Advertisement

Does geography, evolutionary history or ecology drive ploidy and genome size variation in the Minuartia verna group (Caryophyllaceae) across Europe?

  • Klára Nunvářová KabátováEmail author
  • Filip Kolář
  • Vlasta Jarolímová
  • Karol Krak
  • Jindřich Chrtek
Original Article

Abstract

Polyploidization, a key driver of plant diversification, is believed to have interacted with Pleistocene climatic oscillations and local ecological factors, leading to a complex spatio-ecological mosaic of diploid and polyploid populations. The typical ecogeographic pattern in European plants involves spatially restricted diploids growing in southern regions, interpreted as glacial refugia, and their widespread polyploid derivatives occupying larger and more northerly situated ranges with harsher environments. Whether this is true for individual ploidy-variable groups is, however, largely unknown because we lack sufficiently detailed investigations of ploidy-variable plant groups jointly applying cytological, ecological and genetic methods. We assessed ploidy and genome size variation, elevational and edaphic preferences, and plastid DNA variation within the Minuartia verna aggregate, a group of low-competitive heliophilous plants growing from the Mediterranean to Arctic Europe. Contrary to the expectations, tetraploids have a restricted distribution (Southern Europe) and inhabit a relatively narrow environmental niche. The distribution of diploids, on the other hand, spans the full range of conditions, including climatic (i.e. highest elevations and latitudes) and edaphic extremes (i.e. toxic serpentine and metalliferous substrates). The distribution pattern of the two ploidies could be explained by their distinct evolutionary histories, suggesting expansion of the diploid-dominated haplotype group accompanied by long-term persistence and local differentiation of tetraploids in refugia in the Balkan Peninsula. In summary, our study contradicts the prevailing view of polyploids as successful colonizers of novel and challenging habitats and points to the importance of combining ecological and genetic data when studying ploidy-variable species complexes.

Keywords

Caryophyllaceae Cytogeography Ecology Genome size Polyploidy Sabulina verna group 

Notes

Acknowledgements

We are grateful to Sandro Bogdanović, Zuzana Chumová, Tomáš Figura, Božo Frajman, Adam Knotek, Jan Prančl, Peter Schӧnswetter, Jan Suda, Kristýna Šemberová, Pavel Trávníček, Tomáš Urfus and Petr Vít for their help with the field sampling and plant collection, Pavel Martinec for finalizing the map graphics and to Yuriy Kobiv for consultation. We also thank Lenka Flašková for helping in the molecular biology lab. Fred Rooks kindly improved our English.

Funding

The study was funded by the Grant Agency of Charles University in Prague (GAUK, Project No. 388215), the International Association for Plant Taxonomy (IAPT) via a Research Grant (2015) and partly also by the long-term research development project RVO 67985939 of the Czech Academy of Sciences.

Compliance with ethical standards

Conflict of interest

We state that all subjects involved in the study are mentioned in proper context and that we are aware of no conflict of interest.

Supplementary material

606_2019_1621_MOESM1_ESM.pdf (104 kb)
Supplementary material 1 (PDF 104 kb)
606_2019_1621_MOESM2_ESM.pdf (157 kb)
Supplementary material 2 (PDF 158 kb)
606_2019_1621_MOESM3_ESM.pdf (52 kb)
Supplementary material 3 (PDF 52 kb)
606_2019_1621_MOESM4_ESM.pdf (84 kb)
Supplementary material 4 (PDF 84 kb)
606_2019_1621_MOESM5_ESM.pdf (63 kb)
Supplementary material 5 (PDF 63 kb)
606_2019_1621_MOESM6_ESM.pdf (67 kb)
Supplementary material 6 (PDF 67 kb)

