Skip to main content
SpringerLink
Log in

A meta-analysis of the effects of plant traits and geographical scale on the magnitude of adaptive differentiation as measured by the difference between QST and FST

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

Abstract

The impact of directional selection on specific trait types in plant species, and how a species’ life history mediates this response to selection remains understudied. Discovering such interactions is however crucial for understanding the interplay between ecological and genetic processes underlying local adaptation in plants, and to evaluate a species’ evolutionary potential with respect to changing environments. Furthermore, it remains unclear whether the degree of adaptive differentiation generally increases with the geographical distance between plant populations. Here, we present a weighted mixed model based meta-analysis aimed at unraveling the potential interactions between plant trait types, life history characteristics and QST–FST comparisons, and assessing the effect of geographical scale on population differentiation. Based on 51 studies we found that QST values exceeded their corresponding FST values in 71.74 % out of 401 cases. Furthermore, different trait types were found to be differently susceptible to natural selection and the magnitude of QST–FST comparisons was mediated by a plant species’ life span. These findings may be closely related to the genetic architectures of trait types and life histories, with the proportion of large-effect genes likely shaping the response to natural selection. QST–FST values also increased with increasing distance between populations, pinpointing the combined effects of environmental differentiation and isolation by distance on the magnitude of population divergence. Finally, our model showed an inverse relationship between FST and QST–FST values, presumably resulting from isolation by distance, the exchange of advantageous alleles, or genetic correlations among 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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aitken SN, Yeaman S, Holliday JA et al (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl 1:95–111

    Google Scholar 

  • Albert CH et al (2010) A multi-trait approach reveals the structure and the relative importance of intra- versus interspecific variability in plant traits. Funct Ecol 24(6):1192–1201

    Google Scholar 

  • Albert CH et al (2011) When and how should intraspecific variability be considered in trait-based plant ecology? Perspect Plant Ecol Evol Syst 13(3):217–225

    Google Scholar 

  • Alleaume-Benharira M, Pen IR, Ronce O (2006) Geographical patterns of adaptation within a species’ range: interactions between drift and gene flow. J Evol Biol 19:203–215

    PubMed  CAS  Google Scholar 

  • Anderson JT, Geber MA (2009) Demographic source-sink dynamics restrict local adaptation in elliott’s blueberry (Vaccinium elliottii). Evolution 64(2):370–384

    PubMed  Google Scholar 

  • Andreasen K, Baldwin BC (2001) Unequal evolutionary rates between annual and perennial lineages of checker mallows (Sidalcea, Malvaceae): evidence from 18S–26S rDNA internal and external transcribed spacers. Mol Biol Evol 18(6):936–944

    PubMed  CAS  Google Scholar 

  • Baraloto C et al (2010) Functional trait variation and sampling strategies in species-rich plant communities. Evolution 24(1):208–216

    Google Scholar 

  • Becker U et al (2006) Local adaptation in the monocarpic perennial Carlina vulgaris at different spatial scales across Europe. Oecologia 150(3):506–518

    PubMed  Google Scholar 

  • Bellard C et al (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15(4):365–377

    Google Scholar 

  • Bergelson J, Roux F (2010) Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana. Nat Rev Genet 11:867–879

    PubMed  CAS  Google Scholar 

  • Bisschoff A, Crémieux L, Smilauerova M et al (2006) Detecting local adaptation in widespread grassland species: the importance of scale and local plant community. J Ecol 94:1130–1142

    Google Scholar 

  • Bolnick DI et al (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26(4):183–192

    PubMed  Google Scholar 

  • Bradshaw HD, Stettler RF (1995) Molecular genetics of growth and development in Populus. IV. Mapping QTLs with large effects on growth, form, and phenology traits in a forest tree. Genetics 139:963–973

    PubMed  CAS  Google Scholar 

  • Castro J, Reich PB, Sánchez-Miranda A, Guerrero JD (2008) Evidence that the negative relationship between seed mass and relative growth rate is not physiological but linked to species identity: a within-family analysis of Scots pine. Tree Physiol 28:1077–1082

