Patterns of genetic variation in Pilosella echioides and its selected relatives: results of variation in ploidy level, facultative apomixis and past and present hybridization

Abstract

We used allozymes to elucidate the genetic variation of Pilosella echioides and P. rothiana in the Pannonian Basin and its relationship with morphology and modes of reproduction. The former species consists of sexual diploid, apomictic tetraploid, and very rare sexual tetraploid populations; the latter is exclusively tetraploid and apomictic. As expected, we detected the highest intra-population variation in diploid populations of P. echioides. Nonetheless, 73 % of populations of tetraploid P. echioides and 64 % of P. rothiana consisted of 2–7 multilocus allozyme genotypes, the means being 5.75 in P. echioides and 2.64 in P. rothiana. Both the proportion of distinguishable genotypes (G/N) per population and genotype diversity (D) per population significantly differed between diploid P. echioides (means 0.415 and 0.828, respectively) on the one hand and tetraploid P. echioides (means 0.252 and 0.387, respectively) and P. rothiana (means 0.213 and 0.347, respectively) on the other. Rather surprisingly, we found an excess of homozygotes (positive F IS) in diploids, which indicates inbreeding. Tetraploids of P. echioides have most likely originated from only a few polyploidization events and have spread thanks to agamospermy—at least populations from the NW part of the area under study seem to be monophyletic. Genetic differences within the putatively hybridogeneous species P. rothiana are small. It seems plausible that it has a common origin and that it spreads independently of its parents (P. echioides and P. officinarum). A certain level of genetic diversity can be caused by residual sexuality or less likely by repeated polytopic hybridization between P. echioides and P. officinarum. Pilosella sterrochaetia is reported here from Hungary for the first time. It is an extremely rare primary diploid hybrid between diploid P. echioides and P. leucopsilon. Its intermediate nuclear genome size also confirms its hybrid origin.

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References

  1. Arft AM, Ranker TA (1998) Allopolyploid origin and population genetics of the rare orchid Spiranthes diluvialis. Amer J Bot 85:110–122

    Article  CAS  Google Scholar 

  2. Bräutigam S (1992) Hieracium L. In: Meusel H, Jäger EJ (eds) Vergleichende Chorologie der zentraleuropäischen Flora 3. Gustav Fischer, Jena, pp 325–333, 550–560

  3. Brochmann C, Soltis DE, Soltis PS (1992) Electrophoretic relationships and phylogeny of Nordic polyploids in Draba (Brassicaceae). Pl Syst Evol 182:35–70

    Article  Google Scholar 

  4. Bruun HH, Scheepens JF, Tyler T (2007) An allozyme study of sexual and vegetative regeneration in Hieracium pilosella L. Can J Bot 85:10–15

    Article  CAS  Google Scholar 

  5. Crawford DJ, Archibald JK, Santos-Guerra A, Mort ME (2006) Allozyme diversity within and divergence among species of Tolpis (Asteraceae-Lactuceae) in the Canary Islands: systematic, evolutionary, and biogeographical implications. Amer J Bot 93:656–664

    Article  CAS  Google Scholar 

  6. Doležel J, Doleželová M, Novák FJ (1994) Flow cytometric estimation of nuclear DNA amount in diploid bananas (Musa acuminata and M. balbisiana). Biol Pl 36:351–357

    Article  Google Scholar 

  7. Doležel J, Greilhuber J, Suda J (2007) Estimation of nuclear DNA content in plants using flow cytometry. Nat Prot 2:2233–2244

    Article  Google Scholar 

  8. Eckert CG, Barrett SCH (1993) Clonal reproduction and patterns of genotypic diversity in Decodon verticillatus (Lythraceae). Amer J Bot 80:1175–1182