References

  1. Acosta MC, Premoli AC (2010) Evidence of chloroplast capture in South American Nothofagus (subgenus Nothofagus, Nothofagaceae). Molec Phylogenet Evol 54:235–242.  https://doi.org/10.1016/j.ympev.2009.08.008 CrossRefPubMedGoogle Scholar
  2. Albach DC, Greilhuber J (2004) Genome size variation and evolution in Veronica. Ann Bot (Oxford) 94:897–911.  https://doi.org/10.1093/aob/mch219 CrossRefGoogle Scholar
  3. Bancheva S, Greilhuber J (2006) Genome size in Bulgarian Centaurea s.l. (Asteraceae). Pl Syst Evol 257:95–117.  https://doi.org/10.1007/s00606-005-0384-7 CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effect models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  5. Baumbach H (2005) Genetische Differenzierung mitteleuropäischer Schwermetallsippen von Silene vulgaris, Minuartia verna und Armeria maritima unter Berücksichtigung biogeographischer, montanhistorischer und physiologischer Aspekte. Jena, Univ., Diss Bot 398: 1–128Google Scholar
  6. Bennett MD (1976) DNA amount, latitude and crop plant distribution. In: Jones K, Brandham PE (eds) Current chromosome research. Environm Exp Bot 16: 93-108.  https://doi.org/10.1016/0098-8472(76)90001-0 CrossRefGoogle Scholar
  7. Bennett MD, Bhandol P, Leitch IJ (2000) Nuclear DNA amounts in angiosperms and their modern uses: 807 new estimates. Ann Bot (Oxford) 86:859–909.  https://doi.org/10.1006/anbo.2000.1253 CrossRefGoogle Scholar
  8. Bennetzen JL (2002) Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica 115:29–36.  https://doi.org/10.1023/A:1016015913350 CrossRefPubMedGoogle Scholar
  9. Birks HJB, Willis KJ (2008) Alpines, trees and refugia in Europe. Pl Ecol Diversity 1:147–160.  https://doi.org/10.1080/17550870802349146 CrossRefGoogle Scholar
  10. Brochmann C, Brysting AK, Alsos IG, Borgen L, Grundt HH, Scheen A-C, Elven R (2004) Polyploidy in arctic plants. Biol J Linn Soc 82:521–536CrossRefGoogle Scholar
  11. Calgano V, de Mazancourt C (2010) Glmulti: an R package for easy automated model selection with (generalized) linear models. J Stat Softw 34:1–29.  https://doi.org/10.18637/jss.v034.i12 CrossRefGoogle Scholar
  12. Casazza G, Granato L, Minuto L, Conti E (2012) Polyploid evolution and pleistocene glacial cycles: a case study from the alpine primrose Primula marginata (Primulaceae). BMC Evol Biol 12:56.  https://doi.org/10.1186/1471-2148-12-56 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Clarkson JJ, Lim KY, Kovarik A, Chase MW, Knapp S, Leitch AR (2005) Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytol 168:241–252.  https://doi.org/10.1111/j.1469-8137.2005.01480.x CrossRefPubMedGoogle Scholar
  14. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Molec Ecol 9:1657–1660.  https://doi.org/10.1046/j.1365-294x.2000.01020.x CrossRefGoogle Scholar
  15. Dalgaard V (1989) Chromosome numbers in vascular plants from the Disko Bugt area (West Greenland). Willdenowia 19:199–213Google Scholar
  16. Davis SD, Sperry JS, Hacke UG (1999) The relationship between xylem conduit diameter and cavitation caused by freezing. Amer J Bot 86:1367–1372.  https://doi.org/10.2307/2656919 CrossRefGoogle Scholar
  17. de Montmollin B (1986) Etude cytotaxonomique de la flore de la Crète. III. Nombres chromosomiques. Candollea 41:431–439Google Scholar
  18. Devos KMJ, Brown KM, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079.  https://doi.org/10.1101/gr.132102 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Dillenberger MS, Kadereit JW (2014) Maximum polyphyly: multiple origins and delimitation with plesiomorphic characters require a new circumscription of Minuartia (Caryophyllaceae). Taxon 63:64–88.  https://doi.org/10.12705/631.5 CrossRefGoogle Scholar
  20. Doležel J, Bartoš J (2005) Plant DNA flow cytometry and estimation of nuclear genome size. Ann Bot (Oxford) 95:99–110.  https://doi.org/10.1159/000082381 CrossRefGoogle Scholar
  21. Doležel J, Greilhuber J, Suda J (2007) Estimation of nuclear DNA content in plants using flow cytometry. Nature Protoc 2:2233–2244.  https://doi.org/10.1038/nprot.2007.310 CrossRefGoogle Scholar
  22. Doyle JJ (2012) Polyploidy in legumes. In: Soltis PS, Soltis DE (eds) Polyploidy and genome evolution. Springer, Heidelberg, pp 147–180.  https://doi.org/10.1007/978-3-642-31442-1_9 CrossRefGoogle Scholar
