Manuscript published: December 21, 2021 (version 1)
  5. Version of Record published: January 7, 2022 (version 2)

Copyright

© 2021, Wolf et al.

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.

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  1. Eva M Wolf
  2. Emmanuel Gaquerel
  3. Mathias Scharmann
  4. Levi Yant
  5. Marcus A Koch
(2021)
Evolutionary footprints of a cold relic in a rapidly warming world
eLife 10:e71572.
https://doi.org/10.7554/eLife.71572

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