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Differentiation in morphology and flowering phenology between two Campanula thyrsoides L. subspecies

Abstract

Subspecies are usually characterised by sets of morphological discontinuities. By means of common garden experiments, we investigated genetic differentiation in morphological and phenological traits in two geographically disjunct subspecies of Campanula thyrsoides L., i.e. subsp. thyrsoides (=C.* thyrsoides) occurring in the European Alps and Jura Mountains, and subsp. carniolica (=C.* carniolica) occurring in the Southeastern Alps and the Dinaric Arc. Nine out of 16 investigated traits were significantly different between C.* thyrsoides and C.* carniolica. For C.* carniolica inflorescence length was 1.4×, and above-ground biomass 2.7× higher, while flower density was significantly lower. Campanula* carniolica also showed delayed flowering and flower development from bottom to top as compared to C.* thyrsoides which flowered from top to bottom. The inflorescence growth was indeterminate and flowering took several weeks in C.* carniolica, whereas C.* thyrsoides showed determinate flowering, rapidly opening all flowers within a few days. This differentiation in flowering phenology is likely to be adaptive. The submediterranean climate favours indeterminate flowering in C.* carniolica, allowing ongoing growth of the inflorescence throughout the long summer until environmental conditions worsen, whereas determinate and early flowering in C.* thyrsoides is favourable in the short growing season in the high Alps where seed production must be secured before temperature drops. Glacial survival in refugia with different climates (alpine vs. submediterranean) may have caused this regional differentiation.

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References

  • Ægisdóttir HH, Kuss P, Stöcklin J (2009) Isolated populations of a rare alpine plant show high genetic diversity and considerable population differentiation. Ann Bot 104:1313–1322

    PubMed  Article  Google Scholar 

  • Aeschimann D, Lauber K, Moser DM, Theurillat J-P (2004) Flora Alpina. Haupt Verlag, Bern

    Google Scholar 

  • Albert CH, Thuiller W, Yoccoz NG, Soudant A, Boucher F, Saccone P, Lavorel S (2010) Intraspecific functional variability: extent, structure and sources of variation. J Ecol 98:604–613

    Article  Google Scholar 

  • Alvarez N, Thiel-Egenter C, Tribsch A, Holderegger R, Manel S, Schönswetter P, Taberlet P, Brodbeck S, Gaudeul M, Gielly L, Kupfer P, Mansion G, Negrini R, Paun O, Pellecchia M, Rioux D, Schupfer F, Van Loo M, Winkler M, Gugerli F, Consortium IntraBioDiv (2009) History or ecology? Substrate type as a major driver of spatial genetic structure in Alpine plants. Ecol Lett 12:632–640

    PubMed  Article  Google Scholar 

  • Clausen J, Keck D, Hiesey WM (1948) Experimental studies on the nature of plant species. III. Environmental responses of climatic races of Achillea. Carnegie Institution of Washington Publication, vol 581, pp 1–129

  • Comes HP, Kadereit JW (2003) Spatial and temporal patterns in the evolution of the flora of the European Alpine System. Taxon 52:451–462

    Article  Google Scholar 

  • Connor JK, Hartl DL (2004) A primer of ecological genetics. Sinauer, Sunderland

    Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland

    Google Scholar 

  • García-Verdugo C, Forrest AD, Balaguer L, Fay MF, Vargas P (2010) Parallel evolution of insular Olea europaea subspecies based on geographical structuring of plastid DNA variation and phenotypic similarity in leaf traits. Bot J Linn Soc 162:54–63

    Article  Google Scholar 

  • Gugerli F, Englisch T, Niklfeld H, Tribsch A, Mirek Z, Ronikier M, Zimmermann NE, Holderegger R, Taberlet P, Consortium IntraBioDiv (2008) Relationships among levels of biodiversity and the relevance of intraspecific diversity in conservation—a project synopsis. Perspect Plant Ecol Evol Syst 10:259–281

    Article  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Jäger EJ (2000) Wuchsform und Lebensgeschichte der Strauß-Glockenblume (Campanula thyrsoides L.) und ihrer subsp. carniolica (Sünderm.) Podl. Ber Bayer Bot Ges 69(70):93–100

