BACKGROUND AND AIMS: The observed positive diversity effect on ecosystem functioning has rarely been assessed in terms of intraspecific trait variability within populations. Intraspecific phenotypic variability could stem both from underlying genetic diversity and from plasticity in response to environmental cues. The latter might derive from modifications to a plant's epigenome and potentially last multiple generations in response to previous environmental conditions. We experimentally disentangled the role of genetic diversity and diversity of parental environments on population productivity, resistance against environmental fluctuations and intraspecific phenotypic variation. METHODS: A glasshouse experiment was conducted in which different types of Arabidopsis thaliana populations were established: one population type with differing levels of genetic diversity and another type, genetically identical, but with varying diversity levels of the parental environments (parents grown in the same or different environments). The latter population type was further combined, or not, with experimental demethylation to reduce the potential epigenetic diversity produced by the diversity of parental environments. Furthermore, all populations were each grown under different environmental conditions (control, fertilization and waterlogging). Mortality, productivity and trait variability were measured in each population. KEY RESULTS: Parental environments triggered phenotypic modifications in the offspring, which translated into more functionally diverse populations when offspring from parents grown under different conditions were brought together in mixtures. In general, neither the increase in genetic diversity nor the increase in diversity of parental environments had a remarkable effect on productivity or resistance to environmental fluctuations. However, when the epigenetic variation was reduced via demethylation, mixtures were less productive than monocultures (i.e. negative net diversity effect), caused by the reduction of phenotypic differences between different parental origins. CONCLUSIONS: A diversity of environmental parental origins within a population could ameliorate the negative effect of competition between coexisting individuals by increasing intraspecific phenotypic variation. A diversity of parental environments could thus have comparable effects to genetic diversity. Disentangling the effect of genetic diversity and that of parental environments appears to be an important step in understanding the effect of intraspecific trait variability on coexistence and ecosystem functioning.

CIDE CSIC Montcada Valencia Spain

Department of Botany Faculty of Sciences University of South Bohemia České Budějovice Czech Republic

Institute of Botany Czech Academy of Sciences Průhonice Czech Republic

Institute of Ecology and Earth Sciences Department of Botany University of Tartu Tartu Estonia

Zobrazit více v PubMed

Akimoto  K, Katakami H, Kim HJ, et al.  2007. Epigenetic inheritance in rice plants. Annals of Botany 100: 205–217. PubMed PMC

Albert  CH. 2015. Intraspecific trait variability matters. Journal of Vegetation Science 26: 7–8.

Albert  CH, Thuiller W, Yoccoz NG, et al.  2010. Intraspecific functional variability: extent, structure and sources of variation. Journal of Ecology 98: 604– 613.

Alonso-Blanco  C, Koornneef M. 2000. Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. Trends in Plant Science 5: 22–29. PubMed

Balvanera  P, Pfisterer AB, Buchmann N, et al.  2006. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters 9: 1146–1156. PubMed

Blonder  B, Vasseur F, Violle C, Shipley B, Enquist BJ, Vile D. 2015. Testing models for the leaf economics spectrum with leaf and whole-plant traits in Arabidopsis thaliana. AoB PLANTS 7: plv049. PubMed PMC

Bolnick  DI, Amarasekare P, Araújo MS, et al.  2011. Why intraspecific trait variation matters in community ecology. Trends in Ecology & Evolution 26: 183–192. PubMed PMC

Booth  RE, Grime JP. 2003. Effects of genetic impoverishment on plant community diversity. Journal of Ecology 91: 721–730.

Bossdorf  O, Arcuri D, Richards CL, Pigliucci M. 2010. Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evolutionary Ecology 24: 541–553.

Bossdorf  O, Richards CL, Pigliucci M. 2008. Epigenetics for ecologists. Ecology Letters 11: 106–115. PubMed

Bradshaw  AD. 2006. Unravelling phenotypic plasticity – why should we bother? The New Phytologist 170: 644–648. PubMed

Cadotte  MW. 2017. Functional traits explain ecosystem function through opposing mechanisms. Ecology Letters 20: 989–996. PubMed

Carmona  CP, de Bello F, Azcárate FM, Mason NWH, Peco B. 2019. Trait hierarchies and intraspecific variability drive competitive interactions in Mediterranean annual plants. Journal of Ecology 107: 2078–2089.

Cook-Patton  SC, Hastings AP, Agrawal AA. 2016. Genotypic diversity mitigates negative effects of density on plant performance: a field experiment and life-cycle analysis of common evening primrose Oenothera biennis. Journal of Ecology 105: 726–735.

