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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  1. 1.

    Wood, T. E. et al. The frequency of polyploid speciation in vascular plants. Proc. Natl Acad. Sci. USA 106, 13875–13879 (2009).

  2. 2.

    Van de Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411 (2017).

  3. 3.

    Salman-Minkov, A., Sabath, N. & Mayrose, I. Whole-genome duplication as a key factor in crop domestication. Nat. Plants 2, 16115 (2016).

  4. 4.

    Storchova, Z. & Pellman, D. From polyploidy to aneuploidy, genome instability and cancer. Nat. Rev. Mol. Cell Biol. 5, 45–54 (2004).

  5. 5.

    Yant, L. & Bomblies, K. Genome management and mismanagement—cell-level opportunities and challenges of whole-genome duplication. Genes Dev. 29, 2405–2419 (2015).

  6. 6.

    Levin D. A. The Role of Chromosomal Change in Plant Evolution (Oxford Univ. Press, Oxford, 2002).

  7. 7.

    Parisod, C., Holderegger, R. & Brochmann, C. Evolutionary consequences of autopolyploidy. New Phytol. 186, 5–17 (2010).

  8. 8.

    te Beest, M. et al. The more the better? The role of polyploidy in facilitating plant invasions. Ann. Bot. 109, 19–45 (2011).

  9. 9.

    Segraves, K. A. The effects of genome duplications in a community context. New Phytol. 215, 57–69 (2017).

  10. 10.

    Haldane J. B. S. The Causes of Evolution (Princeton Univ. Press, Princeton, 1932).

  11. 11.

    Wright, S. The distribution of gene frequencies in populations of polyploids. Proc. Natl Acad. Sci. USA 24, 372–377 (1938).

  12. 12.

    Fisher, R. The theoretical consequences of polyploid inheritance for the mid style form of Lythrum salicaria. Ann. Hum. Genet. 11, 31–38 (1941).

  13. 13.

    Stebbins G. L. Chromosomal Evolution in Higher Plants (Edward Arnold, London, 1971).

  14. 14.

    Haldane, J. B. Theoretical genetics of autopolyploids. J. Genet. 22, 359–372 (1930).

  15. 15.

    Bever, J. D. & Felber, F. The theoretical population genetics of autopolyploidy. Oxford Surv. Evol. Biol. 8, 185 (1992).

  16. 16.

    Otto, S. P. & Whitton, J. Polyploid incidence and evolution. Annu. Rev. Genet. 34, 401–437 (2000).

  17. 17.

    Ronfort, J., Jenczewski, E., Bataillon, T. & Rousset, F. Analysis of population structure in autotetraploid species. Genetics 150, 921–930 (1998).

  18. 18.

    Grant, V. Plant Speciation 2nd edn (Columbia Univ. Press, New York, 1981).

  19. 19.

    Coyne, J. A. & Orr, H. A. Speciation (Sinauer, Sunderland, MA, 2004).

  20. 20.

    Mallet, J. Hybrid speciation. Nature 446, 279 (2007).

  21. 21.

    Slotte, T., Huang, H., Lascoux, M. & Ceplitis, A. Polyploid speciation did not confer instant reproductive isolation in Capsella (Brassicaceae). Mol. Biol. Evol. 25, 1472–1481 (2008).

  22. 22.

    Zohren, J. et al. Unidirectional diploid–tetraploid introgression among British birch trees with shifting ranges shown by restriction site‐associated markers. Mol. Ecol. 25, 2413–2426 (2016).

  23. 23.

    Lafon-Placette, C. et al. Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe. Proc. Natl Acad. Sci. USA 114, e1027–e1035 (2017).

  24. 24.

    Ronfort, J. The mutation load under tetrasomic inheritance and its consequences for the evolution of the selfing rate in autotetraploid species. Genet. Res. 74, 31–42 (1999).

  25. 25.

    Hill, R. Selection in autotetraploids. Theoret. Appl. Genet. 41, 181–186 (1971).

  26. 26.

    Selmecki, A. M. et al. Polyploidy can drive rapid adaptation in yeast. Nature 519, 349–352 (2015).

  27. 27.

    Schmickl, R., Marburger, S., Bray, S. & Yant, L. Hybrids and horizontal transfer: introgression allows adaptive allele discovery. J. Exp. Bot. 68, 5453–5470 (2017).

  28. 28.

    Arnold, M. L. & Kunte, K. Adaptive genetic exchange: a tangled history of admixture and evolutionary innovation. Trends Ecol. Evol. 32, 601–611 (2017).

  29. 29.

    Bomblies, K. & Madlung, A. Polyploidy in the Arabidopsis genus. Chromosome Res. 22, 117–134 (2014).

  30. 30.

    Yant, L. & Bomblies, K. Genomic studies of adaptive evolution in outcrossing Arabidopsis species. Curr. Opin. Plant. Biol. 36, 9–14 (2017).

  31. 31.

    Arnold, B., Kim, S.-T. & Bomblies, K. Single geographic origin of a widespread autotetraploid Arabidopsis arenosa lineage followed by interploidy admixture. Mol. Biol. Evol. 32, 1382–1395 (2015).