    Article  Google Scholar 

  9. Ellstrand NC, Roose ML (1987) Patterns of genotypic diversity in clonal plant species. Amer J Bot 74:121–131

    Article  Google Scholar 

  10. Fehrer J, Šimek R, Krahulcová A, Krahulec F, Chrtek J Jr., Bräutigam E, Bräutigam S (2005) Evolution, hybridisation, and clonal distribution of apo- and amphimictic species of Hieracium subgen. Pilosella (Asteraceae: Lactuceae) in a Central European mountain range. In: Bakker FT, Chatrou LW, Gravendeel B, Pelser PB (eds) Plant species-level systematic: new perspectives an pattern and process. Koeltz, Königstein (Regnum Veget 143:175–201)

  11. Fehrer J, Krahulcová A, Krahulec F, Chrtek J Jr, Rosenbaumová R, Bräutigam S (2007) Evolutionary aspects in Hieracium subgenus Pilosella. In: Hörandl E, Grossniklaus U, van Dijk PJ, Sharbel TF (eds) Apomixis. Evolution, mechanisms and perspectives. A. R. G. Gantner, Rugell, pp 359–390

  12. Gadella TWJ (1987) Sexual tetraploid and apomictic pentaploid populations of Hieracium pilosella (Compositae). Pl Syst Evol 157:219–246

    Article  Google Scholar 

  13. 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

    Article  CAS  Google Scholar 

  14. Gornall RJ (1999) Population genetic structure in agamospermous plants. In: Hollingsworth PM, Bateman RM, Gornall RJ (eds) Molecular systematics and plant evolution. Taylor and Francis, London, pp 118–138

    Google Scholar 

  15. Gottlieb LD (1981) Electrophoretic evidence and plant populations. Progr Phytochem 7:1–46

    CAS  Google Scholar 

  16. Gottlieb LD (1984) Isozyme evidence and problem solving in plant systematics. In: Grant WF (ed) Plant biosystematics. Academic Press, London, pp 343–357

    Google Scholar 

  17. Goudet J (1995) FSTAT: a computer program to calculate F-statistics (version 2.9.3). J Heredity 86:485–486

    Google Scholar 

  18. Greilhuber J, Temsch EM, Loureiro JCM (2007) Nuclear DNA content measurement. In: Doležel J, Greilhuber J, Suda J (eds) Flow cytometry with plant cells. Wiley-VCH, Weinheim, pp 67–101

    Google Scholar 

  19. Greuter W (2006–2009) Compositae (pro parte majore). In: Greuter W, Raab-Straube E von (eds), Compositae. Euro+Med Plantbase—the information resource for Euro-Mediterranean plant diversity. Available at: http://ww2.bgbm.org/EuroPlusMed/

  20. Hardy OJ, Vekemans X (2001) Patterns of allozyme variation in diploid and tetraploid Centaurea jacea at different spatial scales. Evolution 55:943–954

    PubMed  Article  CAS  Google Scholar 

  21. Hörandl E, Greilhuber J, Dobeš C (2000) Isozyme variation within the apomictic Ranunculus auricomus complex: evidence for a sexual progenitor species in southeastern Austria. Pl Biol 2:1–10

    Article  Google Scholar 

  22. Hörandl E, Grossniklaus U, Van Dijk PJ, Sharbel T (eds) (2007) Apomixis: evolution, mechanisms and perspectives. ARG-Gantner, Ruggell, Liechtenstein

    Google Scholar 

  23. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13. v.3.23. Available at http://ibdws.sdsu.edu/

    Google Scholar 

  24. Kaplan Z, Plačková I, Štěpánek J (2002) Potamogeton × fluitans (P. natans × P. lucens) in the Czech Republic. II. Isozyme analysis. Preslia 74:187–195

    Google Scholar 

  25. Kashin AS, Anfalov VE, Demochko YuA (2005) Studying allozyme variation in sexual and apomictic Taraxacum and Pilosella (Asteraceae) populations. Russ J Genet 41:144–154