  23. Dvořáková M (1985) Minuartia glaucina – eine neue Art der Minuartia verna-Gruppe. Preslia 57:1–8Google Scholar
  24. Dvořáková M (1988) Minuartia smejkalii, eine neue Art der Minuartia gerardii-Gruppe (Caryophyllaceae). Preslia 60:1–9Google Scholar
  25. Dvořáková M (1991) Zur Taxonomie und Chorologie von Minuartia orthophylla (Caryophyllaceae). Preslia 63:1–7Google Scholar
  26. Dvořáková M (1999) Zwei neue zur Sektion Polymechana gehörende Minuartia-Arten (Caryophyllaceae). Preslia 70:335–338Google Scholar
  27. Dvořáková M (2000) Taxonomický přehled evropských druhů rodu Minuartia ze sekce Polymechana Mattf. (Taxonomic treatment of Minuartia sect. Polymechana in Europe). In: Soubor prací s taxonomicko-chorologickou tématikou, PhD Thesis, Masaryk University, BrnoGoogle Scholar
  28. Dvořáková M (2003a) Zur Taxonomie und Chorologie der Art Minuartia kabylica. Preslia 75:81–84Google Scholar
  29. Dvořáková M (2003b) Minuartia pauciflora, das karpatische endemit aus der M. verna-Gruppe. Preslia 75:349–356Google Scholar
  30. Ehrendorfer F (1979) Polyploidy and distribution. Basic Life Sci 13:45–60.  https://doi.org/10.1007/978-1-4613-3069-1_3 CrossRefPubMedGoogle Scholar
  31. Ekrt L, Trávníček P, Jarolímová V, Vít P, Urfus T (2009) Genome size and morphology of the Dryopteris affinis group in Central Europe. Preslia 81:261–280Google Scholar
  32. Favarger C (1967) Nombres chromosomiques de quelques taxa principalement balkaniques du genre Minuartia (L.) Hiern. Bot Jahrb Syst 86:280–292Google Scholar
  33. Favarger C (1973) Cytotaxonomie de quelques orophytes des Abruzzes. Acta Bot Acad Sci Hung 19:81–92Google Scholar
  34. Favarger C, Montserrat Recoder P (1987) Commentaires sur la caryologie des espèces de Minuartia L. de la Péninsule Ibérique. Anales Jard Bot Madrid 44:558–564Google Scholar
  35. Frajman B, Rešetnik I, Weiss-Schneeweiss H, Ehrendorfer F, Schönswetter P (2015) Cytotype diversity and genome size variation in Knautia (Caprifoliaceae, Dipsacoideae). BMC Evol Biol 15:140.  https://doi.org/10.1186/s12862-015-0425-y CrossRefPubMedPubMedCentralGoogle Scholar
  36. Franzén R, Gustavsson L-Ǻ (1983) Chromosome numbers in flowering plants from the high mountains of Sterea Ellas, Greece. Willdenowia 13:101–106Google Scholar
  37. 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.). 1. Insights from morphological and allozyme markers. Heredity 80:683–693.  https://doi.org/10.1046/j.1365-2540.1998.00334.x CrossRefGoogle Scholar
  38. Glennon KL, Ritchie ME, Segraves KA (2014) Evidence for shared broad-scale climatic niches of diploid and polyploid plants. Ecol Lett 17:574–582.  https://doi.org/10.1111/ele.12259 CrossRefPubMedGoogle Scholar
  39. Goldblatt P, Johnson DE (eds) (1979) Index to plant chromosome numbers. Missouri Botanical Garden, St. LouisGoogle Scholar
  40. Graebner P (1918) Minuartia L. In: Ascherson P, Graebner P (eds) Synopsis der mitteleuropäischen Flora, vol. 5/1. Gebrüder Borntraeger, Leipzig, pp 698–776Google Scholar
  41. Grant V (1981) Plant speciation, 2nd edn. Columbia Univ Press, New York.  https://doi.org/10.1111/j.1469-8137.2004.00964.x CrossRefGoogle Scholar
  42. Grdiša M, Liber Z, Radosavljević I, Carović-Stanko K, Kolak I, Satovic Z (2014) Genetic diversity and structure of dalmatian pyrethrum (Tanacetum cinerariifolium Trevir. /Sch./ Bip., Asteraceae) within the Balkan refugium. PLoS ONE 9(8):e105265.  https://doi.org/10.1371/journal.pone.0105265 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Greilhuber J (1998) Intraspecific variation in genome size: a critical reassessment. Ann Bot (Oxford) 82:27–35.  https://doi.org/10.1006/anbo.1998.0725 CrossRefGoogle Scholar
  44. Greilhuber J (2005) Intraspecific variation in genome size in angiosperms: identifying its existence. Ann Bot (Oxford) 95:91–98.  https://doi.org/10.1093/aob/mci004 CrossRefGoogle Scholar
  45. Habel JC, Drees C, Schmitt T, Assmann T (2010) Refugial areas and postglacial colonizations in the western palearctic. In: Habel JC, Assmann T (eds) Relict species. Springer, Berlin, pp 189–198.  https://doi.org/10.1007/978-3-540-92160-8_10 CrossRefGoogle Scholar
  46. Hall TA (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  47. Halliday G (1964) Studies in the Minuartia verna complex. In: Heywood VH (ed) Notulae ad floram europaeam spectantes, no 3, vol. 69. Feddes Repert, pp 8–14Google Scholar
