Article

Young inversion with multiple linked QTLs under selection in a hybrid zone

  • Nature Ecology & Evolution 1, Article number: 0119 (2017)
  • doi:10.1038/s41559-017-0119
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Abstract

Fixed chromosomal inversions can reduce gene flow and promote speciation in two ways: by suppressing recombination and by carrying locally favoured alleles at multiple loci. However, it is unknown whether favoured mutations slowly accumulate on older inversions or if young inversions spread because they capture pre-existing adaptive quantitative trait loci (QTLs). By genetic mapping, chromosome painting and genome sequencing, we have identified a major inversion controlling ecologically important traits in Boechera stricta. The inversion arose since the last glaciation and subsequently reached local high frequency in a hybrid speciation zone. Furthermore, the inversion shows signs of positive directional selection. To test whether the inversion could have captured existing, linked QTLs, we crossed standard, collinear haplotypes from the hybrid zone and found multiple linked phenology QTLs within the inversion region. These findings provide the first direct evidence that linked, locally adapted QTLs may be captured by young inversions during incipient speciation.

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Change history

  • Corrected online 25 August 2017

    In Fig. 5 of the version of this Article originally published, the final number on the x axes of each panel was incorrectly written as 1.5; it should have read 7.5. This has now been corrected in all versions of the Article.

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Acknowledgements

C.-R.L. was supported by the National Science Foundation (US) Doctoral Dissertation Improvement Grant 1110445, a European Molecular Biology Organization Long-Term Fellowship, and 105-2311-B-002-040-MY2 from the Ministry of Science and Technology, Taiwan. B.W. was supported by the Swedish Research Council (VR). R.W. was supported by the Bud Antle Endowed Chair of Excellence in Agriculture and Life Sciences, and the AXA Chair in Genome Biology and Evolutionary Genomics. M.A.L. and T.M. were supported by grant P501/10/1014 from the Czech Science Foundation. MES acknowledges support from TKI “Better Plants for New Demands” subsidy (grant number EZ-2012-01). T.M.-O. was supported by grant R01 GM086496 from the National Institutes of Health (USA), and by the Rocky Mountain Biological Laboratory. Work conducted by the US Department of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. We thank J. Phillips for providing genome annotations. We thank L. Carley, K. Donohue, D. Hartl, M. Noor, S. Otto, M. Rausher, M. Wagner and J. Willis for helpful discussion and comments.

Author information

Author notes

    • Cheng-Ruei Lee
    •  & Baosheng Wang

    These authors contributed equally to this work.

Affiliations

  1. Department of Biology, Duke University, Box 90338, Durham, North Carolina 27708, USA

    • Cheng-Ruei Lee
    • , Baosheng Wang
    • , Julius P. Mojica
    • , Nadeesha Perera
    • , Kathryn Ghattas
    •  & Thomas Mitchell-Olds
  2. Institute of Ecology and Evolutionary Biology and Institute of Plant Biology, National Taiwan University, Taipei 10617, Taiwan ROC

    • Cheng-Ruei Lee
  3. Department of Plant Ecology and Genetics, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden

    • Baosheng Wang
  4. Plant Cytogenomics Group, Central European Institute of Technology, Masaryk University, Kamenice 5, Brno CZ-62500, Czech Republic

    • Terezie Mandáková
  5. Department of Biology, Colorado State University, Fort Collins, Colorado 80523, USA

    • Kasavajhala V. S. K. Prasad
  6. Arizona Genomics Institute and BIO5 Institute, School of Plant Sciences, University of Arizona, Tucson, Arizona 85721, USA

    • Jose Luis Goicoechea
    •  & Martin A. Lysak
  7. Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA

    • Uffe Hellsten
    • , Hope N. Hundley
    • , Jenifer Johnson
    • , Kerrie Barry
    • , Stephen Fairclough
    • , Jerry W. Jenkins
    • , Jeremy Schmutz
    •  & Daniel S. Rokhsar
  8. HudsonAlpha Institute for Biotechnology, Huntsville, Alabama 35806, USA

    • Jane Grimwood
    •  & Rod Wing
  9. Phyzen Genomics Institute, Phyzen Inc., Seoul 151–836, South Korea

    • Yeisoo Yu
  10. Arizona Genomics Institute and BIO5 Institute, School of Plant Sciences, University of Arizona, Tucson, Arizona 85721, USA

    • Dave Kudrna
    • , Jianwei Zhang
    • , Jayson Talag
    •  & Wolfgang Golser
  11. Biosystematics Group, Wageningen University and Research Center, Droevendaalsesteeg 1, 6708PB Wageningen, The Netherlands

    • M. Eric Schranz

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Contributions

C.-R.L. and T.M.-O. conceived this work. C.-R.L., T.M.-O., Y.Y., D.K., J.Z. and J.L.G. designed the study. T.M. and M.A.L. performed the chromosome painting. C.-R.L., K.V.S.K.P, N.P., H.N.H., D.K., Y.Y., J.T., W.G., J.Z., J.G. and J.J. worked on the molecular biology and sequencing. S.F., U.H., J.W.J., J.S., D.S.R., R.W. and K.B.; and J.L.G, D.K., Y.Y., J.Z., J.T., W.G. and R.W. planned and analysed the genomic and physical mapping experiments, respectively. C.-R.L., B.W., J.P.M., U.H., J.L.G. and T.M.-O. performed bioinformatic and evolutionary analyses. K.G., C.-R.L. and N.P. performed the experiments with plants. C.-R.L., B.W., J.P.M., M.E.S. and T.M.-O. drafted the manuscript. All authors read, revised and approved the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Cheng-Ruei Lee or Thomas Mitchell-Olds.

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    Supplementary Information

    Supplementary Figures 1–9; Supplementary Tables 1–8