Abstract

Ploidy-variable species allow direct inference of the effects of chromosome copy number on fundamental evolutionary processes. While an abundance of theoretical work suggests polyploidy should leave distinct population genomic signatures, empirical data remains sparse. We sequenced ~300 individuals from 39 populations of Arabidopsis arenosa, a naturally diploid-autotetraploid species. We find that the impacts of polyploidy on population genomic processes are subtle yet pervasive, such as reduced efficiency of purifying selection, differences in linked selection and rampant gene flow from diploids. Initial masking of deleterious mutations, faster rates of nucleotide substitution and interploidy introgression likely conspire to shape the evolutionary potential of polyploids.

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Code availability

Custom scripts used to generate genome scan metrics are available at https://github.com/pmonnahan/ScanTools. Other analysis scripts are available at https://github.com/pmonnahan/ArenosaPloidy.

Data availability

Sequence data that support the findings of this study have been deposited in the Sequence Read Archive (SRA; https://www.ncbi.nlm.nih.gov/sra) with the primary accession code PRJNA484107 (available at http://www.ncbi.nlm.nih.gov/bioproject/484107) and PRJNA472485 for RNAseq data.

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Acknowledgements

The authors thank E. Záveská, M. Lučanová and S. Španiel for help with fieldwork and J. Brookfield and S. Martin for helpful comments on versions of the manuscript. Computational resources were provided by the CESNET LM2015042 and the CERIT Scientific Cloud LM2015085, provided under the programme Projects of Large Research, Development, and Innovations Infrastructures, and by SNIC through Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) under Project SNIC 2017/7–174. L.Y. acknowledges funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement 679056) and the UK Biological and Biotechnology Research Council (BBSRC) via grant BB/P013511/1 to the John Innes Centre. K.B. acknowledges European Research Council Consolidator grant CoG EVO-MEIO 681946 and US National Science Foundation IOS-1146465. Additional support was provided by Czech Science Foundation (project 16–10809S to K.M. and 17–20357Y to F.K.), Charles University (project Primus/SCI/35 to F.K.), and a SNSF Early Postdoc Mobility fellowship (P2ZHP3_158773 to C.S.).

Author information

Author notes

  1. These authors contributed equally: Patrick Monnahan, Filip Kolář and Pierre Baduel.

Affiliations

  1. Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich, UK

    • Patrick Monnahan
    • , Pierre Baduel
    • , Christian Sailer
    • , Jordan Koch
    • , Pirita Paajanen
    • , Kirsten Bomblies
    •  & Levi Yant
  2. Department of Botany, Faculty of Science, Charles University, Prague, Czech Republic

    • Filip Kolář
    • , Roswitha Schmickl
    • , Gabriela Šrámková
    • , Magdalena Bohutínská
    •  & Karol Marhold
  3. Department of Botany, University of Innsbruck, Innsbruck, Austria

    • Filip Kolář
  4. Institute of Botany, The Czech Academy of Sciences, Průhonice, Czech Republic

    • Filip Kolář
    • , Roswitha Schmickl
    •  & Magdalena Bohutínská
  5. Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden

    • Robert Horvath
    • , Benjamin Laenen
    •  & Tanja Slotte
  6. Center for Communicable Disease Dynamics, Department of Epidemiology, Harvard T. H. Chan School of Public Health, Boston, MA, USA

    • Brian Arnold
  7. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA

    • Caroline M. Weisman
  8. Plant Science and Biodiversity Centre, Slovak Academy of Sciences, Bratislava, Slovak Republic

    • Karol Marhold
  9. School of Life Sciences and Future Food Beacon, University of Nottingham, Nottingham, UK

    • Levi Yant

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Contributions

L.Y., K.B., F.K., P.B. and P.M. conceived the study. P.M., F.K., P.B., B.L., C.S., J.K., R.H., R.S. and P.P. performed analyses with input from L.Y., K.B., R.H. and T.S. C.S., P.B., G.F., M.B. and C.M.W. performed laboratory experiments. P.M., F.K. and P.B. wrote the manuscript with primary input from K.B., L.Y., B.A., C.S. and T.S. All authors edited and approved of the final manuscript.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Levi Yant.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–24, Supplementary Tables 1–14 and Supplementary Note

  2. Reporting Summary

  3. Supplementary Data 1

    Measures of genome-wide diversity within the 36 populations of A. arenosa with ≥5 individuals sequenced and details on inclusion of the populations in the downstream analyses.

  4. Supplementary Data 2

    Steps used for processing, mapping, and variant calling.

  5. Supplementary Data 3

    Sequence processing quality assessment of each sequenced individual.

  6. Supplementary Data 4

    Unfolded allele frequency spectra of the 36 A. arenosa populations with ≥5 individuals.

  7. Supplementary Data 5

    Fasta of 291 plastome sequences.

  8. Supplementary Data 6

    Maximum likelihood phylogeny of Arabidopsis plastomes from our study and of Novikova et al. (2016).

  9. Supplementary Data 7

    Example parameter files used in fastsimcoal2.

  10. Supplementary Data 8

    Data used to generate File_S4_AFS.pdf.

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https://doi.org/10.1038/s41559-019-0807-4