  48. Halliday G (1993) Minuartia L. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea, 2nd edn, vol. 1. Cambridge UP, Cambridge, pp 152–160Google Scholar
  49. Hampe A, Jump AS (2011) Climate relicts: past, present, future. Annual Rev Ecol Evol Syst 42:313–333.  https://doi.org/10.1146/annurev-ecolsys-102710-145015 CrossRefGoogle Scholar
  50. Hayek A (1922) Versuch einer natürlichen Gliederung des Formenkreises der Minuartia verna (L.) Hiern. Oesterr Bot Z 71:88–116.  https://doi.org/10.1007/BF01635217 CrossRefGoogle Scholar
  51. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276.  https://doi.org/10.1111/j.1095-8312.1996.tb01434.x CrossRefGoogle Scholar
  52. Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112.  https://doi.org/10.1111/j.1095-8312.1999.tb01160.x CrossRefGoogle Scholar
  53. Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913.  https://doi.org/10.1038/35016000 CrossRefGoogle Scholar
  54. Husband BC, Schemske DW (1998) Cytotype distribution at a diploid-tetraploid contact zone in Chamerion (Epilobium) angustifolium (Onagraceae). Amer J Bot 85:1688–1694.  https://doi.org/10.2307/2446502 CrossRefGoogle Scholar
  55. Husband BC, Baldwin SJ, Suda J (2013) The incidence of polyploidy in natural plant populations: major patterns and evolutionary processes. In: Leitch IJ, Greilhuber J, Doležel J, Wendel JF (eds) Plant genome diversity 2: physical structure, behaviour and evolution of plant genomes. Springer, Wien, pp 255–276.  https://doi.org/10.1007/978-3-7091-1160-4_16 CrossRefGoogle Scholar
  56. Ingvarsson P, Ribstein S, Taylor D (2003) Molecular evolution of insertions and deletion in the chloroplast genome of Silene. Molec Biol Evol 20:1737–1740.  https://doi.org/10.1093/molbev/msg163 CrossRefPubMedGoogle Scholar
  57. Kamari G, Constantinidis T (1994) The Minuartia verna complex in Greece. Bot Chron (Patras) 11:41–54Google Scholar
  58. King RA, Ferris C (1998) Chloroplast DNA phylogeography of Alnus glutinosa. Molec Ecol 7:1151–1161.  https://doi.org/10.1046/j.1365-294x.1998.00432.x CrossRefGoogle Scholar
  59. Knight CA, Molinari NA, Petrov DA (2005) The large genome constraint hypothesis: evolution, ecology and phenotype. Ann Bot (Oxford) 95:177–190.  https://doi.org/10.1093/aob/mci011 CrossRefGoogle Scholar
  60. 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). Biol J Linn Soc 125:491–507.  https://doi.org/10.1093/biolinnean/bly126 CrossRefGoogle Scholar
  61. Kochjarová J (1992) Karyological study of the Slovak flora XXVIII. Acta Fac Rerum Nat Univ Comen Bot 39:67–74Google Scholar
  62. Kolář F, Fér T, Štech M, Trávníček P, Dušková E, Schönswetter P, Suda J (2012) Bringing together evolution on serpentine and polyploidy: spatiotemporal history of the diploid-tetraploid complex of Knautia arvensis (Dipsacaceae). PLoS ONE 7:e39988.  https://doi.org/10.1371/journal.pone.0039988 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Körner C (1989) The nutritional status of plants from high altitudes. A worldwide comparison. Oecologia 81:379–391.  https://doi.org/10.1007/BF00377088 CrossRefPubMedGoogle Scholar
  64. Kron P, Suda J, Husband BC (2007) Applications of flow cytometry to evolutionary and population biology. Annual Rev Ecol Syst 38:847–876.  https://doi.org/10.1146/annurev.ecolsys.38.091206.095504 CrossRefGoogle Scholar
  65. Kurtto A (1983) Atlas Florae Europaeae notes. III: chorology and taxonomy of some SE European taxa of the Caryophyllaceae, subfamilies Alsinoideae and Paronychioideae. Ann Bot Fenn 20:357–360Google Scholar
  66. Lakušić D, Liber Z, Nikolić T, Surina B, Kovačić S, Bogdanović S, Stefanović S (2013) Molecular phylogeny of the Campanula pyramidalis species complex (Campanulaceae) inferred from chloroplast and nuclear non-coding sequences and its taxonomic implications. Taxon 62:505–524.  https://doi.org/10.12705/623.1 CrossRefGoogle Scholar
  67. Laurie DA, Bennett MD (1985) Nuclear DNA content in the genera Zea and Sorghum: intergeneric, interspecific and intraspecific variation. Heredity 55:307–313.  https://doi.org/10.1038/hdy.1985.112 CrossRefGoogle Scholar
  68. Lausi D, Cusma Velari T (1992) Cariologia di taxa critici su suoli calaminari (Cave del Predil, Alpi Giulie, Italia). Stud Geobot 12:153–167Google Scholar
