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Evolutionary Ecology

, Volume 22, Issue 3, pp 383–397 | Cite as

Variation in petiole and internode length affects plant performance in Trifolium repens under opposing selection regimes

  • Jelmer Weijschedé
  • Rick Berentsen
  • Hans de Kroon
  • Heidrun Huber
Original Paper

Abstract

We studied the effects of genotypic and plastic variation in vertical and horizontal spacer lengths on plant performance in a stoloniferous herb subjected to opposing selection regimes. We hypothesized that longer vertical structures are beneficial if plants are subjected to competition, but they should negatively affect plant performance if plants are exposed to aboveground disturbance. To test these hypotheses we subjected 34 genotypes of Trifolium repens to competition and disturbance treatments. Competition was imposed by a grass canopy consisting of Lolium perenne, and disturbance was simulated by regularly clipping the target plants and all the surrounding vegetation at 1 cm above soil level. Conform to our hypothesis, genotypes with longer vertical structures (petioles) produced fewer ramets than genotypes with shorter petioles in the disturbance treatment. However, genotypes with longer petioles did not perform better under competition than genotypes with shorter petioles. Genotypes with highly plastic vertical structures tended to produce more shoot mass under competition, and they produced fewer ramets if subjected to disturbance. Unexpectedly, horizontal structures (stolon internodes) expanded in response to competition which, furthermore, was associated with enhanced plant performance. However, producing longer internodes is inherently associated with costs in terms of increased resource allocation to the longer structures, but not to benefits in terms of increased resource capture. Positive correlations among the length and plasticity of vertical and horizontal structures may explain the apparent positive effect of producing longer internodes on plant performance. Our data thus support the notion that trait correlations may weaken selective forces acting on a focal trait in a specific environment if opposing selection pressures act on genetically correlated traits.

Keywords

Competition Disturbance Shade avoidance Phenotypic plasticity Vertical and horizontal spacers 

Notes

Acknowledgements

We are grateful to J. F. Cahill for his valuable statistical ideas and to E. J. von Wettberg for his helpful conceptual discussions. This manuscript has been greatly improved by the helpful comments made by two anonymous referees.