  32. 32.

    Hollister, J. D. et al. Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLoS Genet. 8, e1003093 (2012).

  33. 33.

    Kolář, F. et al. Ecological segregation does not drive the intricate parapatric distribution of diploid and tetraploid cytotypes of the Arabidopsis arenosa group (Brassicaceae). Biol. J. Linnean Soc. 119, 673–688 (2016).

  34. 34.

    Kolář, F. et al. Northern glacial refugia and altitudinal niche divergence shape genome‐wide differentiation in the emerging plant model Arabidopsis arenosa. Mol. Ecol. 25, 3929–3949 (2016).

  35. 35.

    1001 Genomes Consortium. 1,135 genomes reveal the global pattern of polymorphism in Arabidopsis thaliana. Cell 166, 481–491 (2016).

  36. 36.

    Ingvarsson, P. K. Gene expression and protein length influence codon usage and rates of sequence evolution in Populus tremula. Mol. Biol. Evol. 24, 836–844 (2007).

  37. 37.

    Wright, S. I., Yau, C. K., Looseley, M. & Meyers, B. C. Effects of gene expression on molecular evolution in Arabidopsis thaliana and Arabidopsis lyrata. Mol. Biol. Evol. 21, 1719–1726 (2004).

  38. 38.

    Popescu, C. E., Borza, T., Bielawski, J. P. & Lee, R. W. Evolutionary rates and expression level in Chlamydomonas. Genetics 172, 1567–1576 (2006).

  39. 39.

    Keightley, P. D. & Eyre-Walker, A. Joint inference of the distribution of fitness effects of deleterious mutations and population demography based on nucleotide polymorphism frequencies. Genetics 177, 2251–2261 (2007).

  40. 40.

    Eyre-Walker, A. & Keightley, P. D. Estimating the rate of adaptive molecular evolution in the presence of slightly deleterious mutations and population size change. Mol. Biol. Evol. 26, 2097–2108 (2009).

  41. 41.

    Rousselle, M., Mollion, M., Nabholz, B., Bataillon, T. & Galtier, N. Overestimation of the adaptive substitution rate in fluctuating populations. Biol. Lett. 14, 5 (2018).

  42. 42.

    Venkat, A., Hahn, M. W. & Thornton, J. W. Multinucleotide mutations cause false inferences of lineage-specific positive selection. Nat. Ecol. Evol. 2, 1280–1288 (2018).

  43. 43.

    Yant, L. et al. Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr. Biol. 23, 2151–2156 (2013).

  44. 44.

    Baduel, P., Arnold, B., Weisman, C. M., Hunter, B. & Bomblies, K. Habitat-associated life history and stress-tolerance variation in Arabidopsis arenosa. Plant Physiol. 171, 437–451 (2016).

  45. 45.

    Schmickl, R. & Koch, M. A. Arabidopsis hybrid speciation processes. Proc. Natl Acad. Sci. USA 108, 14192–14197 (2011).

  46. 46.

    Gerstein, A. C. & Otto, S. P. Ploidy and the causes of genomic evolution. J. Hered. 100, 571–581 (2009).

  47. 47.

    Favarger, C. in Plant Biosystematics (ed. Grant, W. F.) 453–476 (Elsevier, 1984).

  48. 48.

    Brochmann, C. et al. Polyploidy in arctic plants. Biol. J. Linnean Soc. 82, 521–536 (2004).

  49. 49.

    Butruille, D. V. & Boiteux, L. S. Selection–mutation balance in polysomic tetraploids: impact of double reduction and gametophytic selection on the frequency and subchromosomal localization of deleterious mutations. Proc. Natl Acad. Sci. USA 97, 6608–6613 (2000).

  50. 50.

    Willis, J. H. Inbreeding load, average dominance and the mutation rate for mildly deleterious alleles in Mimulus guttatus. Genetics 153, 1885 (1999).

  51. 51.

    Schmickl, R., Marburger, S., Bray, S. & Yant, L. Hybrids and horizontal transfer: introgression allows adaptive allele discovery. J. Exp. Bot. 68, 5453–5470 (2017).

  52. 52.

    Lowe, W. H., Muhlfeld, C. C. & Allendorf, F. W. Spatial sorting promotes the spread of maladaptive hybridization. Trends Ecol. Evol. 30, 456–462 (2015).

  53. 53.

    Yukilevich, R. Asymmetrical patterns of speciation uniquely support reinforcement in Drosophila. Evolution 66, 1430–1446 (2012).

  54. 54.

    Hylander, N. Cardaminopsis suecica (Fr.) Hiit., a northern amphidiploid species. Bulletin du Jardin botanique de l’Etat 27, 591–604 (1957).

  55. 55.

    Baduel, P., Hunter, B., Yeola, S. & Bomblies, K. Genetic basis and evolution of rapid cycling in railway populations of tetraploid Arabidopsis arenosa. PLoS Genet. 14, e1007510 (2018).

  56. 56.

    Husband, B. C. & Sabara, H. A. Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium (Onagraceae). New Phytol. 161, 703–713 (2004).

