BACKGROUND AND AIMS: Polyploidy is an important driver of plant diversification and adaptation to novel environments. As a consequence of genome doubling, polyploids often exhibit greater colonizing ability or occupy a wider ecological niche than diploids. Although elevation has been traditionally considered as a key driver structuring ploidy variation, we do not know if environmental and phenotypic differentiation among ploidy cytotypes varies along an elevational gradient. Here, we tested for the consequences of genome duplication on genetic diversity, phenotypic variation and habitat preferences on closely related diploid and tetraploid populations that coexist along approx. 2300 m of varying elevation. METHODS: We sampled and phenotyped 45 natural diploid and tetraploid populations of Arabidopsis arenosa in one mountain range in Central Europe (Western Carpathians) and recorded abiotic and biotic variables at each collection site. We inferred genetic variation, population structure and demographic history in a sub-set of 29 populations genotyped for approx. 36 000 single nucleotide polymorphisms. KEY RESULTS: We found minor effects of polyploidy on colonization of alpine stands and low genetic differentiation between the two cytotypes, mirroring recent divergence of the polyploids from the local diploid lineage and repeated reticulation events among the cytotypes. This pattern was corroborated by the absence of ecological niche differentiation between the two cytotypes and overall phenotypic similarity at a given elevation. CONCLUSIONS: The case of A. arenosa contrasts with previous studies that frequently showed clear niche differentiation between cytotypes. Our work stresses the importance of considering genetic structure and past demographic processes when interpreting the patterns of ploidy distributions, especially in species that underwent recent polyploidization events.

Department of Botany Charles University Prague Czech Republic

Institute of Botany Plant Science and Biodiversity Centre Slovak Academy of Sciences Bratislava Slovak Republic

Institute of Botany The Czech Academy of Sciences Průhonice Czech Republic

Institute of Botany University of Innsbruck Innsbruck Austria

Zobrazit více v PubMed

Adams KL, Wendel JF. 2005. Polyploidy and genome evolution in plants. Current Opinion in Plant Biology 8: 135–141. PubMed

Arnold B, Kim S-T, Bomblies K. 2015. Single geographic origin of a widespread autotetraploid Arabidopsis arenosa lineage followed by interploidy admixture. Molecular Biology and Evolution 32: 1382–1395. PubMed

Baack EJ, Stanton ML. 2005. Ecological factors influencing tetraploid speciation in snow buttercups (Ranunculus adoneus): niche differentiation and tetraploid establishment. Evolution 59: 1936–1944. PubMed

Baduel P, Arnold B, Weisman CM, Hunter B, Bomblies K. 2016. Habitat-associated life history and stress-tolerance variation in Arabidopsis arenosa. Plant Physiology 171: 437–451. PubMed PMC

Balao F, Herrera J, Talavera S. 2011. Phenotypic consequences of polyploidy and genome size at the microevolutionary scale: a multivariate morphological approach. New Phytologist 192: 256–265. PubMed

Barringer BC. 2007. Polyploidy and self-fertilization in flowering plants. American Journal of Botany 94: 1527–1533. PubMed

te Beest M, Le Roux JJ, Richardson DM, et al. . 2012. The more the better? The role of polyploidy in facilitating plant invasions. Annals of Botany 109: 19–45. PubMed PMC

Brochmann C, Brysting AK, Alsos IG, et al. . 2004. Polyploidy in arctic plants. Biological Journal of the Linnean Society 82: 521–536.

Čertner M, Fenclová E, Kúr P, et al. . 2017. Evolutionary dynamics of mixed-ploidy populations in an annual herb: dispersal, local persistence and recurrent origins of polyploids. Annals of Botany 120: 303–315. PubMed PMC

Chen ZJ. 2007. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annual Review of Plant Biology 58: 377–406. PubMed PMC

Comai L. 2005. The advantages and disadvantages of being polyploid. Nature Reviews. Genetics 6: 836–846. PubMed

Corneillie S, Storme ND, Acker RV, et al. . 2019. Polyploidy affects plant growth and alters cell wall composition. Plant Physiology 179: 74–87. PubMed PMC

Ehrendorfer F. 1980. Polyploidy and distribution. In: Lewis WH, ed. Polyploidy. New York: Plenum Press, 45–60.

Ellenberg H, Weber H, Düll R, Wirth V, Werner W, Paulissen D. 1991. Zeigwerte von Pflanzen in MittelEuropa. Scripta Geobotanica 18: 248.