  69. Lazarević M, Kuzmanović N, Lakusić D, Alegro A, Schӧnswetter P, Frajman B (2015) Patterns of cytotype distribution and genome size variation in the genus Sesleria Scop. (Poaceae). Bot J Linn Soc 179:126–143.  https://doi.org/10.1111/boj.12306 CrossRefGoogle Scholar
  70. Leitch I, Bennett MD (2004) Genome downsizing in polyploid plants. Biol J Linn Soc 82:651–663.  https://doi.org/10.1111/j.1095-8312.2004.00349.x CrossRefGoogle Scholar
  71. Leitch IJ, Hanson L, Lim KY, Kovarik A, Chase MW, Clarkson JJ, Leitch AR (2008) The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae). Ann Bot (Oxford) 101:805–814.  https://doi.org/10.1093/aob/mcm326 CrossRefGoogle Scholar
  72. Leong-Škorničková J, Šída O, Jarolímová V, Sabu M, Fér T, Trávníček P, Suda J (2007) Chromosome numbers and genome size variation in Indian species of Curcuma (Zingiberaceae). Ann Bot (Oxford) 100:505–526.  https://doi.org/10.1093/aob/mcm144 CrossRefGoogle Scholar
  73. Lepais O, Muller SD, Saad-Limam SB, Benslama M, Rhazi L, Belouahem-Abed D, Daoud-Bouattour A, Gammar AM, Ghrabi-Gammar Z, Bacles CFE (2013) High genetic diversity and distinctiveness of rear-edge climate relicts maintained by ancient tetraploidisation for Alnus glutinosa. PLoS ONE 8:e75029.  https://doi.org/10.1371/journal.pone.0075029 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Levin DA (2000) The origin, expansion, and demise of plant species. Oxford University Press, New YorkGoogle Scholar
  75. Levin DA (2002) The role of chromosomal change in plant evolution. Oxford University Press, OxfordGoogle Scholar
  76. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452.  https://doi.org/10.1093/bioinformatics/btp187 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Loureiro J, Trávníček P, Rauchová J, Urfus T, Vít P, Štech M, Castro S, Suda J (2010) The use of flow cytometry in the biosystematics, ecology and population biology of homoploid plants. Preslia 82:3–21Google Scholar
  78. Löve Á (1980a) Chromosome number reports LXVIII. Taxon 29:533–547CrossRefGoogle Scholar
  79. Löve Á (1980b) Chromosome number reports LXIX. Taxon 29:703–730CrossRefGoogle Scholar
  80. Ma JK, Devos M, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869.  https://doi.org/10.1101/gr.1466204 CrossRefPubMedPubMedCentralGoogle Scholar
  81. MacGillivray CW, Grime JP (1995) Genome size predicts frost resistance in British herbaceous plants: implications for rates of vegetation response to global warming. Funct Ecol 9:320–325.  https://doi.org/10.2307/2390580 CrossRefGoogle Scholar
  82. Májovský J, Uhríková A (1985) Karyotaxonomisches Studium einiger Arten der slowakischen Flora V. Acta Fac Rerum Nat Univ Comen Bot 32:59–65Google Scholar
  83. Májovský J, Uhríková A, Javorčíková D, Mičieta K, Králik E, Dúbravcová Z, Feráková V, Murín A, Černušáková D, Hindáková M, Schwarzová T, Záborský J (2000) Prvý doplnok karyotaxonomického prehľadu flóry Slovenska. Acta Fac Rerum Nat Univ Comen Bot, Suppl 1:1–127Google Scholar
  84. Mandák B, Vít P, Krak K, Trávníček P, Havrdová A, Hadincová V, Zákravský P, Jarolímová V, Bacles CFE, Douda J (2016) Flow cytometry, microsatellites and niche models reveal the origins and geographical structure of Alnus glutinosa populations in Europe. Ann Bot (Oxford) 117:107–120.  https://doi.org/10.1093/aob/mcv158 CrossRefGoogle Scholar
  85. Mandáková T, Joly S, Krzywinski M, Mummenhoff K, Lysak MA (2010) Fast diploidization in close mesopolyploid relatives of Arabidopsis. Pl Cell 22:2277–2290.  https://doi.org/10.1105/tpc.110.074526 CrossRefGoogle Scholar
  86. Martin SL, Husband BC (2013) Adaptation of diploid and tetraploid Chamerion angustifolium to elevation but not local environment. Evolution 67:1780–1791.  https://doi.org/10.1111/evo.12065 CrossRefPubMedGoogle Scholar
  87. Meusel HE, Jäger E, Weinert E (1965) Vergleichende Chorologie der zentraleuropäischen Flora. Gustav Fischer Verlag, JenaGoogle Scholar
  88. Murray BG (2005) When does intraspecific C-value variation become taxonomically significant? Ann Bot (Oxford) 95:119–125.  https://doi.org/10.1093/aob/mci007 CrossRefGoogle Scholar
  89. Nieto Feliner G (2011) Southern European glacial refugia: a tale of tales. Taxon 60:365–372.  https://doi.org/10.1002/tax.602007 CrossRefGoogle Scholar