  57. 57.

    Kolář, F., Čertner, M., Suda, J., Schönswetter, P. & Husband, B. C. Mixed-ploidy species: progress and opportunities in polyploid research. Trends Plant Sci. 22, 1041–1055 (2017).

  58. 58.

    Soltis, D. E. & Soltis, P. S. Polyploidy: recurrent formation and genome evolution. Trends Ecol. Evol. 14, 348–352 (1999).

  59. 59.

    Arnold, B. J. et al. Borrowed alleles and convergence in serpentine adaptation. Proc. Natl Acad. Sci. USA 113, 8320–8325 (2016).

  60. 60.

    Doyle, J. J. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull. 19, 11–15 (1987).

  61. 61.

    Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12 (2011).

  62. 62.

    Hu, T. T. et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 43, 476–481 (2011).

  63. 63.

    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

  64. 64.

    DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491–498 (2011).

  65. 65.

    McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

  66. 66.

    Wright, S. I., Lauga, B. & Charlesworth, D. Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol. Biol. Evol. 19, 1407–1420 (2002).

  67. 67.

    Jombart, T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).

  68. 68.

    Nei, M. Genetic distance between populations. Am. Nat. 106, 283–292 (1972).

  69. 69.

    Pembleton, L. W., Cogan, N. O. & Forster, J. W. StAMPP: an R package for calculation of genetic differentiation and structure of mixed‐ploidy level populations. Mol. Ecol. Res. 13, 946–952 (2013).

  70. 70.

    Huson, D. H. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14, 68–73 (1998).

  71. 71.

    Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

  72. 72.

    Excoffier, L., Dupanloup, I., Huerta-Sánchez, E., Sousa, V. C. & Foll, M. Robust demographic inference from genomic and SNP data. PLoS Genet. 9, e1003905 (2013).

  73. 73.

    Raj, A., Stephens, M. & Pritchard, J. K. fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 197, 573–589 (2014).

  74. 74.

    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

  75. 75.

    Nordborg, M. et al. The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3, e196 (2005).

  76. 76.

    Novikova, P. Y. et al. Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism. Nat. Genet. 48, 1077–1082 (2016).

  77. 77.

    Paradis, E. pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26, 419–420 (2010).

  78. 78.

    Dray, S. & Dufour, A.-B. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22, 1–20 (2007).

  79. 79.

    Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493 (2011).

  80. 80.

    Nadachowska‐Brzyska, K., Burri, R., Smeds, L. & Ellegren, H. PSMC analysis of effective population sizes in molecular ecology and its application to black‐and‐white Ficedula flycatchers. Mol. Ecol. 25, 1058–1072 (2016).

  81. 81.

    Zeng, K., Fu, Y.-X., Shi, S. & Wu, C.-I. Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174, 1431–1439 (1996).

  82. 82.

    Weir, B. S. & Cockerham, C. C. Estimating F‐statistics for the analysis of population structure. Evolution 38, 1358–1370 (1984).

  83. 83.

    Cruickshank, T. E. & Hahn, M. W. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol. Ecol. 23, 3133–3157 (2014).

  84. 84.

    Hardy, O. J. & Vekemans, X. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. Res. 2, 618–620 (2002).

  85. 85.

    Martin, S. H. & Van Belleghem, S. M. Exploring evolutionary relationships across the genome using topology weighting.Genetics 206, 429–438 (2017).

  86. 86.

    Duret, L. & Mouchiroud, D. Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate. Mol. Biol. Evol. 17, 68–070 (2000).

  87. 87.

    Rocha, E. P. & Danchin, A. An analysis of determinants of amino acids substitution rates in bacterial proteins. Mol. Biol. Evol. 21, 108–116 (2004).

  88. 88.

    Slotte, T. et al. Genomic determinants of protein evolution and polymorphism in Arabidopsis. Genome Biol. Evol. 3, 1210–1219 (2011).

  89. 89.

    Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome. Biol. 14, R36 (2013).

  90. 90.

    Lunter, G. & Goodson, M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21, 936–939 (2011).

  91. 91.

    Anders, S., Pyl, P. T. & Huber, W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015).

  92. 92.

    Love, M., Anders, S. & Huber, W. Differential analysis of count data–the DESeq2 package. Genome. Biol. 15, 550 (2014).

  93. 93.

    Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).

  94. 94.

    Gossmann, T. I. et al. Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Mol. Biol. Evol. 27, 1822–1832 (2010).

  95. 95.

    Martin, S. H. et al. Natural selection and genetic diversity in the butterfly Heliconius melpomene. Genetics 203, 525–541 (2016).

  96. 96.

    Bates, D., Martin, M., Ben, B. & Walker S. lme4: linear mixed effects models using Eigen and S4 (R package v.1.0–6, 2014); http://CRAN.R-project.org/package=lme4

  97. 97.

    Kelleher, J., Etheridge, A. M. & McVean, G. Efficient coalescent simulation and genealogical analysis for large sample sizes. PLoS Comput. Biol. 12, e1004842 (2016).

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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.


  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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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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