Excoffier L, Dupanloup I, Huerta-Sánchez E, Sousa VC, Foll M. 2013. Robust demographic inference from genomic and SNP data. PLoS Genetics 9: e1003905. doi: 10.1371/journal.pgen.1003905. PubMed DOI PMC

Exposito-Alonso M, Becker C, Schuenemann VJ, et al. . 2018. The rate and potential relevance of new mutations in a colonizing plant lineage. PLoS Genetics 14: e1007155. doi: 10.1371/journal.pgen.1007155. PubMed DOI PMC

Futák J. 1980. Phytogeographical division of Slovakia (1:1 000 000). In: Mazúr E, ed. Atlas Slovenskej socialistickej republiky. Bratislava: Slovenské pedagogické nakladateľstvo.

Gauthier P, Lumaret R, Bédécarrats A. 1998. Genetic variation and gene flow in Alpine diploid and tetraploid populations of Lotus (L. alpinus (D.C.) Schleicher/L. corniculatus L.). I. Insights from morphological and allozyme markers. Heredity 80: 683–693.

Glennon KL, Ritchie ME, Segraves KA. 2014. Evidence for shared broad-scale climatic niches of diploid and polyploid plants. Ecology Letters 17: 574–582. PubMed

Hair J, Anderson R, Tatham R, Black W. 2006. Multivariate data analysis, 6th edn. Pearson: New Jersey.

Hanelt P. 1966. Polyploidie – frequenz und geographische verbreitung bei höheren pflanzen. Biologische Rundschau 4: 183–196.

Hanzl M, Kolář F, Nováková D, Suda J. 2014. Nonadaptive processes governing early stages of polyploid evolution: insights from a primary contact zone of relict serpentine Knautia arvensis (Caprifoliaceae). American Journal of Botany 101: 935–945. PubMed

Hegarty MJ, Hiscock SJ. 2008. Genomic clues to the evolutionary success of polyploid plants. Current Biology 18: R435–R444. PubMed

Hu TT, Pattyn P, Bakker EG, et al. . 2011. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nature Genetics 43: 476–481. PubMed PMC

Hülber K, Sonnleitner M, Flatscher R, et al. . 2009. Ecological segregation drives fine-scale cytotype distribution of Senecio carniolicus in the Eastern Alps. Preslia 81: 309–319. PubMed PMC

Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23: 254–267. PubMed

Jamrichová E, Petr L, Jiménez‐Alfaro B, et al. . 2017. Pollen-inferred millennial changes in landscape patterns at a major biogeographical interface within Europe. Journal of Biogeography 44: 2386–2397.

Jankovska V, Pokorný P. 2008. Forest vegetation of the last full-glacial period in the Western Carpathians (Slovakia and Czech Republic). Preslia 80: 307–324.

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

Kirchheimer B, Schinkel CCF, Dellinger AS, et al. . 2016. A matter of scale: apparent niche differentiation of diploid and tetraploid plants may depend on extent and grain of analysis. Journal of Biogeography 43: 716–726. PubMed PMC

Knotek A, Kolář F. 2018. Different low-competition island habitats in Central Europe harbour similar levels of genetic diversity in relict populations of Galium pusillum agg. (Rubiaceae). Biological Journal of the Linnean Society 125: 491–507.

Kolář F, Fuxová G, Záveská E, et al. . 2016. a Northern glacial refugia and altitudinal niche divergence shape genome-wide differentiation in the emerging plant model Arabidopsis arenosa. Molecular Ecology 25: 3929–3949. PubMed

Kolář F, Lučanová M, Záveská E, et al. . 2016. b Ecological segregation does not drive the intricate parapatric distribution of diploid and tetraploid cytotypes of the Arabidopsis arenosa group (Brassicaceae). Biological Journal of the Linnean Society 119: 673–688.

Kolář F, Čertner M, Suda J, Schönswetter P, Husband BC. 2017. Mixed-ploidy species: progress and opportunities in polyploid research. Trends in Plant Science 22: 1041–1055. PubMed

Koutecký P. 2015. MorphoTools: a set of R functions for morphometric analysis. Plant Systematics and Evolution 301: 1115–1121.

Levin DA. 1983. Polyploidy and novelty in flowering plants. The American Naturalist 122: 1–25.

Levin DA. 2002. The role of chromosomal change in plant evolution. Oxford: Oxford University Press.

Lindner L, Dzierżek J, Marciniak B, Nitychoruk J. 2010. Outline of Quaternary glaciations in the Tatra Mts.: their development, age and limits. Geological Quarterly 47: 269–280.

Löve A, Löve D. 1967. Polyploidy and altitude: Mt. Washington. Biologisches Zentralblatt Suppl: 307–312.

Lowry E, Lester SE. 2006. The biogeography of plant reproduction: potential determinants of species’ range sizes. Journal of Biogeography 33: 1975–1982.