References

  1. Anten NPR, Casado-Garcia R, Nagashima H (2005) Effects of mechanical stress and plant density on mechanical characteristics, growth, and lifetime reproduction of tobacco plants, Am Nat 166:650–660PubMedCrossRefGoogle Scholar
  2. Aphalo PJ, Ballare CL (1995) On the importance of information-acquiring systems in plant-plant interactions. Funct Ecol 9:5–14CrossRefGoogle Scholar
  3. Ballare CL, Scopel AL, Sanchez RA (1991) Photocontrol of stem elongation in plant neighborhoods—effects of photon fluence rate under natural conditions of radiation. Plant Cell Environ 14:57–65CrossRefGoogle Scholar
  4. Ballare CL, Scopel AL, Jordan ET, Vierstra RD (1994) Signaling among neighboring plants and the development of size inequalities in plant-populations. Proc Natl Acad Sci USA 91:10094–10098PubMedCrossRefGoogle Scholar
  5. Cain ML (1994) Consequences of foraging in clonal plant species. Ecology 75:933–944CrossRefGoogle Scholar
  6. Cahill JF (2002) Interactions between root and shoot competition vary among species. Oikos 99:101–112CrossRefGoogle Scholar
  7. Cahill JF (2003) Lack of relationship between below-ground competition and allocation to roots in 10 grassland species. J Ecol 91:532–540CrossRefGoogle Scholar
  8. Callahan HS, Pigliucci M (2002) Shade-induced plasticity and its ecological significance in wild populations of Arabidopsis thaliana. Ecology 83:1965–1980Google Scholar
  9. de Kroon H, Hutchings MJ (1995) Morphological plasticity in clonal plants—the foraging concept reconsidered. J Ecol 83:143–152CrossRefGoogle Scholar
  10. DeWitt TJ, Sih A,Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81CrossRefGoogle Scholar
  11. Donohue K, Messiqua D, Pyle EH, Heschel MS, Schmitt J (2000) Evidence of adaptive divergence in plasticity: density- and site-dependent selection on shade-avoidance responses in Impatiens capensis. Evolution 54:1956–1968PubMedGoogle Scholar
  12. Dorn LA, Pyle EH, Schmitt J (2000) Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs. Evolution 54:1982–1994PubMedGoogle Scholar
  13. Dudley SA, Schmitt J (1996) Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. Am Nat 147:445–465CrossRefGoogle Scholar
  14. Evans RC, Turkington R (1988) Maintenance of morphological variation in a biotically patchy environment. New Phytol 109:369–376CrossRefGoogle Scholar
  15. Farley RA, Fitter AH (1999) Temporal and spatial variation in soil resources in a deciduous woodland. J Ecol 87:688–696CrossRefGoogle Scholar
  16. Galloway LF (1995) Response to natural environmental heterogeneity: maternal effects and selection on life-history characters and plasticities in Mimulus guttatus. Evolution 49:1095–1107CrossRefGoogle Scholar
  17. Garland T, Kelly SA (2006) Phenotypic plasticity and experimental evolution. J Exp Biol 209:2344–2361PubMedCrossRefGoogle Scholar
  18. Gautier H, Varlet-Grancher C, Baudry N (1998) Comparison of horizontal spread of white clover (Trifolium repens L.) grown under two artificial light sources differing in their content of blue light. Ann Bot 82:41–48CrossRefGoogle Scholar
  19. Geber MA, Griffen LR (2003) Inheritance and natural selection on functional traits. Int J Plant Sci 164:S21–S42CrossRefGoogle Scholar
  20. Griffith TM, Sultan SE (2006) Plastic and constant developmental traits contribute to adaptive differences in co-occurring Polygonum species. Oikos 114:5–14CrossRefGoogle Scholar
  21. Hirose T, Werger MJA (1995) Canopy structure and photon flux partitioning among species in a herbaceous plant community. Ecology 76:466–474CrossRefGoogle Scholar
  22. Huber H, Hutchings MJ (1997) Differential response to shading in orthotropic and plagiotropic shoots of the clonal herb Glechoma hirsuta. Oecologia 112:485–491CrossRefGoogle Scholar
  23. Huber H, Fijan A, During HJ (1998) A comparative study of spacer plasticity in erect and stoloniferous herbs. Oikos 81:576–586CrossRefGoogle Scholar
  24. Huber H, Kane NC, Heschel MS, von Wettberg EJ, Banta J, Leuck AM, Schmitt J (2004) Frequency and microenvironmental pattern of selection on plastic shade-avoidance traits in a natural population of Impatiens capensis. Am Nat 163:548–563PubMedCrossRefGoogle Scholar
  25. Hutchings MJ, Turkington R, Carey P, Klein E (1997) Morphological plasticity in Trifolium repens L.: the effects of clone genotype, soil nutrient level, and the genotype of conspecific neighbours. Can J Bot-Revue Canadienne de Botanique 75:1382–1393Google Scholar
  26. Jackson RB, Caldwell MM (1993) Geostatistical patterns of soil heterogeneity around individual perennial plants. J Ecol 81:683–692CrossRefGoogle Scholar
  27. Kleijn D, van Groenendael JM (1999) The exploitation of heterogeneity by a clonal plant in habitats with contrasting productivity levels. J Ecol 87:873–884CrossRefGoogle Scholar
  28. Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226CrossRefGoogle Scholar
  29. Leeflang L (1999) Are stoloniferous plants able to avoid neighbours in response to low R:FR ratios in reflected light? Plant Ecol 141:59–65CrossRefGoogle Scholar
  30. Marcuvitz S, Turkington R (2000) Differential effects of light quality, provided by different grass neighbours, on the growth and morphology of Trifolium repens L. (white clover). Oecologia 125:293–300CrossRefGoogle Scholar
