Alpine Botany

, Volume 121, Issue 1, pp 23–35 | Cite as

The stability of Quaternary speciation: a case study in Primula sect. Auricula

  • J. W. Kadereit
  • H. Goldner
  • N. Holstein
  • G. Schorr
  • L.-B. Zhang
Original Paper


Primula sect. Auricula, a group of 25 species distributed in the European Alpine System, has been hypothesised to have diversified in the Quaternary through speciation in geographically isolated glacial refugia. We here examine whether the integrity of species is endangered through hybridisation upon contact in the Holocene. To do this, we (1) critically screened the literature for reported hybrids and supplemented this with our own knowledge of the group, (2) performed an admixture analysis of AFLP variation of two partly sympatric species pairs, P. hirsuta/P. daonensis and P. latifolia/P. marginata, and (3) analysed long-known hybrid populations of P. lutea × P. hirsuta in Wipptal/Austria to identify possible mechanisms of reproductive isolation. The literature survey revealed that populations of the 32 hybrid combinations known have been observed at 63 localities. In the admixture analysis, two admixed individuals per species were found among 524 individuals of P. latifolia and P. marginata, and 21 admixed individuals were found among 234 individuals of P. hirsuta. The analysis of P. lutea × P. hirsuta hybrids revealed that they show reduced pollen and seed fertility, and are limited to soils with intermediate pH values. We conclude that although species of P. sect. Auricula can readily be hybridised experimentally, hybridisation is rare in nature and species are stable. Mechanisms of reproductive isolation include geographical and ecogeographical isolation, ecological hybrid inviability and reduced hybrid fertility.


Admixture AFLPs Edaphic differentiation Hybrid fitness Quaternary refugia Reproductive isolation 


