Abstract

It is well recognized that environmental degradation caused by human activities can result in dramatic losses of species and diversity. However, comparatively little is known about the ability of biodiversity to re-emerge following ecosystem recovery. Here, we show that a European whitefish subspecies, the gangfisch Coregonus lavaretus macrophthalmus, rapidly increased its ecologically functional diversity following the restoration of Lake Constance after anthropogenic eutrophication. In fewer than ten generations, gangfisch evolved a greater range of gill raker numbers (GRNs) to utilize a broader ecological niche. A sparse genetic architecture underlies this variation in GRN. Several co-expressed gene modules and genes showing signals of positive selection were associated with GRN and body shape. These were enriched for biological pathways related to trophic niche expansion in fishes. Our findings demonstrate the potential of functional diversity to expand following habitat restoration, given a fortuitous combination of genetic architecture, genetic diversity and selection.

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Data availability

The sequence datasets have been deposited in the National Center for Biotechnology Information Sequence Read Archive with the BioProject accession code PRJNA497182 (corresponding to BioSample accessions SAMN10250325 to SAMN10250521). Phenotype and ecological data are available at the ‘Enlighten: Research Data’ repository of the University of Glasgow: https://doi.org/10.5525/gla.researchdata.680.

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Acknowledgements

We thank H. Thiele, M. Schmid, W. Kornberger and A. Sulger for assistance with specimen and data collection, D. Straile for providing background data, and P. Hirsch, H. Recknagel and A. Yurchencko for comments and advice. This work was funded by a Marie Curie Action Career Integration Grant (321999) to K.R.E., a BBSRC WestBio Doctoral Training Partnership studentship to M.C., C.E.A. and K.R.E. (BB/J013854/1), ERASMUS+ (to J.B.-G. and K.R.E.), a Fisheries Society of the British Isles Research Grant (to K.R.E. and A.J.), and AFF funding from the University of Konstanz to E.Y. and J.B.-G.

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Author notes

  1. These authors contributed equally: Arne Jacobs, Madeleine Carruthers.

Affiliations

  1. Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK

    • Arne Jacobs
    • , Madeleine Carruthers
    • , Colin E. Adams
    •  & Kathryn R. Elmer
  2. Limnological Institute, University of Konstanz, Konstanz, Germany

    • Reiner Eckmann
    • , Elizabeth Yohannes
    •  & Jasminca Behrmann-Godel
  3. Scottish Centre for Ecology and the Natural Environment, University of Glasgow, Glasgow, UK

    • Colin E. Adams

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Contributions

J.B.-G. and K.R.E. designed the experiment. A.J., M.C., K.R.E. and J.B.-G. collected the data. M.C. generated and analysed the eco-morphological and transcriptomic data. A.J. generated and analysed the genomic data, and analysed the eco-morphological and stable isotope data. R.E. analysed the life history data. E.Y. generated the stable isotope data. C.E.A., J.B.-G. and K.R.E. supervised the project. A.J. wrote the paper, along with M.C., J.B.-G. and K.R.E. All authors commented on and approved the final manuscript.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Jasminca Behrmann-Godel or Kathryn R. Elmer.

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https://doi.org/10.1038/s41559-018-0742-9