  90. Nieto Feliner G (2014) Patterns and processes in plant phylogeography in the Mediterranean basin: a review. Perspect Pl Ecol Evol Syst 16:265–278.  https://doi.org/10.1016/j.ppees.2014.07.002 CrossRefGoogle Scholar
  91. Obermayer R, Greilhuber J (2005) Does genome size in Dasypyrum villosum vary with fruit colour? Heredity 95:91–95.  https://doi.org/10.1038/sj.hdy.6800696 CrossRefPubMedGoogle Scholar
  92. Otto F (1990) DAPI staining of fixed cells for high-resolution flowcytometry of nuclear DNA. In: Crissman HA, Darzynkiewicz Z (eds) Methods in cell biology: flow cytometry. Academic Press, San Diego, pp 105–110.  https://doi.org/10.1016/S0091-679X(08)60516-6 CrossRefGoogle Scholar
  93. Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annual Rev Genet 34:401–437.  https://doi.org/10.1146/annurev.genet.34.1.401 CrossRefPubMedGoogle Scholar
  94. Parisod C, Holderegger R, Brochmann C (2010) Evolutionary consequences of autopolyploidy. New Phytol 186:5–17.  https://doi.org/10.1111/j.1469-8137.2009.03142.x CrossRefPubMedGoogle Scholar
  95. Pawłowski B (1939) Stanowisko systematyczne i pokrewienstwo Minuartia oxypetala (Wol.) Kulcz. Acta Soc Bot Poloniae 16:153–166CrossRefGoogle Scholar
  96. Petit C, Lesbros P, Ge X, Thompson JD (1997) Variation in flowering phenology and selfing rate across a contact zone between diploid and tetraploid Arrhenatherum elatius (Poaceae). Heredity 79:31–40.  https://doi.org/10.1038/hdy.1997.120 CrossRefGoogle Scholar
  97. Petrov D (2001) Evolution of genome size: new approaches to an old problem. Trends Genet 17:23–28.  https://doi.org/10.1016/S0168-9525(00)02157-0 CrossRefPubMedGoogle Scholar
  98. Pignatti S (1974) Note critiche sulla flora d´Italia. II. Il gruppo di Minuartia verna. Giorn Bot Ital 108:95–104.  https://doi.org/10.1080/11263507409426351 CrossRefGoogle Scholar
  99. Price HJ, Chambers KL, Bachmann K (1981) Genome size variation in diploid Microseris bigelovii (Asteraceae). Bot Gaz 142:156–159.  https://doi.org/10.1086/337206 CrossRefGoogle Scholar
  100. Pustahija F, Brown SC, Bogunić F, Bašić N, Muratović E, Ollier S, Hidalgo O, Bourge M, Stevanović V, Siljak-Yakovlev S (2013) Small genomes dominate in plants growing on serpentine soils in west Balkans, an exhaustive study of 8 habitats covering 308 taxa. Pl Soil 373:427–453.  https://doi.org/10.1007/s11104-013-1794-x CrossRefGoogle Scholar
  101. R Core Team (2014) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. Available at: http://www.R-project.org/
  102. Ramsey J, Ramsey TS (2014) Ecological studies of polyploidy in the 100 years following its discovery. Philos Trans R Soc Lond B Biol Sci 369:20130352.  https://doi.org/10.1098/rstb.2013.0352 CrossRefPubMedPubMedCentralGoogle Scholar
  103. Ramsey J, Schemske DW (2002) Neopolyploidy in flowering plants. Annual Rev Ecol Syst 33:589–639.  https://doi.org/10.1146/annurev.ecolsys.33.010802.150437 CrossRefGoogle Scholar
  104. Raven PH, Evert RF, Eichhorn E (1986) Biology of plants, 4th edn. Worth Publishers, New YorkGoogle Scholar
  105. Rayburn AL, Auger JA (1990) Genome size variation in Zea mays ssp. mays adapted to different altitudes. Theor Appl Genet 79:470–474.  https://doi.org/10.1007/BF00226155 CrossRefPubMedGoogle Scholar
  106. Regele D, Gruenebach 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.  https://doi.org/10.23855/preslia.2017.291 CrossRefGoogle Scholar
  107. Rešetnik I, Baričevič D, Batîr Rusu D, Carović-Stanko K, Chatzopoulou P, Dajić-Stevanović Z, Gonceariuc M, Grdiša M, Greguraš D, Ibraliu A, Jug-Dujaković M, Krasniqi E, Liber Z, Murtić S, Pećanac D, Radosavljević I, Stefkov G, Stešević D, Šoštarić I, Šatović Z (2016) Genetic diversity and demographic history of wild and cultivated/naturalised plant populations: evidence from Dalmatian sage (Salvia officinalis L., Lamiaceae). PLoS ONE 11:e0159545.  https://doi.org/10.1371/journal.pone.0159545 CrossRefPubMedPubMedCentralGoogle Scholar
  108. Rice A, Glick L, Abadi S, Einhorn M, Kopelman NM, Salman-Minkov A, Mayzel J, Chay O, Mayrose I (2015) The chromosome counts database (CCDB) – a community resource of plant chromosome numbers. New Phytol 206:19–26.  https://doi.org/10.1111/nph.13191 CrossRefPubMedGoogle Scholar