  1. Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New YorkGoogle Scholar
  2. Bell CD, Donoghue MJ (2005) Dating the Dipsacales: comparing models, genes, and evolutionary implications. Am J Bot 92:284–296CrossRefGoogle Scholar
  3. Brochmann C, Brysting AK (2008) The Arctic: an evolutionary freezer? Pl Ecol Div 1:181–195CrossRefGoogle Scholar
  4. Choler P, Erschbamer B, Tribsch A, Gielly L, Taberlet P (2004) Genetic introgression as a potential to widen a species’ niche: Insights from alpine Carex curvula. Proc Nat Acad Science USA 101:171–176CrossRefGoogle Scholar
  5. Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843PubMedCrossRefGoogle Scholar
  6. Corander J, Marttinen P, Siren J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinform 9:539CrossRefGoogle Scholar
  7. Ellstrand NC (1992) Gene flow among seed plant populations. New For 6:241–256CrossRefGoogle Scholar
  8. Emde K, Szöcs A (2001) Geomorphologisch-bodenkundliches und gewässerökologisches Laborpraktikum – Eine praxisorientierte Anleitung zur physikalischen und chemischen Boden- und Gewässeruntersuchung. Geographisches Institut, MainzGoogle Scholar
  9. Ernst A, Moser F (1925) Enstehung, Erscheinungsform und Fortpflanzung des Artbastardes Primula pubescens Jacq. Archiv der Julius-Klaus-Stiftung für Vererbungsforschung, Sozialanthropologie und Rassenhygiene, Zürich 1:273–453Google Scholar
  10. Gahan PB, Kalina M (1968) The use of tetrazolium salts in the histochemical demonstration of succinic dehydrogenase activity in plant tissues. Histochem Cell Biol 14:81–88Google Scholar
  11. Gower JC (1966) Some distance properties of latent root and vector models used in multivariate analysis. Biometrika 53:325–338Google Scholar
  12. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9Google Scholar
  13. Hansen KT, Elven R, Brochmann C (1999) Molecules and morphology in concert: tests of some hypotheses in arctic Potentilla (Rosaceae). Am J Bot 87:1466–1479CrossRefGoogle Scholar
  14. Harper JL, Clatworthy JN, McNaughton IH, Sager GR (1961) The evolution and ecology of species living in the same area. Evolution 15:209–227CrossRefGoogle Scholar
  15. Hegi G (1927) Illustrierte Flora von Mitteleuropa, Bd. V/3. J.F. Lehmanns Verlag, MünchenGoogle Scholar
  16. Hess HE, Landolt E, Hirzel R (1970) Flora der Schweiz und angrenzender Gebiete, Bd. 2. Birkhäuser, Basel und StuttgartGoogle Scholar
  17. Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568PubMedCrossRefGoogle Scholar
  18. Ho SYW, Shapiro B, Phillips MJ, Cooper A, Drummond AJ (2007) Evidence for time dependency of molecular rate estimates. Syst Biol 56:515–522PubMedCrossRefGoogle Scholar
  19. Horne EC, Kumpatla SP, Patterson KA, Gupta M, Thompson SA (2004) Improved high-throughput sunflower and cotton genomic DNA extraction and PCR fidelity. Pl Mol Biol Rep 22:83a–83iGoogle Scholar
  20. Huter R (1873) Botanische Mittheilungen. Österr Bot Z 23:121–127Google Scholar
  21. Jacquin NJ (1778) Miscellanea Austriaca. Ex Officina Krausiana, Vindobonae (Wien)Google Scholar
  22. Kadereit JW, Griebeler EM, Comes HP (2004) Quaternary diversification in European alpine plants—pattern and process. Phil Trans R Soc Lond B 359:265–274CrossRefGoogle Scholar
  23. Kerner von Marilaun A (1875) Die Primulaceen-Bastarde der Alpen. Österr Bot Z 25:153–164CrossRefGoogle Scholar
  24. Kreß A (1973) Über Primula-villosa-pedemontana-Hybriden und ihre Stammsippen. Ber Bayer Bot Ges Erforsch Heim Flora 44:197–200Google Scholar
  25. Kreß A (1981) Primulaceen-Studien 2: Primula sectio Auricula subsect. Erythrodrosum: Neue Unterarten und Hybriden. Gröbenzell bei MünchenGoogle Scholar
  26. Kreß A (1998) Die Aurikeln, eine Gruppe europäischer, gebirgsbewohnender Primeln. In: Jung WW (ed.). Naturerlebnis Alpen. Jubiläumsschrift zum 50-jährigen Bestehen der Naturkundlichen Abteilung der Sektion München im Deutschen Alpenverein e.V. Dr. Friedrich Pfeil, München, pp 49–65Google Scholar