    Article  CAS  Google Scholar 

  26. Kato T (1987) Hybridization between Dianthus superbus var. longicalycinus and D. shinanensis evidenced by resolvable esterase isozymes from herbarium specimens. Ann Tsukuba Bot Gard 6:9–18

    Google Scholar 

  27. Kirschner J, Štěpánek J, Tichý M, Krahulcová A, Kirschnerová L, Pellar L (1994) Variation in Taraxacum bessarabicum and allied taxa of the section Piesis (Compositae): allozyme diversity, karyotypes and breeding behaviour. Folia Geobot Phytotax 29:61–83

    Article  Google Scholar 

  28. Krahulcová A, Krahulec F (1999) Chromosome numbers and reproductive systems in selected representatives of Hieracium subgen. Pilosella in the Krkonoše Mts (the Sudeten Mts). Preslia 71:217–234

    Google Scholar 

  29. Krahulcová A, Krahulec F, Chapman HM (2000) Variation in Hieracium subgen. Pilosella (Asteraceae): what do we know about its sources? Folia Geobot 35:319–338

    Article  Google Scholar 

  30. Krahulcová A, Rotreklová O, Krahulec F, Rosenbaumová R, Plačková I (2009) Enriching ploidy level diversity: the role of apomictic and sexual biotypes of Hieracium subgen. Pilosella (Asteraceae) that coexist in polyploid populations. Folia Geobot 44:281–306

    Article  Google Scholar 

  31. Krahulec F, Krahulcová A, Fehrer J, Bräutigam S, Plačková I, Chrtek J Jr (2004) The Sudetic group of Hieracium subgen. Pilosella from the Krkonoše Mts: a synthetic view. Preslia 76:223–243

    Google Scholar 

  32. Krahulec F, Krahulcová A, Fehrer J, Bräutigam S, Schuhwerk F (2008) The agamic complex of Hieracium subgen. Pilosella in the Šumava Mts.: its structure and comparison with other regions in Central Europe. Preslia 80:1–26

    Google Scholar 

  33. Křišťálová V, Chrtek J, Krahulcová A, Bräutigam S, Krahulec F (2010) Populations of species of Pilosella in ruderal habitats in the city of Prague: frequency, chromosome numbers and mode of reproduction. Preslia 82:437–464

    Google Scholar 

  34. Liston A, Wilson BL, Doescher PS, Robinson WA, Harris N, Svejcar T (2003) Genetic evidence for sexual and clonal reproduction in a 59-year old population of Festuca idahoensis (Poaceae). Oecologia 137:216–225

    PubMed  Article  CAS  Google Scholar 

  35. Magyari E, Chapman JC, Passmore DG, Allen JRM, Huntley JP, Huntley B (2010) Holocene persistence of wooded steppe in Great Hungarian Plain. J Biogeogr 37:915–935

    Article  Google Scholar 

  36. Mahy G, Bruederle LP, Connors B, Van Hofwegen M, Vorsa N (2000) Allozyme evidence for genetic autopolyploidy and high genetic diversity in tetraploid cranberry, Vaccinium oxycoccos (Ericaceae). Amer J Bot 87:1882–1889

    Article  CAS  Google Scholar 

  37. Mráz P, Chrtek J Jr, Fehrer J, Plačková I (2005) Rare recent natural hybridization in Hieracium s.str.—evidence from morphology, allozymes and chloroplast DNA. Pl Syst Evol 255:177–192

    Article  Google Scholar 

  38. Mráz P, Šingliarová B, Urfus T, Krahulec F (2008) Cytogeography of Pilosella officinarum (Compositae): altitudinal and longitudinal differences in ploidy level distribution in the Czech Republic and Slovakia and the general pattern in Europe. Ann Bot 101:59–71

    PubMed  Article  PubMed Central  Google Scholar 

  39. Nägeli C, Peter A (1885) Die Hieracien Mittel-Europas. Monographische Bearbeitung der Piloselloiden mit mit besonderer Berücksichtigung der mitteleuropäischen Sippen. R. Oldenbourg, München

