Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Genotypic and environmental variation in specific leaf area in a widespread Alpine plant after transplantation to different altitudes

  • 1435 Accesses

  • 89 Citations

Abstract

Specific leaf area (SLA) is an important plant functional trait as it is an indicator of ecophysiological characteristics like relative growth rate, stress tolerance and leaf longevity. Substantial intraspecific variation in SLA is common and usually correlates with environmental conditions. For instance, SLA decreases with increasing altitude, which is understood as adjustment to temperature. It is generally assumed that intraspecific variation is mostly the result of environmentally induced phenotypic plasticity, but genetic effects may also be present, due to local adaptation or genetic drift. In this study, genotypic and environmental effects on SLA were experimentally separated for the widespread Alpine bell flower Campanula thyrsoides by transplanting plants to three common gardens at contrasting altitudes (600, 1,235 and 1,850 m a.s.l.). Seeds were sampled from 18 populations in four phylogeographic regions within the European Alps. A strong plastic response was observed: SLA decreased with increasing altitude of the common gardens (22.0% of variation). The phylogeographic regions were differentiated in SLA in the common gardens (10.1% of variation), indicating that SLA is at least partly genetically determined. Plants from the six easternmost populations experienced a submediterranean climate and showed decreased SLA values in the three common gardens compared to populations to the west, which may be explained as adaptation to drought. Within these submediterranean populations, SLA decreased with altitude of origin in two out of three common gardens. Concluding, SLA shows strong phenotypic plasticity as well as substantial genetic effects, the latter probably being the result of adaptation to local conditions rather than genetic drift.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. 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

  2. Atkin OK, Loveys BR, Atkinson LJ, Pons TL (2006) Phenotypic plasticity and growth temperature: understanding interspecific variability. J Exp Bot 57:267–281

  3. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155

  4. Bradshaw AD (1984) Ecological significance of genetic variation between populations. In: Dirzo R, Sarukhán J (eds) Perspectives on plant population ecology. Sinauer, Sunderland, pp 213–228

  5. Brunies SE (1906) Die Flora des Ofengebietes. Fiebig, Chur

  6. Clausen J, Keck D, Hiesey WM (1940) Experimental studies on the nature of plant species. I. Effect of varied environment on western North American plants. Carnegie Institution, Washington D.C.

  7. Cordell S, Goldstein G, Mueller-Dombois D, Webb D, Vitousek PM (1998) Physiological and morphological variation in Metrosideros polymorpha, a dominant Hawaiian tree species, along an altitudinal gradient: the role of phenotypic plasticity. Oecologia 113:188–196

  8. Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557

  9. Díaz S, Cabido M, Casanoves F (1998) Plant functional traits and environmental filters at a regional scale. J Veg Sci 9:113–122

  10. Díaz S, Hodgson JG, Thompson K, Cabido M, Cornelissen JHC, Jalili A, Montserrat-Martí G, Grime JP, Zarrinkamar F, Asri Y, Band SR, Basconcelo S, Castro-Díez P, Funes G, Hamzehee B, Khoshnevi M, Pérez-Harguindeguy N, Pérez-Rontomé MC, Shirvany FA, Vendramini F, Yazdani S, Abbas-Azimi R, Bogaard A, Boustani S, Charles M, Dehghan M, de Torres-Espuny L, Falczuk V, Guerrero-Campo J, Hynd A, Jones G, Kowsary E, Kazemi-Saeed F, Maestro-Martínez M, Romo-Díez A, Shaw S, Siavash B, Villar-Salvador P, Zak MR (2004) The plant traits that drive ecosystems: evidence from three continents. J Veg Sci 15:295–304

  11. Ennos RA (2001) Inferences about spatial patterns in plant populations from the analysis of molecular markers. In: Silvertown J, Antonovics J (eds) Integrating ecology and evolution in a spatial context. Blackwell Science, London, pp 45–71

  12. Fernández RJ, Wang M, Reynolds JF (2002) Do morphological changes mediate plant responses to water stress? A steady-state experiment with two C4 grasses. New Phytol 155:79–88

  13. Galen C, Shore JS, Deyoe H (1991) Ecotypic divergence in alpine Polemonium viscosum: genetic structure, quantitative variation, and local adaptation. Evolution 45:1218–1228

  14. Galmés J, Cifre J, Medrano H, Flexas J (2005) Modulation of relative growth rate and its conmponents by water stress in Mediterranean species with different growth forms. Oecologia 145:21–31

  15. Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1195

  16. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

  17. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

  18. Jump AS, Peñuelas J (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett 8:1010–1020

  19. Jurik TW (1986) Temporal and spatial patterns of specific leaf weight in successional northern hardwood tree species. Am J Bot 73:1083–1092