  109. Roskov Y, Ower G, Orrell T, Nicolson D, Bailly N, Kirk PM, Bourgoin T, DeWalt RE, Decock W, Nieukerken E, van Zarucchi J, Penev L (eds) (2019) Species 2000 & ITIS catalogue of life, 25th March 2019. Naturalis, Leiden. Available at: www.catalogueoflife.org/col.
  110. Runemark H (1996) Reports (590–678). In: Kamari G, Felber F, Garbari F (eds) Mediterranean chromosome number report – 6. Fl Medit 6:223–243Google Scholar
  111. Sӑvulescu T (ed) (1953) Flora Republicii Populare Române, vol. 2. Editura Academiei Republicii Populare Române, BucureştiGoogle Scholar
  112. Schinkel CCF, Kirchheimer B, Dellinger A, Klatt S, Winkler M, Dullinger S, Hӧrandl E (2016) Correlations of polyploidy and apomixis with elevation and associated environmental gradients in an alpine plant. AoB PLANTS 8:plw064.  https://doi.org/10.1093/aobpla/plw064 CrossRefPubMedPubMedCentralGoogle Scholar
  113. Schmitt T, Varga Z (2012) Extra-mediterranean refugia: the rule and not the exception? Frontiers Zool 9:22.  https://doi.org/10.1186/1742-9994-9-22 CrossRefPubMedPubMedCentralGoogle Scholar
  114. Schönswetter P, Suda J, Popp M, Weiss-Schneeweiss H, Brochmann C (2007) Circumpolar phylogeography of Juncus biglumis (Juncaceae) inferred from AFLP fingerprints, cpDNA sequences, nuclear DNA content and chromosome numbers. Molec Phylogen Evol 42:92–103.  https://doi.org/10.1016/j.ympev.2006.06.016 CrossRefGoogle Scholar
  115. Segraves KA, Thompson JN, Soltis PS, Soltis DE (1999) Multiple origins of polyploidy and the geographic structure of Heuchera grossulariifolia. Molec Ecol 8:253–262.  https://doi.org/10.1046/j.1365-294X.1999.00562.x CrossRefGoogle Scholar
  116. Siljak-Yakovlev S, Pustahija F, Šolić EM, Bogunić F, Muratović E, Bašić N, Catrice O, Brown SC (2010) Towards a genome size and chromosome number database of Balkan flora: c-values in 343 taxa with novel values for 242. Advanced Sci Lett 3:190–213.  https://doi.org/10.1166/asl.2010.1115 CrossRefGoogle Scholar
  117. Slovák M, Vít P, Urfus T, Suda J (2009) Complex pattern of genome size variation in a polymorphic member of the Asteraceae. J Biogeogr 36:372–384.  https://doi.org/10.1111/j.1365-2699.2008.02005.x CrossRefGoogle Scholar
  118. Šmarda P, Bureš P, Horová L, Foggi B, Rossi G (2008) Genome size and GC content evolution of Festuca ancestral expansion and subsequent reduction. Ann Bot (Oxford) 101:421–433.  https://doi.org/10.1093/aob/mcm307 CrossRefGoogle Scholar
  119. Soltis DE (1984) Autopolyploidy in Tolmiea menziesii (Saxifragaceae). Amer J Bot 71:1171–1174.  https://doi.org/10.1002/j.1537-2197.1984.tb11971.x CrossRefGoogle Scholar
  120. Soltis DE, Buggs RJA, Barbazuk WB, Chamala S, Chester M, Gallagher JP, Schnable PS, Soltis PS (2012) The early stages of polyploidy: rapid and repeated evolution in Tragopogon. In: Soltis DE (ed) Polyploidy and genome evolution. Springer, Berlin, pp 271–292.  https://doi.org/10.1007/978-3-642-31442-1_14 CrossRefGoogle Scholar
  121. Soltis DE, Visger CJ, Marchant DB, Soltis PS (2016) Polyploidy: pitfalls and paths to a paradigm. Amer J Bot 103:1146–1166.  https://doi.org/10.3732/ajb.1500501 CrossRefGoogle Scholar
  122. Sonnleitner M, Flatscher R, Escobar García P, Rauchová J, Suda J, Schneeweiss GM, Hülber K, Schönswetter P (2010) Distribution and habitat segregation on different spatial scales among diploid, tetraploid and hexaploid cytotypes of Senecio carniolicus (Asteraceae) in the Eastern Alps. Ann Bot (Oxford) 106:967–977.  https://doi.org/10.1093/aob/mcq192 CrossRefGoogle Scholar
  123. Španiel S, Marhold K, Zozomová-Lihová J (2017) The polyploid Alyssum montanum-A. repens complex in the Balkans: a hotspot of species and genetic diversity. Pl Syst Evol 303:1443–1465.  https://doi.org/10.1007/s00606-017-1470-3 CrossRefGoogle Scholar
  124. Stace CA (2000) Cytology and cytogenetics as a fundamental taxonomic resource for the 20th and 21st centuries. Taxon 49:451–477.  https://doi.org/10.2307/1224344 CrossRefGoogle Scholar
  125. Starlinger F, Vitek E, Pascher K, Kiehn M (1994) Neue Chromosomenzählungen für die Flora Rumäniens. In: Heltmann H, Wendelberger G (eds) Beiträge zur Flora, Vegetation und Fauna von Siebenbürgen. Naturwiss Forsch Siebenbürgen 5:181–194Google Scholar
  126. Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New YorkCrossRefGoogle Scholar