  40. Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  41. Noyes RD, Soltis DE (1996) Genotypic variation in agamospermous Erigeron compositus (Asteraceae). Amer J Bot 83:1292–1303

    Article  CAS  Google Scholar 

  42. Obbard DJ, Harris SA, Pannell JR (2006) Simple allelic-phenotype diversity and differentiation statistics for allopolyploids. Heredity 97:296–303

    PubMed  Article  CAS  Google Scholar 

  43. Peckert T, Chrtek J Jr, Plačková I (2005) Genetic variation in agamospermous populations of Hieracium echioides in southern Slovakia and northern Hungary (Danube Basin). Preslia 77:307–315

    Google Scholar 

  44. Pielou EC (1969) An introduction to mathematical ecology. Wiley, New York

    Google Scholar 

  45. Podani J (2001) SYN-TAX 2000. Computer programs for data analysis in ecology and systematics. In: User’s manual. Scientia Publishing, Budapest

  46. Richards AJ (1997) Plant breeding systems. Chapman & Hall, London

    Google Scholar 

  47. Roose ML, Gottlieb LD (1976) Genetic and biochemical consequences of polyploidy in Tragopogon. Evolution 30:818–830

    Article  CAS  Google Scholar 

  48. Rosquist G, Prentice HC (2002) Genetic variation in Scandinavian Anthericum liliago (Anthericaceae): allopolyploidy, hybridization and immigration history. Pl Syst Evol 236:55–72

    Article  CAS  Google Scholar 

  49. Rotreklová O, Krahulcová A, Vaňková D, Peckert T, Mráz P (2002) Chromosome numbers and breeding systems in some species of Hieracium subgen. Pilosella from Central Europe. Preslia 74:27–44

    Google Scholar 

  50. Rotreklová O, Krahulcová A, Mráz P, Mrázová V, Mártonfiová L, Peckert T, Šingliarová B (2005) Chromosome numbers and breeding systems in some species of Hieracium subgen. Pilosella from Europe. Preslia 77:177–195

    Google Scholar 

  51. Schuhwerk F, Lippert W (1997) Chromozomenzahlen von Hieracium L. (Compositae, Lactuceae) Teil 1. Sendtnera 4:181–206

    Google Scholar 

  52. Schuhwerk F, Lippert W (2002) Chromosomenzahlen von Hieracium L. (Compositae, Lactuceae). Teil 4. Sendtnera 8:167–194

  53. Šingliarová B, Chrtek J Jr, Mráz P (2008) Loss of genetic diversity in isolated populations of an alpine endemic Pilosella alpicola subsp. ullepitschii: effect of long-term vicariance or long-distance dispersal? Pl Syst Evol 275:181–191

    Article  Google Scholar 

  54. Šingliarová B, Chrtek J, Plačková I, Mráz P (2011) Allozyme variation in diploid, polyploid and mixed-ploidy populations of the Pilosella alpicola group (Asteraceae): relation to morphology, origin of polyploids and breeding system. Folia Geobot 46:387–410

    Article  Google Scholar 

  55. Sipes SD, Wolf PG (1997) Clonal structure and patterns of allozyme diversity in the rare endemic Cycladenia humilis var. jonesii (Apocynaceae). Amer J Bot 84:401–409

    Article  CAS  Google Scholar 

  56. Soltis DE, Rieseberg LH (1986) Autopolyploidy in Tolmiea menziesii (Saxifragaceae): genetic insights from enzyme electrophoresis. Amer J Bot 73:310–318