  27. Kropf M, Kadereit JW, Comes HP (2003) Differential cycles of range contraction and expansion in European high mountain plants during the Late Quaternary: insights from Pritzelago alpina (L.) O. Kuntze (Brassicaceae). Mol Ecol 12:931–949PubMedCrossRefGoogle Scholar
  28. Lehmann JGC (1817) Monographia Generis Primularum. Barth, Lipsiae (Leipzig)Google Scholar
  29. Levin DA (2000) The origin, expansion and demise of plant species. Oxford University Press, New YorkGoogle Scholar
  30. Levin DA, Francisco-Ortega J, Jansen RK (1996) Hybridization and the extinction of rare plant species. Conserv Biol 10:10–16CrossRefGoogle Scholar
  31. Lexer C, Kremer A, Petit RJ (2006) Shared alleles in sympatric oaks: recurrent gene flow is a more parsimonious explanation then ancestral polymorphism. Mol Ecol 15:2007–2012PubMedCrossRefGoogle Scholar
  32. Leybold F (1855) Stirpium in alpibus orientali-australibus nuperrime repertatum nonullarumque no satis adhuc expositarum Icones quibus brevem ex recentissimis observatioibus derivatam adjunxit. Flora 22:337–349Google Scholar
  33. Lowry DB, Modliszewski JL, Wright KM, Wu CA, Willis JH (2008) The strength and genetic basis of reproductive isolating barriers in flowering plants. Phil Trans R Soc B 363:3009–3021PubMedCrossRefGoogle Scholar
  34. Lüdi W (1927) Primulaceae. In: Hegi G (ed) Illustrierte Flora von Mitteleuropa. Verlag von JF Lehmanns, München, pp 1715–1877Google Scholar
  35. Magallón SA, Sanderson MJ (2005) Angiosperm divergence times: the effect of genes, codon positions, and time constraints. Evolution 59:1653–1670PubMedCrossRefGoogle Scholar
  36. Mast AR, Kelso S, Conti E (2006) Are any primroses (Primula) primitively monomorphic? New Phytol 171:605–616PubMedCrossRefGoogle Scholar
  37. Milne RI, Abbott RJ (2008) Reproductive isolation among two interfertile Rhododendron species: low frequency of post-F1 hybrid genotypes in alpine hybrid zones. Mol Ecol 17:1108–1121PubMedCrossRefGoogle Scholar
  38. Moser DM (1998) Ein neuer Reliktendemit der Grigna Meridionale, Provincia di Como, Italien: Primula grignensis D. M. Moser (sect. Auricula, subsect. Erythrodrosum Schott). Candollea 53:387–393Google Scholar
  39. Moser DM (1999) Merkblätter Artenschutz—Blütenpflanzen und Farne. Primula daonensis, S. 234-235. BUWAL, BernGoogle Scholar
  40. Neilreich A (1859) Flora von Nieder-Oesterreich. WienGoogle Scholar
  41. Nosil P, Vines TH, Funk DJ (2005) Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719PubMedGoogle Scholar
  42. Pax F (1889) Monographische Übersicht über die Arten der Gattung Primula. Bot Jahrb Syst 10:75–241Google Scholar
  43. Pax F, Knuth R (1905) Primulaceae. In: Engler A (ed) Das Pflanzenreich. W Engelmann, LeipzigGoogle Scholar
  44. Pigniatti S (1982) Flora d’Italia, vol 2. EdagricoleGoogle Scholar
  45. Prosser F (2000) La distribuzione delle entità endemiche strette in Trentino alla luce delle più recenti esplorazioni floristiche. Annali dei Musei Civici di Rovereto, Sezione: Archeologia, Storia. Scienze Naturali suppl 14:31–64Google Scholar
  46. Prosser F, Scrotegagna S (1998) Primula recubariensis, a new species of Primula sect. Auricula Duby endemic to the SE Prealps, Italy. Willdenowia 28:27–45Google Scholar
  47. Pulquério MJF, Nichols RA (2007) Dates from molecular clocks: how wrong can we be? Trends Ecol Evol 22:180–184PubMedCrossRefGoogle Scholar
  48. Reichenbach HGL (1830) Flora Germanica Excursoria. Carl Cnobloch, Lipsiae (Leipzig)Google Scholar
  49. Reichenbach HGL (1855) Icones Florae Germanicae et Helveticae. Apud Fridericum Hofmeister, Lipsiae (Leipzig)Google Scholar
  50. Renner SS (2005) Relaxed molecular clocks for dating historical plant dispersal events. Trends Plant Sci 10:550–558PubMedCrossRefGoogle Scholar
  51. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Ann Rev Ecol Syst 27:83–109CrossRefGoogle Scholar
  52. Richards AJ (1993) Primula. Timber Press, Portland, OregonGoogle Scholar