    PubMed  Google Scholar 

  • Chun YJ, Le Corre V, Bretagnolle F (2011) Adaptive divergence for a fitness-related trait among invasive Ambrosia artemisiifolia populations in France. Mol Ecol 20(7):1378–1388

    PubMed  Google Scholar 

  • Colautti RI, Lee CR, Mitchell-Olds T (2012) Origin, fate, and architecture of ecologically relevant genetic variation. Curr Opin Plant Biol 15:199–204

    PubMed  Google Scholar 

  • Díaz S et al (2007) Incorporating plant functional diversity effects in ecosystem service assessments. PNAS 104(52):20684–20689

    PubMed  Google Scholar 

  • Donohue K (2009) Completing the cycle: maternal effects as the missing link in plant life histories. Philos Trans R Soc B 364:1059–1074

    CAS  Google Scholar 

  • Draghi JA, Whitlock MC (2012) Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution. doi:10.1111/j.1558-5646.2012.01649.x

    PubMed  Google Scholar 

  • Edelaar P, Burraco P, Gomez-Mestre I (2011) Comparisons between Qst and Fst: How wrong have we been? Mol Ecol 20(23):4830–4839

    PubMed  Google Scholar 

  • Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634

    PubMed  CAS  Google Scholar 

  • Ehrlich PR, Raven PH (1969) Differentiation of populations. Science 165:1228–1232

    PubMed  CAS  Google Scholar 

  • Elith J, Leathrick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40:677–697

    Google Scholar 

  • Freeman JS et al (2009) QTL influencing growth and wood properties in Eucalyptus globules. Tree Genet Genomes 5(4):713–722

    Google Scholar 

  • Frewen BE et al (2000) Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus. Genetics 154:837–845

    PubMed  CAS  Google Scholar 

  • Galloway LF, Fenster CB (2000) Population differentiation in an annual legume: local adaptation. Evolution 54:1173–1181

    PubMed  CAS  Google Scholar 

  • Goudet J, Büchi L (2006) The effects of dominance, regular inbreeding and sampling design on QST an estimator of population differentiation for quantitative traits. Genetics 172:1337–1347

    PubMed  Google Scholar 

  • Goudet J, Martin G (2007) Under neutrality, QST ≤ FST when there is dominance in an island model. Genetics 176:1371–1374

    PubMed  Google Scholar 

  • Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194

    Google Scholar 

  • Guillaume F (2011) Migration-induced phenotypic divergence: the migration-selection balance of correlated traits. Evolution 65(6):1723–1738

    PubMed  Google Scholar 

  • Haggerty BP, Galloway LF (2010) Response of individual components of reproductive phenology to growing season length in a monocarpic herb. J Ecol 99(1):242–253

    Google Scholar 

  • Hendry AP (2002) Qst >=< Fst? Trends Ecol Evol 17:502

    Google Scholar 

  • Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173(5):579–588

    PubMed  Google Scholar 

  • Hill WG, Zhang XS (2012) On the pleiotropic structure of the genotype–phenotype map and the evolvability of complex organisms. Genetics 3. doi:10.1534/genetics.111.135681

  • Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485

    PubMed  CAS  Google Scholar 

  • Jaramillo-Correa JP, Beaulieu J, Bousquet J (2001) Contrasting evolutionary forces driving population structure at expressed sequence tag polymorphisms, allozymes and quantitative traits in white spruce. Mol Ecol 10:2729–2740

    PubMed  CAS  Google Scholar 

  • Jia P, Bayaerta T, Li X, Du G (2011) Relationships between flowering phenology and functional traits in eastern Tibet alpine meadow. Arct Antarct Alp Res 43(4):585–592

    Google Scholar 

  • Joshi J, Schmid B, Caldeira MC et al (2001) Local adaptation enhance performance of common plant species. Ecol Lett 4:536–544

    Google Scholar 

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

    Google Scholar 

  • Keller SR, Soolanayakanahally RY, Guy RD et al (2011) Climate-driven local adaptation of ecophysiology and phenology in balsam poplar, Populus balsamifera L. (Salicaceae). Am J Bot 98(1):99–108