    Google Scholar 

  • Jolivet C, Bernasconi G (2007) Molecular and quantitative genetic differentiation in European populations of Silene latifolia (Caryophyllaceae). Ann Bot 100:119–127

    PubMed  Article  Google Scholar 

  • Kudo G (1993) Relationship between flowering time and fruit set of the entomophilous alpine shrub, Rhododendron aureum (Ericaceae), inhabiting snow patches. Am J Bot 80:1300–1304

    Article  Google Scholar 

  • Kuss P, Ægisdóttir HH, Stöcklin J (2007) The biological flora of Central Europe: Campanula thyrsoides L. Perspect Plant Ecol Evol Syst 9:37–51

    Article  Google Scholar 

  • Kuss P, Pluess AR, Ægisdóttir HH, Stöcklin J (2008a) Spatial isolation and genetic differentiation in naturally fragmented plant populations of the Swiss Alps. J Plant Ecol 1:149–159

    Article  Google Scholar 

  • Kuss P, Rees M, Ægisdóttir HH, Ellner SP, Stöcklin J (2008b) Evolutionary demography of long-lived monocarpic perennials: a time-lagged integral projection model. J Ecol 96:821–832

    Article  Google Scholar 

  • McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291

    Article  Google Scholar 

  • Merxmüller H (1952) Untersuchungen zur Sippengliederung und Arealbildung in den Alpen. I. Jahrb Vereins Schutze Alpenpflanz Tiere 17:96–133

    Google Scholar 

  • Merxmüller H (1953) Untersuchungen zur Sippengliederung und Arealbildung in den Alpen. II. Jahrb Vereins Schutze Alpenpflanz Tiere 18:138–158

    Google Scholar 

  • Merxmüller H (1954) Untersuchungen zur Sippengliederung und Arealbildung in den Alpen. III. Jahrb Vereins Schutze Alpenpflanz Tiere 19:97–139

    Google Scholar 

  • Milla R, Escudero A, Iriondo JM (2009) Inherited variability in multiple traits determines fitness in populations of an annual legume from contrasting latitudinal origins. Ann Bot 103:1279–1289

    PubMed  Article  Google Scholar 

  • Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. OIKOS 100:403–405

    Article  Google Scholar 

  • Olsson K, Ågren J (2002) Latitudinal population differentiation in phenology, life history and flower morphology in the perennial herb Lythrum salicaria. J Evol Biol 15:983–996

    Article  Google Scholar 

  • Ouborg NJ, Van Treuren R, Van Damme JMM (1991) The significance of genetic erosion in the process of extinction. II. Morphological variation and fitness components in populations of varying size of Salvia pratensis L. and Scabiosa columbaria L. Oecologia 86:359–367

    Article  Google Scholar 

  • Paun O, Schönswetter P, Winkler M, Consortium Intrabiodiv (2008) Historical divergence vs. contemporary gene flow: Evolutionary history of the calcicole Ranunculus alpestris group (Ranunculaceae) in the European Alps and the Carpathians. Mol Ecol 17:4263–4275

    PubMed  Article  CAS  Google Scholar 

  • Podlech D (1964) Die Krainer Straußglockenblume. Ber Bayer Bot Ges 37:111

    Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  • Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Ann Rev Ecol Syst 16:179–214

    Article  Google Scholar 

  • Rotundo JL, Aguiar MR (2008) Herbivory resistance traits in populations of Poa ligularis subjected to historically different sheep grazing pressure in Patagonia. Plant Ecol 194:121–133

    Article  Google Scholar 

  • Sandring S, Riihimäki M-A, Savolainen O, Ågren J (2007) Selection on flowering time and floral display in an alpine and a lowland population of Arabidopsis lyrata. J Evol Biol 20:558–567

    PubMed  Article  CAS  Google Scholar 

  • Scheepens JF, Frei ES, Stöcklin J (2010) Genotypic and environmental variation in specific leaf area in a widespread Alpine plant after transplantation to different altitudes. Oecologia 164:141–150

    PubMed  Article  CAS  Google Scholar 

  • Schmid B, Dolt C (1994) Effects of maternal and paternal environment and genotype on offspring phenotype in Solidago altissima L. Evolution 48:1525–1549

    Article  Google Scholar 

  • Schönswetter P, Schneeweiss GM (2009) Androsace komovensis sp. nov., a long mistaken local endemic from the southern Balkan Peninsula with biogeographic links to the Eastern Alps. Taxon 58:544–549