  53. Richardson JE, Weitz FM, Fay MF, Cronk QCB, Linder HP, Reeves G, Chase MW (2001) Rapid and recent origin of species richness in the Cape flora of South Africa. Nature 412:181–1383PubMedCrossRefGoogle Scholar
  54. Richardson JE, Pennington RT, Pennington TD, Hollingsworth PM (2004) Rapid diversification of a species-rich genus of neotropical rain forest trees. Science 293:2241–2245Google Scholar
  55. Rieseberg LH (1991) Hybridization in rare plants: insights from case studies in Cerocarpus and Helianthus. In: Falk DA, Holsinger KE (eds) Genetics and conservation of rare plants. Oxford University Press, New York, pp 171–181Google Scholar
  56. Rieseberg LH, Wood TE, Baack EJ (2006) The nature of plant species. Nature 440:524–527PubMedCrossRefGoogle Scholar
  57. Rodriguez-Riano T, Dafni A (2000) A new procedure to assess pollen viability. Sex Plant Reprod 12:241–244CrossRefGoogle Scholar
  58. Rull V (2008) Speciation timing and neotropical diversity: the Tertiary–Quaternary debate in the light of molecular phylogenetic evidence. Mol Ecol 17:2722–2729PubMedCrossRefGoogle Scholar
  59. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, New YorkGoogle Scholar
  60. Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380PubMedCrossRefGoogle Scholar
  61. Schorr G (2009) Rekonstruktion der eiszeitlichen Verbreitung und Artbildung vier alpiner Primeln durch Artenverbreitungsmodelle und Phylogeographie. PhD dissertation, MainzGoogle Scholar
  62. Schott HW (1852) Wilde Blendlinge bei österreichischen Primeln. WienGoogle Scholar
  63. Seehausen O (2006) Conservation: losing biodiversity by reverse speciation. Curr Biol 16:334–337CrossRefGoogle Scholar
  64. Seehausen O, Takimoto G, Roy D, Jokela J (2008) Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol Ecol 17:30–44PubMedCrossRefGoogle Scholar
  65. von Hagen KB, Kadereit JW (2001) The phylogeny of Gentianella (Gentianaceae) and its rapid colonization of the southern hemisphere as revealed by nuclear and chloroplast DNA sequence variation. Org Divers Evol 1:61–79CrossRefGoogle Scholar
  66. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414PubMedCrossRefGoogle Scholar
  67. Widmer E (1891) Die europäischen Arten der Gattung Primula. Druck und Verlag von R Oldenbourg, MünchenGoogle Scholar
  68. Willis KJ, Niklas KJ (2004) The role of Quaternary environmental change in plant macroevolution: the exception or the rule? Phil Trans R Soc Lond B 359:159–172CrossRefGoogle Scholar
  69. Zhang L-B, Kadereit JW (2004) Classification of Primula L sect. Auricula Duby (Primulaceae) based on two molecular data sets (ITS, AFLPs) and morphology. Bot J Linn Soc 146:1–26CrossRefGoogle Scholar
  70. Zhang L-B, Kadereit JW (2005) Typification and synonymization in Primula L sect. Auricula Duby (Primulaceae). Taxon 54:775–788CrossRefGoogle Scholar
  71. Zhang L-B, Comes HP, Kadereit JW (2004) The temporal course of Quaternary speciation in the European high mountain endemic Primula sect Auricula (Primulaceae). Int J Plant Sci 165:191–207CrossRefGoogle Scholar
  72. Zhang M-L, Uhink C, Kadereit JW (2007) The Phylogeny and biogeography of Epimedium/Vancouveria (Berberidaceae): Western North American–East Asian disjunctions, the origin of European mountain plant taxa and East Asian specific diversity. Syst Bot 32:81–92CrossRefGoogle Scholar

Copyright information

© Swiss Botanical Society 2011

Authors and Affiliations

  • J. W. Kadereit
    • 1
  • H. Goldner
    • 2
  • N. Holstein
    • 3
  • G. Schorr
    • 1
  • L.-B. Zhang
    • 4
    • 5
  1. 1.Institut für Spezielle Botanik und Botanischer GartenJohannes Gutenberg-Universität MainzMainzGermany
  2. 2.Gries am BrennerAustria
  3. 3.Department Biologie I, Systematische BotanikLudwig-Maximilians-Universität MünchenMunichGermany
  4. 4.Chengdu Institute of BiologyChinese Academy of SciencesChengduChina
  5. 5.Missouri Botanical GardenSt. LouisUSA

Personalised recommendations