  31. Pierik R, Visser EJW, de Kroon H, Voesenek LACJ (2003) Ethylene is required in tobacco to successfully compete with proximate neighbours. Plant Cell Environ 26:1229–1234CrossRefGoogle Scholar
  32. Pigliucci M, Kolodynska A (2002) Phenotypic plasticity to light intensity in Arabidopsis thaliana: invariance of reaction norms and phenotypic integration. Evol Ecol 16:27–47CrossRefGoogle Scholar
  33. Pigliucci M, Tyler GA, Schlichting CD (1998) Mutational effects on constraints on character evolution and phenotypic plasticity in Arabidopsis thaliana. J Genet 77:95–103CrossRefGoogle Scholar
  34. Poulton J, Winn AA (2002) Costs of canalization and plasticity in response to neighbors in Brassica rapa. Plant Species Biol 17:109–118CrossRefGoogle Scholar
  35. Price EAC, Hutchings MJ (1996) The effects of competition on growth and form in Glechoma hederacea. Oikos 75:279–290CrossRefGoogle Scholar
  36. Scheiner SM, Berrigan D (1998) The genetics of phenotypic plasticity. VIII. The cost of plasticity in Daphnia pulex. Evolution 52:368–378CrossRefGoogle Scholar
  37. Schlichting CD, Smith H (2002) Phenotypic plasticity: linking molecular mechanisms with evolutionary outcome. Evol Ecol 16:189–211CrossRefGoogle Scholar
  38. Schmitt J (1997) Is photomorphogenic shade avoidance adaptive? Perspectives from population biology. Plant Cell Environ 20:826–830CrossRefGoogle Scholar
  39. Schmitt J, Wulff RD (1993) Light spectral quality, phytochrome and plant competition. Trends Ecol Evol 8:47–51CrossRefGoogle Scholar
  40. Schmitt J, McCormac AC, Smith H (1995) A test of the adaptive plasticity hypothesis using transgenic and mutant plants disabled in phytochrome-mediated elongation responses to neighbors. Am Nat 146:937–953CrossRefGoogle Scholar
  41. Schmitt J, Dudley SA, Pigliucci M (1999) Manipulative approaches to testing adaptive plasticity: phytochrome-mediated shade-avoidance responses in plants. Am Nat 154:S43–S54CrossRefGoogle Scholar
  42. Schmitt J, Stinchcombe JR, Heschel MS, Huber H (2003) The adaptive evolution of plasticity: phytochrome-mediated shade avoidance responses. Integr Comp Biol 43:459–469CrossRefGoogle Scholar
  43. Smith H (1982) Light quality, photoperception, and plant strategy. Annu Rev Plant Physiol Plant Mol Biol 33:481–518Google Scholar
  44. Smith H, Whitelam GC (1997) The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Environ 20:840–844CrossRefGoogle Scholar
  45. Solangaarachchi SM, Harper JL (1987) The effect of canopy filtered light on the growth of white clover Trifolium repens. Oecologia 72:372–376CrossRefGoogle Scholar
  46. Stuefer JF, Van Hulzen JB, During HJ (2002) A genotypic trade-off between the number and size of clonal offspring in the stoloniferous herb Potentilla reptans. J Evol Biol 15:880–884CrossRefGoogle Scholar
  47. Sultan SE (1995) Phenotypic plasticity and plant adaptation. Acta Botanica Neerlandica 44:363–383Google Scholar
  48. Thompson L (1993) The influence of natural canopy density on the growth of white clover, Trifolium repens. Oikos 67:321–324CrossRefGoogle Scholar
  49. Thompson L (1995) Sites of photoperception in white clover. Grass Forage Sci 50:259–262CrossRefGoogle Scholar
  50. Thompson L, Harper JL (1988) The effect of grasses on the quality of transmitted radiation and its influence on the growth of white clover Trifolium repens. Oecologia 75:343–347CrossRefGoogle Scholar
  51. Van Hinsberg A (1997) Morphological variation in Plantago lanceolata L.: effects of light quality and growth regulators on sun and shade populations. J Evol Biol 10:687–701CrossRefGoogle Scholar
  52. van Kleunen M, Fischer M (2001) Adaptive evolution of plastic foraging responses in a clonal plant. Ecology 82:3309–3319CrossRefGoogle Scholar
  53. van Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–60PubMedCrossRefGoogle Scholar
  54. van Tienderen PH (1991) Evolution of generalists and specialists in spatially heterogeneous environments. Evolution 45:1317–1331CrossRefGoogle Scholar
  55. Via S, Lande R (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39:505–522CrossRefGoogle Scholar
  56. Waite S (1994) Field evidence of plastic growth responses to habitat heterogeneity in the clonal herb Ranunculus repens. Ecol Res 9:311–316CrossRefGoogle Scholar
  57. Weijschede J, Martinkova J, de Kroon H, Huber H (2006) Shade avoidance in Trifolium repens: costs and benefits of plasticity in petiole length and leaf size. New Phytol 172:655–666PubMedCrossRefGoogle Scholar
  58. Weinig C (2000a) Differing selection in alternative competitive environments: shade-avoidance responses and germination timing. Evolution 54:124–136PubMedGoogle Scholar
  59. Weinig C (2000b) Plasticity versus canalization: population differences in the timing of shade-avoidance responses. Evolution 54:441–451PubMedGoogle Scholar
  60. Weinig C, Gravuer KA, Kane NC, Schmitt J (2004) Testing adaptive plasticity to UV: costs and benefits of stem elongation and light-induced phenolics. Evolution 58:2645–2656PubMedGoogle Scholar
  61. Zobel M, Zobel K (2002) Studying plant competition: from root biomass to general aims. J Ecol 90:578–580CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Jelmer Weijschedé
    • 1
  • Rick Berentsen
    • 1
  • Hans de Kroon
    • 1
  • Heidrun Huber
    • 1
  1. 1.Department of EcologyRadboud University NijmegenNijmegenThe Netherlands

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