Madlung A. 2013. Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110: 99–104. PubMed PMC

Manzaneda AJ, Rey PJ, Bastida JM, Weiss‐Lehman C, Raskin E, Mitchell‐Olds T. 2012. Environmental aridity is associated with cytotype segregation and polyploidy occurrence in Brachypodium distachyon (Poaceae). New Phytologist 193: 797–805. PubMed PMC

Martin SL, Husband BC. 2013. Adaptation of diploid and tetraploid Chamerion angustifolium to elevation but not local environment. Evolution 67: 1780–1791. PubMed

McKenna A, Hanna M, Banks E, et al. . 2010. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research 20: 1297–1303. PubMed PMC

Meirmans PG, Van Tienderen PH. 2013. The effects of inheritance in tetraploids on genetic diversity and population divergence. Heredity 110: 131–137. PubMed PMC

Měsíček J, Goliašová K. 2002. Cardaminopsis (CA Mey.) Hayek. In: Goliašová K, Šípošová H, eds. Flóra Slovenska. Bratislava: Veda, 388–415.

Molina‐Henao YF, Hopkins R. 2019. Autopolyploid lineage shows climatic niche expansion but not divergence in Arabidopsis arenosa. American Journal of Botany 106: 61–70. PubMed

Monnahan P, Kolář F, Baduel P, et al. . 2019. Pervasive population genomic consequences of genome duplication in Arabidopsis arenosa. Nature Ecology & Evolution 3: 457–468. PubMed

Nei M. 1972. Genetic distance between populations. The American Naturalist 106: 283–292.

Oksanen J, Blanchet FG, Kindt R, et al. . 2013. Vegan: community ecology package. R Package Version. 2.0–10. CRAN.

Otisková V, Koutecký T, Kolář F, Koutecký P. 2014. Occurrence and habitat preferences of diploid and tetraploid cytotypes of Centaurea stoebe in the Czech Republic. Preslia 86: 67–80.

Otto SP. 2007. The evolutionary consequences of polyploidy. Cell 131: 452–462. PubMed

Otto SP, Whitton J. 2000. Polyploid incidence and evolution. Annual Review of Genetics 34: 401–437. PubMed

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

Parisod C, Besnard G. 2007. Glacial in situ survival in the Western Alps and polytopic autopolyploidy in Biscutella laevigata L. (Brassicaceae). Molecular Ecology 16: 2755–2767. PubMed

Parisod C, Holderegger R, Brochmann C. 2010. Evolutionary consequences of autopolyploidy. New Phytologist 186: 5–17. PubMed

Pembleton LW, Cogan NOI, Forster JW. 2013. StAMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Molecular Ecology Resources 13: 946–952. PubMed

Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE. 2012. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7: e37135. doi: 10.1371/journal.pone.0037135. PubMed DOI PMC

Petit C, Bretagnolle F, Felber F. 1999. Evolutionary consequences of diploid–polyploid hybrid zones in wild species. Trends in Ecology & Evolution 14: 306–311. PubMed

Pickrell JK, Pritchard JK. 2012. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genetics 8: e1002967. doi: 10.1371/journal.pgen.1002967. PubMed DOI PMC

Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC. 2012. nlme: linear and nonlinear mixed effects models. R package version 3.

del Pozo JC, Ramirez-Parra E. 2015. Whole genome duplications in plants: an overview from Arabidopsis. Journal of Experimental Botany 66: 6991–7003. PubMed

Raabová J, Fischer M, Münzbergová Z. 2008. Niche differentiation between diploid and hexaploid Aster amellus. Oecologia 158: 463–472. PubMed

Regele D, Grünebach M, Erschbamer B, Schönswetter P. 2017. Do ploidy level, morphology, habitat and genetic relationships in Alpine Vaccinium uliginosum allow for the discrimination of two entities? Preslia 89: 291–308.

Rice A, Šmarda P, Novosolov M, et al. . 2019The global biogeography of polyploid plants. Nature Ecology & Evolution 3: 265–273. PubMed

Ripley B, Venables B, Bates DM, et al. . 2013. Support functions and datasets for Venables and Ripley’s MASS. Package MASS; http://cran. r-project.org/web/packages/MASS/index.html

Robinson DO, Coate JE, Singh A, et al. . 2018. Ploidy and size at multiple scales in the Arabidopsis sepal. The Plant Cell 30: 2308–2329. PubMed PMC

Ronfort J. 1999. The mutation load under tetrasomic inheritance and its consequences for the evolution of the selfing rate in autotetraploid species. Genetics Research 74: 31–42.

R Studio Team 2015. RStudio: integrated development for R. RStudio, Inc., Boston, MA, USA: http://www.rstudio.com/.

