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Experimental evidence for rapid genomic adaptation to a new niche in an adaptive radiation

Nature Ecology & Evolutionvolume 2pages11281138 (2018) | Download Citation

Abstract

A substantial part of biodiversity is thought to have arisen from adaptive radiations in which one lineage rapidly diversified into multiple lineages specialized to many different niches. However, selection and drift reduce genetic variation during adaptation to new niches and may thus prevent or slow down further niche shifts. We tested whether rapid adaptation is still possible from a highly derived ecotype in the adaptive radiation of threespine stickleback on the Haida Gwaii archipelago, Western Canada. In a 19-year selection experiment, we let giant sticklebacks from a large blackwater lake evolve in a small clearwater pond without vertebrate predators. A total of 56 whole genomes from the experiment and 26 natural populations revealed that adaptive genomic change was rapid in many small genomic regions and encompassed 75% of the change between 12,000-year-old ecotypes. Genomic change was as fast as phenotypic change in defence and trophic morphology, and both were largely parallel between the short-term selection experiment and long-term natural adaptive radiation. Our results show that functionally relevant standing genetic variation can persist in derived radiation members, allowing adaptive radiations to unfold very rapidly.

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Acknowledgements

We thank B. Deagle, S. D. Leaver, C. B. Lowe, S. D. Brady, J. Turner, K. Lindblad-Toh and the Broad Institute Genomics Platform for help with sequences, samples and morphometric analysis, and B. Moa for bioinformatics support. This work was funded by the National Research Council Canada grant NRC2354 to T.E.R. and National Institute of Health grants 3P50HG002568-09S1 ARRA and 3P50HG002568 to D.M.K.

Author information

Affiliations

  1. Department of Biology, University of Victoria, Victoria, British Columbia, Canada

    • David A. Marques
    •  & Thomas E. Reimchen
  2. Aquatic Ecology & Evolution, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland

    • David A. Marques
  3. Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Kastanienbaum, Switzerland

    • David A. Marques
  4. Department of Developmental Biology, HHMI and Stanford University School of Medicine, Stanford, CA, USA

    • Felicity C. Jones
    •  & David M. Kingsley
  5. Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany

    • Felicity C. Jones
  6. Earlham Institute, Norwich Research Park, Norwich, UK

    • Federica Di Palma
  7. Department of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK

    • Federica Di Palma

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Contributions

T.E.R. conceived the study, ran the experiment, collected fish and ecological data in the field, and acquired morphological data. D.M.K., F.C.J. and F.D.P. generated sequencing data and genotype calls. D.A.M. designed and performed all subsequent analyses and wrote the manuscript with contributions from all co-authors.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to David A. Marques.

Supplementary information

  1. Supplementary Information

    Supplementary Results, Supplementary Figures and Supplementary Data

  2. Reporting Summary

  3. Supplementary Tables

    Supplementary Table 1: List of genomic outlier regions. Supplementary Table 2: List of QTL overlapping with outlier regions. Supplementary Table 3: List of candidate genes centred on selective sweep signatures in outlier regions. Supplementary Table 4: Genomic evolution in the 13 generation selection experiment and beyond.

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https://doi.org/10.1038/s41559-018-0581-8