  20. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

  21. Körner C (2003) Alpine plant life, 2nd edn. Springer, Heidelberg

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

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

  24. Larcher W (2003) Physiological plant ecology, 4th edn. Springer, Heidelberg

  25. Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct Ecol 16:545–556

  26. Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277

  27. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

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

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

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

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

  32. Milla R, Giménez-Benavides L, Escudero A, Reich PB (2009) Intra- and interspecific performance in growth and reproduction increase with altitude: a case study with two Saxifraga species from northern Spain. Funct Ecol 23:111–118

  33. Monty A, Mahy G (2009) Clinal differentiation during invasion: Senecio inaequidens (Asteraceae) along altitudinal gradients in Europe. Oecologia 159:305–315

  34. Morecroft MD, Woodward FI (1996) Experiments on the causes of altitudinal differences in the leaf nutrient contents, size and δ13C of Alchemilla alpina. New Phytol 134:471–479

  35. Niinemets Ü (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82:453–469

  36. Ozenda P (1988) Die Vegetation der Alpen im Europäischen Gebirgsraum. Fischer, Stuttgart

  37. Petit C, Fréville H, Mignot A, Colas B, Riba M, Imbert E, Hurtrez-Boussés S, Virevaire M, Olivieri I (2001) Gene flow and local adaptation in two endemic plant species. Biol Conserv 100:21–34

  38. Pigliucci M, Pollard H, Cruzan MB (2003) Comparative studies of evolutionary responses to light environments in Arabidopsis. Am Nat 161:68–82

  39. Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588

  40. Price TD, Qvarnström A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc Royal Soc Lond Ser B 270:1433–1440

  41. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  42. Rawson HM, Gardner PA, Long MJ (1987) Sources of variation in specific leaf area in wheat grown at high temperature. Aust J Plant Physiol 14:287–298

  43. Roach DA, Wulff RD (1987) Maternal effects in plants. Annu Rev Ecol Syst 18:209–235

  44. Rogers AR (1986) Population differences in quantitative characters as opposed to gene frequencies. Am Nat 127:729–730

  45. SAS Institute (2003) JMP version 5.0.1.2. SAS, Cary

  46. Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annu Rev Ecol Syst 17:667–694

  47. 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

  48. Sims DA, Pearcy RW (1992) Response of leaf anatomy and photosynthetic capacity in Alocasia macrorrhiza (Araceae) to a transfer from low to high light. Am J Bot 79:449–455

  49. Spitze K (1993) Population structure in Daphnia obtusa: quantitative genetic and allozyme variation. Genetics 135:367–374

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

  51. Turesson G (1922) The genotypical response of the plant species to habitat. Hereditas 3:211–350

  52. Waldmann P, Andersson S (1998) Comparison of quantitative genetic variation and allozyme diversity within and between populations of Scabiosa canescens and S. columbaria. Heredity 81:79–86

  53. Weiher E, Keddy PA (1999) Assembly rules as general constraints on community composition. In: Weiher E, Keddy PA (eds) Ecological assembly rules: perspectives, advances, retreats. Cambridge University Press, Cambridge, pp 251–271

  54. Weiher E, Van der Werf A, Thompson K, Roderick M, Garnier E, Eriksson O (1999) Challenging Theophrastus: a common core list of plant traits for functional ecology. J Veg Sci 10:609–620

  55. Westoby M, Wright IJ (2006) Land plant ecology on the basis of functional traits. Trends Ecol Evol 21:261–268

  56. Woodward FI (1983) The significance of interspecific differences in specific leaf area to the growth of selected herbaceous species from different altitudes. New Phytol 95:313–323

  57. Wright IJ, Westoby M (2002) Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytol 155:403–416

  58. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827

Download references

Acknowledgments

We are grateful to Serge Aubert, director of the Station Alpine Joseph Fourier (Jardin Botanique Alpin du Lautaret), for his help in collecting plant material in the western Alps, to Guy Villaume, Olivier Bignucolo and Lucienne de Witte for help in the field, to Christine Arnold and Stephan Burkhard for weighing the leaf material, to Jens Paulsen for help with obtaining climate data and to Gemeinde Haldenstein and the CCES BioChange project of the ETH Zürich for enabling the use of field sites at Mt. Calanda. We thank Reinout Havinga, Martijn Herber, Rubén Milla and an anonymous reviewer for constructive comments on previous versions of the manuscript. This study has been supported financially by the Swiss National Science Foundation, project no. 3100AO-116785 to Jürg Stöcklin. The experiment in this study complies with the current laws of the country in which they were performed.

Author information

Correspondence to J. F. Scheepens.

Additional information

Communicated by Meelis Partel.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Scheepens, J.F., Frei, E.S. & Stöcklin, J. Genotypic and environmental variation in specific leaf area in a widespread Alpine plant after transplantation to different altitudes. Oecologia 164, 141–150 (2010). https://doi.org/10.1007/s00442-010-1650-0

Download citation

Keywords

  • Altitude of origin
  • Campanula thyrsoides
  • Genetic effect
  • Local adaptation
  • Phenotypic plasticity