Schmickl R, Paule J, Klein J, Marhold K, Koch MA. 2012. The evolutionary history of the Arabidopsis arenosa complex: diverse tetraploids mask the Western Carpathian center of species and genetic diversity. PLoS One 7: e42691. doi: 10.1371/journal.pone.0042691. PubMed DOI PMC

Schönswetter P, Lachmayer M, Lettner C, et al. . 2007. Sympatric diploid and hexaploid cytotypes of Senecio carniolicus (Asteraceae) in the Eastern Alps are separated along an altitudinal gradient. Journal of Plant Research 120: 721–725. PubMed

Segraves KA, Thompson JN. 1999. Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia. Evolution 53: 1114–1127. PubMed

Simón-Porcar VI, Silva JL, Meeus S, Higgins JD, Vallejo-Marín M. 2017. Recent autopolyploidization in a naturalized population of Mimulus guttatus (Phrymaceae). Botanical Journal of the Linnean Society 185: 189–207.

Šingliarová B, Zozomová-Lihová J, Mráz P. 2019. Polytopic origin and scale-dependent spatial segregation of cytotypes in primary diploid–autopolyploid contact zones of Pilosella rhodopea (Asteraceae). Biological Journal of the Linnean Society 126: 360–379.

Sonnleitner M, Flatscher R, Escobar García P, et al. . 2010. Distribution and habitat segregation on different spatial scales among diploid, tetraploid and hexaploid cytotypes of Senecio carniolicus (Asteraceae) in the Eastern Alps. Annals of Botany 106: 967–977. PubMed PMC

Sonnleitner M, Hülber K, Flatscher R, et al. . 2015. Ecological differentiation of diploid and polyploid cytotypes of Senecio carniolicus sensu lato (Asteraceae) is stronger in areas of sympatry. Annals of Botany 117: 269–276. PubMed PMC

Stebbins GL. 1950. Variation and evolution in plants. New York: Columbia University Press.

Sukumaran J, Holder MT. 2010. DendroPy: a Python library for phylogenetic computing. Bioinformatics 26: 1569–1571. PubMed

Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595. PubMed PMC

Thompson KA, Husband BC, Maherali H. 2014. Climatic niche differences between diploid and tetraploid cytotypes of Chamerion angustifolium (Onagraceae). American Journal of Botany 101: 1868–1875. PubMed

Tichý L, Bruelheide H. 2002. JUICE, software for vegetation classification. Journal of Vegetation Science 13: 451–453.

Treier UA, Broennimann O, Normand S, et al. . 2009. Shift in cytotype frequency and niche space in the invasive plant Centaurea maculosa. Ecology 90: 1366–1377. PubMed

Tribsch A, Schönswetter P, Stuessy TF. 2002. Saponaria pumila (Caryophyllaceae) and the Ice Age in the European Alps. American Journal of Botany 89: 2024–2033. PubMed

Van de Peer Y, Mizrachi E, Marchal K. 2017. The evolutionary significance of polyploidy. Nature Reviews. Genetics 18: 411–424. PubMed

Vanderhoeven S, Hardy O, Vekemans X, et al. . 2002. A morphometric study of populations of the Centaurea jacea complex (Asteraceae) in Belgium. Plant Biology 4: 403–412.

Winkler M, Escobar García P, Gattringer A, et al. . 2017. A novel method to infer the origin of polyploids from Amplified Fragment Length Polymorphism data reveals that the alpine polyploid complex of Senecio carniolicus (Asteraceae) evolved mainly via autopolyploidy. Molecular Ecology Resources 17: 877–892. PubMed

Zasadni J, Kłapyta P. 2014. The Tatra Mountains during the Last Glacial Maximum. Journal of Maps 10: 440–456.

Zozomová‐Lihová J, Malánová‐Krásná I, Vít P, et al. . 2015. Cytotype distribution patterns, ecological differentiation, and genetic structure in a diploid–tetraploid contact zone of Cardamine amara. American Journal of Botany 102: 1380–1395. PubMed

Morphological and environmental differentiation as prezygotic reproductive barriers between parapatric and allopatric Campanula rotundifolia agg. cytotypes

Repeated colonization of alpine habitats by Arabidopsis arenosa viewed through freezing resistance and ice management strategies

Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives

Transcriptional activity of transposable elements along an elevational gradient in Arabidopsis arenosa

So Closely Related and Yet So Different: Strong Contrasts Between the Evolutionary Histories of Species of the Cardamine pratensis Polyploid Complex in Central Europe

Intricate Distribution Patterns of Six Cytotypes of Allium oleraceum at a Continental Scale: Niche Expansion and Innovation Followed by Niche Contraction With Increasing Ploidy Level

Parallel Alpine Differentiation in Arabidopsis arenosa