    Article  CAS  Google Scholar 

  57. Soltis DE, Soltis PS (1989) Genetic consequences of autopolyploidy in Tolmiea (Saxifragaceae). Evolution 43:586–594

    Article  Google Scholar 

  58. Soó R (1970) A magyar flóra és vegetáció rendszertani – növényföldrajzi kézikönyve IV. Akadémiai kiadó, Budapest

    Google Scholar 

  59. Suda J, Krahulcová A, Trávníček P, Rosenbaumová R, Peckert T, Krahulec F (2007) Genome size variation and species relationships in Hieracium sub-genus Pilosella (Asteraceae) as inferred by flow cytometry. Ann Bot 100:1323–1335

    PubMed  Article  PubMed Central  Google Scholar 

  60. Sydes MA, Peakall R (1998) Extensive clonality in the endangered shrub Haloragodendron lucasii (Haloragaceae) revealed by allozymes and RAPDs. Molec Ecol 7:87–93

    Article  Google Scholar 

  61. Tomiuk J, Guldbrandtsen B, Loeschcke V (1998) Population differentiation through mutation and drift—a comparison of genetic identity measures. Genetica 102(103):545–558

    PubMed  Article  Google Scholar 

  62. Tomiuk J, Guldbrandtsen B, Loeschcke V (2009) Genetic similarity of polyploids: a new version of the computer program POPDIST (version 1.2.0) considers intraspecific genetic differentiation. Mol Ecol Res 9:1364–1368

    Article  Google Scholar 

  63. Trávníček P, Dočkalová Z, Rosenbaumová R, Kubátová B, Szeląg Z, Chrtek J (2011) Bridging global and microregional scales: ploidy distribution in Pilosella echioides (Asteraceae) in central Europe. Ann Bot 107:443–454

    PubMed  Article  PubMed Central  Google Scholar 

  64. Tyler T (2005) Patterns of allozyme variation in Nordic Pilosella. Pl Syst Evol 250:133–145

    Article  Google Scholar 

  65. Weeden NF, Wendel JF (1989) Genetics of plant isozymes. In: Soltis P, Soltis D (eds) Isozymes in plant biology. Dioscorides Press, Portland, pp 46–72

    Google Scholar 

  66. Yeh FC, Yang R-C, Boyle T (1999) POPGENE version 1.32. Microsoft Window-based freeware for population genetic analysis. Available at: http://www.ualberta.ca/~fyeh/

  67. Zahn KH (1921–1923) Hieracium. In: Engler A (ed) Das Pflanzenreich 75, 76, 77, 80, 82 (IV/280), Wilhelm Engelmann, Leipzig

  68. Zahn KH (1922–1930) Hieracium. In: Ascherson P, Graebner P (eds) Synopsis der mitteleuropäischen Flora 12(1). Gebrüder Borntraeger, Leipzig

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Acknowledgments

We thank Eva Ibermajerová and Eva Morávková for providing greenhouse and garden support, Karin Kottová and Adéla Macková for carrying out the allozyme analyses and curators of herbarium collection BP (especially to Zoltán Barina) for their help during our herbarium studies. Fred Rooks kindly improved our English. The study was funded by the Academy of Sciences of the Czech Republic (grant No. KJB601110813 and the long-term research development project No. RVO 67985939), the Czech Science Foundation (grants No. P506/10/1363 and 13-18610P), Charles University in Prague (grant No. 1207/2007), the Ministry of Education, Youth and Sports of the Czech Republic (grants No. MSM 0021620828 and MSM 6007665806) and the project Postdoc USB (No. CZ.1.07/2.3.00/30.0006 to PT) realized through the EU Education for Competitiveness Operational Programme (funded by the European Social Fund and the Czech State Budget).

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Chrtek, J., Plačková, I., Dočkalová, Z. et al. Patterns of genetic variation in Pilosella echioides and its selected relatives: results of variation in ploidy level, facultative apomixis and past and present hybridization. Plant Syst Evol 300, 2091–2104 (2014). https://doi.org/10.1007/s00606-014-1041-9

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Keywords

  • Pilosella
  • Allozymes
  • Apomixis
  • Pannonian Basin
  • Genetic variation