    PubMed  Google Scholar 

  • Kenward M, Roger J (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997

    PubMed  CAS  Google Scholar 

  • Khan AI et al (2011) Negative epistasis between beneficial mutations in an evolving bacterial population. Science 332(6034):1193–1196

    PubMed  CAS  Google Scholar 

  • Kingsolver JG, Diamond SE (2011) Phenotypic selection in natural populations: what limits directional selection? Am Nat 177(3):345–357

    Google Scholar 

  • Kingsolver JG, Hoekstra HE, Hoekstra JM et al (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261

    PubMed  CAS  Google Scholar 

  • Kittelson PM, Maron JL (2001) Fine-scale genetically based differentiation of life-history traits in the perennial shrub Lupinus arboreus. Evolution 55(12):2429–2438

    PubMed  CAS  Google Scholar 

  • Kremer A, Ronce O, Robledo-Arnuncio JJ et al (2012) Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecol Lett 15(4):378–392

    Google Scholar 

  • Kromrey JD, Rendina-Gobioff G (2006) On knowing what we do not know: an empirical comparison of methods to detect publication bias in meta-analysis. Educ Phychol Meas 66(3):357–373

    Google Scholar 

  • Kruuk LEB, Garant D (2007) A wake-up call for studies of natural selection. J Evol Biol 20:30–33

    PubMed  CAS  Google Scholar 

  • Kruuk LEB, Slate J, Wilson AJ (2008) New answers for old questions: the evolutionary quantitative genetics of wild animal populations. Annu Rev Ecol Evol Syst 39:525–548

    Google Scholar 

  • Lavergne S et al (2010) Biodiversity and climate change: integrating evolutionary and ecological responses of species and communities. Annu Rev Ecol Evol Syst 41:321–350

    Google Scholar 

  • Lavorel S, Grigulis K (2012) How fundamental plant functional trait relationships scale-up to trade-offs and synergies in ecosystem services. J Ecol 100(1):128–140

    Google Scholar 

  • Leimu R, Fischer M (2008) A meta-analysis of local adaptation in plants. PLoS ONE 3(12):1–8

    Google Scholar 

  • Leinonen T, O’Hara RB, Cano JM, Merilä J (2008) Comparative studies of quantitative trait and neutral marker divergence a meta-analysis. J Evol Biol 21:1–17

    PubMed  CAS  Google Scholar 

  • Lenormand T (2002) Gene flow and the limits of natural selection. Trends Ecol Evol 17:183–189

    Google Scholar 

  • Lenssen JBM, Van Kleunen M, Fischer M, De Kroon H (2004) Local adaptation of clonal plant Ranunculus reptans to flooding along a small-scale gradient. J Ecol 92:696–706

    Google Scholar 

  • Levin DA (1979) The nature of plant species. Science 204:381–384

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Littell RC, Stroup WW, Freund RJ (2002) SAS for linear models. SAS Institute, Cary

    Google Scholar 

  • Lopez S et al (2008) Migration load in plants: role of pollen and seed dispersal in heterogeneous landscapes. J Evol Biol 21(1):294–309

    PubMed  CAS  Google Scholar 

  • López-Fanjul C, Fernández A, Toro MA (2003) The effect of neutral nonadditive gene action on the quantitative index of population divergence. Genetics 164:1627–1633

    PubMed  Google Scholar 

  • López-Fanjul C, Fernández A, Toro MA (2007) The effect of dominance on the use of QST–FST contrast to detect natural selection on quantitative traits. Genetics 176(1):725–727

    PubMed  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Assocs., Inc., Sunderland

    Google Scholar 

  • Macaskill P, Walter SD, Irwig L (2001) A comparison of methods to detect publication bias in meta-analysis. Stat Med 20:641–654

    PubMed  CAS  Google Scholar 

  • McGill BJ et al (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21(4):178–185

    PubMed  Google Scholar 

  • McGuigan K, Rowe L, Blows MW (2011) Pleiotropy, apparent stabilizing selection and uncovering fitness optima. Trends Ecol Evol 26(1):22–29

    PubMed  Google Scholar 

  • McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17(6):285–291

    Google Scholar 

  • Merilä J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903

    Google Scholar 

  • Merilä J, Sheldon BC (1999) Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83:103–109

