Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

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.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 166:650–660

    Article  PubMed  Google Scholar 

  • Aphalo PJ, Ballare CL (1995) On the importance of information-acquiring systems in plant-plant interactions. Funct Ecol 9:5–14

    Article  Google Scholar 

  • 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 14:57–65

    Article  Google Scholar 

  • 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 91:10094–10098

    Article  PubMed  CAS  Google Scholar 

  • Cain ML (1994) Consequences of foraging in clonal plant species. Ecology 75:933–944

    Article  Google Scholar 

  • Cahill JF (2002) Interactions between root and shoot competition vary among species. Oikos 99:101–112

    Article  Google Scholar 

  • Cahill JF (2003) Lack of relationship between below-ground competition and allocation to roots in 10 grassland species. J Ecol 91:532–540

    Article  Google Scholar 

  • Callahan HS, Pigliucci M (2002) Shade-induced plasticity and its ecological significance in wild populations of Arabidopsis thaliana. Ecology 83:1965–1980

    Google Scholar 

  • de Kroon H, Hutchings MJ (1995) Morphological plasticity in clonal plants—the foraging concept reconsidered. J Ecol 83:143–152

    Article  Google Scholar 

  • DeWitt TJ, Sih A,Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

    Article  Google Scholar 

  • 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 54:1956–1968

    PubMed  CAS  Google Scholar 

  • Dorn LA, Pyle EH, Schmitt J (2000) Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs. Evolution 54:1982–1994

    PubMed  CAS  Google Scholar 

  • Dudley SA, Schmitt J (1996) Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. Am Nat 147:445–465

    Article  Google Scholar 

  • Evans RC, Turkington R (1988) Maintenance of morphological variation in a biotically patchy environment. New Phytol 109:369–376

    Article  Google Scholar 

  • Farley RA, Fitter AH (1999) Temporal and spatial variation in soil resources in a deciduous woodland. J Ecol 87:688–696

    Article  Google Scholar 

  • Galloway LF (1995) Response to natural environmental heterogeneity: maternal effects and selection on life-history characters and plasticities in Mimulus guttatus. Evolution 49:1095–1107

    Article  Google Scholar 

  • Garland T, Kelly SA (2006) Phenotypic plasticity and experimental evolution. J Exp Biol 209:2344–2361

    Article  PubMed  Google Scholar 

  • 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 82:41–48

    Article  Google Scholar 

  • Geber MA, Griffen LR (2003) Inheritance and natural selection on functional traits. Int J Plant Sci 164:S21–S42

    Article  Google Scholar 

  • Griffith TM, Sultan SE (2006) Plastic and constant developmental traits contribute to adaptive differences in co-occurring Polygonum species. Oikos 114:5–14

    Article  Google Scholar 

  • Hirose T, Werger MJA (1995) Canopy structure and photon flux partitioning among species in a herbaceous plant community. Ecology 76:466–474

    Article  Google Scholar 

  • Huber H, Hutchings MJ (1997) Differential response to shading in orthotropic and plagiotropic shoots of the clonal herb Glechoma hirsuta. Oecologia 112:485–491

    Article  Google Scholar 

  • Huber H, Fijan A, During HJ (1998) A comparative study of spacer plasticity in erect and stoloniferous herbs. Oikos 81:576–586

    Article  Google Scholar 

  • 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 163:548–563

    Article  PubMed  Google Scholar 

  • 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 75:1382–1393

    Google Scholar 

  • Jackson RB, Caldwell MM (1993) Geostatistical patterns of soil heterogeneity around individual perennial plants. J Ecol 81:683–692

    Article  Google Scholar 

  • Kleijn D, van Groenendael JM (1999) The exploitation of heterogeneity by a clonal plant in habitats with contrasting productivity levels. J Ecol 87:873–884

    Article  Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    Article  Google Scholar 

  • Leeflang L (1999) Are stoloniferous plants able to avoid neighbours in response to low R:FR ratios in reflected light? Plant Ecol 141:59–65

    Article  Google Scholar 

  • 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 125:293–300

    Article  Google Scholar 

  • Pierik R, Visser EJW, de Kroon H, Voesenek LACJ (2003) Ethylene is required in tobacco to successfully compete with proximate neighbours. Plant Cell Environ 26:1229–1234

    Article  CAS  Google Scholar 

  • Pigliucci M, Kolodynska A (2002) Phenotypic plasticity to light intensity in Arabidopsis thaliana: invariance of reaction norms and phenotypic integration. Evol Ecol 16:27–47

    Article  Google Scholar 

  • Pigliucci M, Tyler GA, Schlichting CD (1998) Mutational effects on constraints on character evolution and phenotypic plasticity in Arabidopsis thaliana. J Genet 77:95–103