    Google Scholar 

  • Schönswetter P, Stehlik I, Holderegger R, Tribsch A (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol 14:3547–3555

    PubMed  Article  Google Scholar 

  • Stöcklin J, Kuss P, Pluess AR (2009) Genetic diversity, phenotypic variation and local adaptation in the alpine landscape: case studies with alpine plant species. Bot Helv 119:125–133

    Article  Google Scholar 

  • Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185

    PubMed  Article  Google Scholar 

  • Stuessy TF (1990) Plant taxonomy: the systematic evaluation of comparative data. Columbia University Press, New York

    Google Scholar 

  • Sultan S (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–542

    PubMed  Article  CAS  Google Scholar 

  • Sündermann E (1925) Eine interessante Form von Campanula thyrsoidea L. Allgem Bot Z 26(27):23–24

    Google Scholar 

  • Suzuki RO (2008) Dwarf morphology of the annual plant Persicaria longiseta as a local adaptation to a grazed habitat, Nara Park, Japan. Plant Spec Biol 23:174–182

    Article  Google Scholar 

  • Tackenberg O, Stöcklin J (2008) Wind dispersal of alpine plant species: a comparison with lowland species. J Veg Sci 19:109–118

    Article  Google Scholar 

  • Tackenberg O, Poschlod P, Bonn S (2003) Assessment of wind dispersal potential in plant species. Ecol Monogr 73:191–205

    Article  Google Scholar 

  • Thiel-Egenter C, Holderegger R, Brodbeck S, Gugerli F (2009) Concordant genetic breaks, identified by combining clustering and tessellation methods, in two co-distributed alpine plant species. Mol Ecol 18:4495–4507

    PubMed  Article  CAS  Google Scholar 

  • Tomažič G (1941) Senozeti in pasniki na plitvih in suhih tleh Slovenije. Zbornik Prirodoslovnega drustva 2:76–82

    Google Scholar 

  • Tribsch A, Schönswetter P (2003) Patterns of endemism and comparative phylogeography confirm palaeoenvironmental evidence for Pleistocene refugia in the Eastern Alps. Taxon 52:477–497

    Article  Google Scholar 

  • Weber E, Schmid B (1998) Latitudinal population differentiation in two species of Solidago Asteraceae) introduced into Europe. Am J Bot 85:1110–1121

    Article  Google Scholar 

  • Welter SC, Steggal JW (1993) Contrasting the tolerance of wild and domesticated tomatoes to herbivory: agroecological implications. Ecol Appl 3:271–278

    Article  Google Scholar 

  • Westberg E, Poppendieck HH, Kadereit JW (2010) Ecological differentiation and reproductive isolation of two closely related sympatric species of Oenanthe (Apiaceae). Biol J Linn Soc 101:526–535

    Article  Google Scholar 

  • Winkler M, Tribsch A, Paun O, Englisch T, Schönswetter P (2010) Pleistocene distribution range shifts were accompanied by breeding system divergence within Hornungia alpina (Brassicaceae) in the Alps. Mol Phylogenet Evol 54:571–582

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Serge Aubert for helping us collecting plant material in the western Alps, Guy Villaume for practical assistence in the common gardens on Mt. Calanda, Thomas Fabbro and Beatrice Krummen for gathering data from natural populations, Gemeinde Haldenstein and the CCES BioChange project of the ETH Zürich providing access to field sites on Mt. Calanda, and Kai and Christine Huovinen for the experimental site in Davos. This study has been supported financially by the Swiss National Science Foundation, project no. 3100AO-116785 to Jürg Stöcklin.

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Correspondence to J. F. Scheepens.

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Responsible editor: Christian Parisod.

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Scheepens, J.F., Kuss, P. & Stöcklin, J. Differentiation in morphology and flowering phenology between two Campanula thyrsoides L. subspecies. Alp Botany 121, 37–47 (2011). https://doi.org/10.1007/s00035-011-0087-3

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  • DOI: https://doi.org/10.1007/s00035-011-0087-3

Keywords

  • Campanula thyrsoides subsp. carniolica
  • Common garden
  • Determinate flowering
  • European Alps
  • Glacial history