    PubMed  Google Scholar 

  • Møller AP, Jennions MD (2001) Testing and adjusting for publication bias. Trends Ecol Evol 16(10):580–586

    Google Scholar 

  • Moloney KA et al (2009) Rethinking the common garden in invasion research. Perspect Plant Ecol Evol Syst 11(4):311–320

    Google Scholar 

  • Morrissey MB et al (2012) Genetic analysis of life-history constrain and evolution in a wild ungulate population. Am Nat 179(4):97–114

    Google Scholar 

  • Muir CD, Moyle LC (2009) Antagonistic epistasis for ecophysiological trait differences between Solanum species. New Phytol 183(3):789–802

    PubMed  Google Scholar 

  • O’Brien EK, Mazanec RA, Krauss SL (2007) Provenance variation of ecologically important traits of forest trees: implications for restoration. J Appl Ecol 44:583–593

    Google Scholar 

  • O’Hara RB, Merilä J (2005) Bias and precision in QST estimates: problems and some solutions. Genetics 171:1331–1339

    PubMed  Google Scholar 

  • Orr HA (2000) Adaptation and the cost of complexity. Evolution 54:13–20

    Google Scholar 

  • Pavlicev M, Wagner GP (2012) A model of developmental evolution: selection, pleiotropy and compensation. Trends Ecol Evol 27(6):316–322

    Google Scholar 

  • Pico FX, Méndez-Vigo B, Martínez-Zapater JM, Alonso-Blanco C (2008) Natural genetic variation of Arabidopsis thaliana is geographically structured in the Iberian Peninsula. Genetics 188:421–433

    Google Scholar 

  • Poorter L, Bongers L, Bongers F (2006) Architecture of 54 moist-forest tree species: traits, trade-offs and functional groups. Ecology 87(5):1289–1301

    PubMed  Google Scholar 

  • Price T, Schluter D (1991) On the low heritability of life history traits. Evolution 45:853–861

    Google Scholar 

  • Prinzenberg AE et al (2010) Relationships between growth, growth response to nutrient supply, and ion content using a recombinant inbred line population in Arabidopsis. Plant Physiol 154(3):1361–1371

    PubMed  CAS  Google Scholar 

  • Pujol B et al (2008) Are QST–FST comparisons for natural populations meaningful? Mol Ecol 17(22):4782–4785

    PubMed  CAS  Google Scholar 

  • Razeto-Barry P et al (2010) Molecular evolution, mutation size and gene pleiotropy: a geometric reexamination. Genetics 187(3):877–885

    PubMed  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17(1):230–237

    Google Scholar 

  • Rieseberg LH, Widmer A, Arntz AM, Burke JM (2002) Directional selection is the primary cause of phenotypic diversification. PNAS 99(19):12242–12245

    PubMed  CAS  Google Scholar 

  • Rohde A et al (2011) Bud set in poplar: genetic dissection of a complex trait in natural and hybrid populations. New Phytol 189(1):106–121

    PubMed  CAS  Google Scholar 

  • Roumet C, Urcelay C, Díaz S (2006) Suites of root traits differ between annual and perennial species growing in the field. New Phytol 170:357–368

    PubMed  Google Scholar 

  • Sambatti JBM, Rice KJ (2006) Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis). Evolution 60(4):696–710

    PubMed  Google Scholar 

  • Santure AW, Whang J (2009) The joint effects of selection and dominance on the QST–FST contrast. Genetics 181(1):259–276

    PubMed  Google Scholar 

  • Savoleinen O, Pyhäjärvi T, Knürr T (2007) Gene flow and local adaptation in trees. Annu Rev Ecol Evol Syst 38:595–619

    Google Scholar 

  • Scheepens JF, Frei ES, Stöcklin J (2010) Genotypic and environmental variation in specific leaf area in widespread alpine plant after transplantation to different altitudes. Oecologia 164(1):141–150

    PubMed  CAS  Google Scholar 

  • Setoguchi H, Mitsui Y, Ikeda H et al (2011) Genetic structure of the critically endangered plant Tricyrtis ishiiana (Convallariaceae) in relict populations of Japan. Conserv Genet 12:491–501