  127. Stebbins GL (1971) Chromosomal evolution in higher plants. Edward Arnold (Publishers) Ltd., LondonGoogle Scholar
  128. Stebbins GL (1984) Polyploidy and the distribution of the arctic-alpine flora: new evidence and a new approach. Bot Helv 94:1–13Google Scholar
  129. Stewart JR, Lister AM (2001) Cryptic northern refugia and the origins of the modern biota. Trends Ecol Evol 16:608–611.  https://doi.org/10.1016/S0169-5347(01)02338-2 CrossRefGoogle Scholar
  130. Stewart JR, Lister AM, Barnes I, Dalén L (2010) Refugia revisited: individualistic responses of species in space and time. Proc Roy Soc B Biol Sci 277:661–671.  https://doi.org/10.1098/rspb.2009.1272 CrossRefGoogle Scholar
  131. Štorchová H, Hrdličková R, Chrtek J Jr, Tetera M, Fitze D, Fehrer J (2000) An improved method of DNA isolation from plants collected in the field and conserved in saturated NaCl/CTAB solution. Taxon 49:79–84.  https://doi.org/10.2307/1223934 CrossRefGoogle Scholar
  132. Strid A (1980) Reports. In: Löve Á (ed.) Chromosome number reports LXIX, Taxon 29: 709–710. https://www.jstor.org/stable/1220359
  133. Suda J, Krahulcová A, Trávníček P, Rosenbaumová R, Peckert T, Krahulec F (2007a) Genome size variation and species relationships in Hieracium subgenus Pilosella (Asteraceae) as inferred by flow cytometry. Ann Bot (Oxford) 100:1323–1335.  https://doi.org/10.1093/aob/mcm218 CrossRefGoogle Scholar
  134. Suda J, Weiss-Schneeweiss H, Tribsch A, Schneeweiss G, Trávníček P, Schönswetter P (2007b) Complex distribution patterns of di-, tetra- and hexaploid cytotypes in the European high mountain plant Senecio carniolicus willd. (Asteraceae). Amer J Bot 94:1391–1401.  https://doi.org/10.3732/ajb.94.8.1391 CrossRefGoogle Scholar
  135. Surina B, Schönswetter P, Schneeweiss GM (2011) Quaternary range dynamics of ecologically divergent species (Edraianthus serpyllifolius and E. tenuifolius, Campanulaceae) within the Balkan refugium. J Biogeogr 38:1381–1393.  https://doi.org/10.1111/j.1365-2699.2011.02493.x CrossRefGoogle Scholar
  136. Temsch EM, Temsch W, Ehrendorfer-Schratt L, Greilhuber J (2010) Heavy metal pollution, selection, and genome size: the species of the Žerjav study revisited with flow cytometry. J Bot 2010:596542.  https://doi.org/10.1155/2010/596542 Google Scholar
  137. Thompson KA, Husband BC, Maherali H (2014) Climatic niche differences between diploid and tetraploid cytotypes of Chamerion angustifolium (Onagraceae). Amer J Bot 101:1868–1875.  https://doi.org/10.3732/ajb.1400184 CrossRefGoogle Scholar
  138. Turrill WB (1929) The plant-life of the Balkan peninsula. A phytogeographical study. Clarendon, OxfordGoogle Scholar
  139. Uhríková A, Králik E (2000) Karyologické štúdium slovenskej flóry XXIX. Acta Fac Rerum Nat Univ Comen Bot 40:17–22Google Scholar
  140. Uhríková A, Dúbravcová Z, Králik E, Paclová L (1983) Report. In: Löve Á (ed) IOPB Chromosome number reports LXXX, Taxon 32: 507Google Scholar
  141. Weiss-Schneeweiss H, Greilhuber J, Schneeweiss GM (2006) Genome size evolution in holoparasitic Orobanche (Orobanchaceae) and related genera. Amer J Bot 93:148–156.  https://doi.org/10.3732/ajb.93.1.148 CrossRefGoogle Scholar
  142. Weiss-Schneeweiss H, Schneeweiss GM, Stuessy TF, Mabuchi T, Park JM, Jang CG, Sun BY (2007) Chromosomal stasis in diploids contrasts with genome restructuring in auto- and allopolyploid taxa of Hepatica (Ranunculaceae). New Phytol 174:669–682.  https://doi.org/10.1111/j.1469-8137.2007.02019.x CrossRefPubMedGoogle Scholar
  143. Weiss-Schneeweiss H, Emadzade K, Jang TS, Schneeweiss GM (2013) Evolutionary consequences, constraints and potential of polyploidy in plants. Cytogenet Genome Res 140:137–150.  https://doi.org/10.1159/000351727 CrossRefPubMedGoogle Scholar
  144. Wendel JF (2015) The wondrous cycles of polyploidy in plants. Amer J Bot 102:1753–1756.  https://doi.org/10.3732/ajb.1500320 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Botany, Faculty of ScienceCharles University in PraguePrague 2Czech Republic
  2. 2.Institute of Botany of the Czech Academy of SciencesPrůhoniceCzech Republic
  3. 3.Department of BotanyUniversity of InnsbruckInnsbruckAustria
  4. 4.Faculty of Environmental SciencesCzech University of Life Sciences PraguePragueCzech Republic

Personalised recommendations