    Article  Google Scholar 

  • Poulton J, Winn AA (2002) Costs of canalization and plasticity in response to neighbors in Brassica rapa. Plant Species Biol 17:109–118

    Article  Google Scholar 

  • Price EAC, Hutchings MJ (1996) The effects of competition on growth and form in Glechoma hederacea. Oikos 75:279–290

    Article  Google Scholar 

  • Scheiner SM, Berrigan D (1998) The genetics of phenotypic plasticity. VIII. The cost of plasticity in Daphnia pulex. Evolution 52:368–378

    Article  Google Scholar 

  • Schlichting CD, Smith H (2002) Phenotypic plasticity: linking molecular mechanisms with evolutionary outcome. Evol Ecol 16:189–211

    Article  Google Scholar 

  • Schmitt J (1997) Is photomorphogenic shade avoidance adaptive? Perspectives from population biology. Plant Cell Environ 20:826–830

    Article  Google Scholar 

  • Schmitt J, Wulff RD (1993) Light spectral quality, phytochrome and plant competition. Trends Ecol Evol 8:47–51

    Article  Google Scholar 

  • 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 146:937–953

    Article  Google Scholar 

  • Schmitt J, Dudley SA, Pigliucci M (1999) Manipulative approaches to testing adaptive plasticity: phytochrome-mediated shade-avoidance responses in plants. Am Nat 154:S43–S54

    Article  Google Scholar 

  • Schmitt J, Stinchcombe JR, Heschel MS, Huber H (2003) The adaptive evolution of plasticity: phytochrome-mediated shade avoidance responses. Integr Comp Biol 43:459–469

    Article  Google Scholar 

  • Smith H (1982) Light quality, photoperception, and plant strategy. Annu Rev Plant Physiol Plant Mol Biol 33:481–518

    CAS  Google Scholar 

  • Smith H, Whitelam GC (1997) The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Environ 20:840–844

    Article  Google Scholar 

  • Solangaarachchi SM, Harper JL (1987) The effect of canopy filtered light on the growth of white clover Trifolium repens. Oecologia 72:372–376

    Article  Google Scholar 

  • 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 15:880–884

    Article  Google Scholar 

  • Sultan SE (1995) Phenotypic plasticity and plant adaptation. Acta Botanica Neerlandica 44:363–383

    Google Scholar 

  • Thompson L (1993) The influence of natural canopy density on the growth of white clover, Trifolium repens. Oikos 67:321–324

    Article  Google Scholar 

  • Thompson L (1995) Sites of photoperception in white clover. Grass Forage Sci 50:259–262

    Article  Google Scholar 

  • 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 75:343–347

    Article  Google Scholar 

  • 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 10:687–701

    Article  Google Scholar 

  • van Kleunen M, Fischer M (2001) Adaptive evolution of plastic foraging responses in a clonal plant. Ecology 82:3309–3319

    Article  Google Scholar 

  • van Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–60

    Article  PubMed  Google Scholar 

  • van Tienderen PH (1991) Evolution of generalists and specialists in spatially heterogeneous environments. Evolution 45:1317–1331

    Article  Google Scholar 

  • Via S, Lande R (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39:505–522

    Article  Google Scholar 

  • Waite S (1994) Field evidence of plastic growth responses to habitat heterogeneity in the clonal herb Ranunculus repens. Ecol Res 9:311–316

    Article  Google Scholar 

  • 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 172:655–666

    Article  PubMed  Google Scholar 

  • Weinig C (2000a) Differing selection in alternative competitive environments: shade-avoidance responses and germination timing. Evolution 54:124–136

    PubMed  CAS  Google Scholar 

  • Weinig C (2000b) Plasticity versus canalization: population differences in the timing of shade-avoidance responses. Evolution 54:441–451

    PubMed  CAS  Google Scholar 

  • 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 58:2645–2656

    PubMed  CAS  Google Scholar 

  • Zobel M, Zobel K (2002) Studying plant competition: from root biomass to general aims. J Ecol 90:578–580

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Ecology, Radboud University Nijmegen, Toernooiveld 1, Nijmegen, 6525 ED, The Netherlands

    Jelmer Weijschedé, Rick Berentsen, Hans de Kroon & Heidrun Huber

Authors
  1. Jelmer Weijschedé
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rick Berentsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hans de Kroon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Heidrun Huber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jelmer Weijschedé.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weijschedé, J., Berentsen, R., de Kroon, H. et al. Variation in petiole and internode length affects plant performance in Trifolium repens under opposing selection regimes. Evol Ecol 22, 383–397 (2008). https://doi.org/10.1007/s10682-007-9224-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-007-9224-2

Keywords

Search

Navigation