    Google Scholar 

  • Slatkin M (1987) Gene flow and the geography of natural populations. Science 236:787–792

    PubMed  CAS  Google Scholar 

  • Smith SA, Beaulieu JM (2009) Life history influences rates of climatic niche evolution in flowering plants. Proc R Soc B 276(1677):4345–4352

    PubMed  Google Scholar 

  • Smith SA, Donoghue MJ (2008) Rates of molecular evolution are linked to life history of flowering plants. Science 322(5898):86–89

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • SPSS Inc. SPSS Base 17.0 for Windows User’s Guide. SPSS Inc., Chicago IL

  • Stearns FW (2010) One hundred years of pleiotropy: a retrospective. Genetics 186(3):767–773

    PubMed  CAS  Google Scholar 

  • Suding KN, Goldstein LJ (2008) Testing the holy grail framework: using functional traits to predict ecosystem change. New Phytol 180(3):559–562

    PubMed  Google Scholar 

  • Sztepanacz JL, Rundle HD (2012) Reduced genetic variance among high fitness individuals: inferring stabilizing selection on male sexual displays in Drosophila serrata. Evolution. doi:10.1111/j.1558-5646.2012.01658.x

    PubMed  Google Scholar 

  • Thomas JA et al (2010) A generation time effect on the rate of molecular evolution in invertebrates. Mol Biol Evol 27(5):1173–1180

    PubMed  CAS  Google Scholar 

  • Violle C, Navas ML, Vile D et al (2007) Let the concept of trait be functional! Oikos 116:882–892

    Google Scholar 

  • Vitasse Y et al (2010) Quantifying phenological plasticity to temperature in two temperate tree species. Funct Ecol 24(6):1211–1218

    Google Scholar 

  • Volis S, Yakubov B, Shulgina I et al (2005) Distinguishing adaptive from nonadaptive genetic differentiation: comparison of QST and FST at two spatial scales. Heredity 95:466–475

    PubMed  CAS  Google Scholar 

  • Wagner GP, Zhang J (2011) The pleiotropic structure of the genotype-phenotype map: the evolvability of complex organisms. Nat Rev Genet 12(204):213

    Google Scholar 

  • Whitlock MC (1999) Neutral additive genetic variance in a metapopulation. Genet Res 74:215–221

    PubMed  CAS  Google Scholar 

  • Whitlock MC (2008) Evolutionary inference from QST. Mol Ecol 17(8):1885–1896

    PubMed  Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354

    Google Scholar 

  • Zanne AE, Falster DS (2010) Plant functional traits—linkages among stem anatomy, plant performance and life history. N Phytol 185(2):348–351

    Google Scholar 

Download references

Acknowledgments

We would like to thank Tuomas Leinonen for providing us raw QST and FST data from the years 2007 and earlier. We appreciate the contributions from Jill Anderson, Mounawer Badri, Zdravko Baruch, Katrina Dlugosch, Met Gandour, Santiago C. González-Martínez, David Hall, Martin Lascoux, Sébastien Lavergne, Andrea Plüss, J.F. (Niek) Scheepens, Dorothy Steane, Jon Hollander, Johan Kroon and Yvonne Willi for providing additional data. We also thank Guy Vranckx and three anonymous referees for valuable comments.

Author information

Authors and Affiliations

  1. Plant Conservation & Population Biology, University of Leuven, Kasteelpark Arenberg 31, 3001, Heverlee, Belgium

    H. De Kort, K. Vandepitte & O. Honnay

  2. Plant Conservation & Population Biology, Biology Department, University of Leuven, Kasteelpark Arenberg 31, 3001, Heverlee, Belgium

    H. De Kort

Authors
  1. H. De Kort
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Vandepitte
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. O. Honnay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H. De Kort.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

De Kort, H., Vandepitte, K. & Honnay, O. A meta-analysis of the effects of plant traits and geographical scale on the magnitude of adaptive differentiation as measured by the difference between QST and FST . Evol Ecol 27, 1081–1097 (2013). https://doi.org/10.1007/s10682-012-9624-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-012-9624-9

Keywords

Search

Navigation