Crutsinger  GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ. 2006. Plant genotypic diversity predicts community structure and governs an ecosystem process. Science (New York, N.Y.) 313: 966–968. PubMed

Cubas  P, Vincent C, Coen E. 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157–161. PubMed

de Bello  F, Lavorel S, Albert CH, et al.  2011. Quantifying the relevance of intraspecific trait variability for functional diversity. Methods in Ecology and Evolution 2: 163–174.

Díaz  S, Lavorel S, de Bello F, Quétier F, Grigulis K, Robson TM. 2007. Incorporating plant functional diversity effects in ecosystem service assessments. Proceedings of the National Academy of Sciences of the United States of America 104: 20684–20689. PubMed PMC

Fridley  JD. 2001. The influence of species diversity on ecosystem productivity: How, where, and why? Oikos 93: 514–526.

Fridley  JD. 2003. Diversity effects on production in different light and fertility environments: An experiment with communities of annual plants. Journal of Ecology 91: 396–406.

Gross  N, Bagousse-Pinguet YL, Liancourt P, Berdugo M, Gotelli NJ, Maestre FT. 2017. Functional trait diversity maximizes ecosystem multifunctionality. Nature Ecology & Evolution 1: 132. PubMed

Hector  A, Hautier Y, Saner P, et al.  2010. General stabilizing effects of plant diversity on grassland productivity through population asynchrony and overyielding. Ecology 91: 2213–2220. PubMed

Herman  JJ, Spencer HG, Donohue K, Sultan SE. 2014. How stable “should” epigenetic modifications be? Insights from adaptive plasticity and bet hedging. Evolution 68: 632–643. PubMed

Herman  JJ, Sultan SE. 2011. Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Frontiers in Plant Science 2: 102. PubMed PMC

Herman  JJ, Sultan SE. 2016. DNA methylation mediates genetic variation for adaptive transgenerational plasticity. Proceedings of the Royal Society B: Biological Sciences 283: 20160988. PubMed PMC

Herrera  CM, Pozo MI, Bazaga P. 2012. Jack of all nectars, master of most: DNA methylation and the epigenetic basis of niche width in a flower-living yeast. Molecular Ecology 21: 2602–2616. PubMed

Hughes  AR, Inouye BD, Johnson MT, Underwood N, Vellend M. 2008. Ecological consequences of genetic diversity. Ecology Letters 11: 609–623. PubMed

Kotowska  AM, Cahill JF Jr, Keddie BA. 2010. Plant genetic diversity yields increased plant productivity and herbivore performance. Journal of Ecology 98: 237–245.

Kraft  NJB, Crutsinger GM, Forrestel EJ, Emery NC. 2014. Functional trait differences and the outcome of community assembly: an experimental test with vernal pool annual plants. Oikos 123: 1391–1399.

Kraft  NJB, Godoy O, Levine JM. 2015. Plant functional traits and the multidimensional nature of species coexistence. Proceedings of the National Academy of Sciences of the United States of America 112: 797–802. PubMed PMC

Kunstler  G, Falster D, Coomes DA, et al.  2016. Plant functional traits have globally consistent effects on competition. Nature 529: 204–207. PubMed

Latzel  V, Allan E, Bortolini Silveira A, Colot V, Fischer M, Bossdorf O. 2013. Epigenetic diversity increases the productivity and stability of plant populations. Nature Communications 4: 2875. PubMed

Latzel  V, Janeček Š, Doležal J, Klimešová J, Bossdorf O. 2014. Adaptive transgenerational plasticity in the perennial Plantago lanceolata. Oikos 123: 41–46.

Latzel  V, Zhang Y, Karlsson Moritz K, Fischer M, Bossdorf O. 2012. Epigenetic variation in plant responses to defence hormones. Annals of Botany 110: 1423–1428. PubMed PMC

Liancourt  P, Boldgiv B, Song DS, et al.  2015. Leaf-trait plasticity and species vulnerability to climate change in a Mongolian steppe. Global Change Biology 21: 3489–3498. PubMed

Liu  CH, Finke A, Díaz M, et al.  2015. Repair of DNA damage induced by the cytidine analog zebularine requires ATR and ATM in Arabidopsis. The Plant Cell 27: 1788–1800. PubMed PMC

Loreau  M, Hector A. 2001. Partitioning selection and complementarity in biodiversity experiments. Nature 412: 72–76. PubMed

Madani  N, Kimball JS, Ballantyne AP, et al.  2018. Future global productivity will be affected by plant trait response to climate. Scientific Reports 8: 2870. PubMed PMC

Marquard  E, Weigelt A, Temperton VM, et al.  2009. Plant species richness and functional composition drive overyielding in a six-year grassland experiment. Ecology 90: 3290–3302. PubMed

Méndez-Vigo  B, Gomaa NH, Alonso-Blanco C, Picó FX. 2013. Among- and within-population variation in flowering time of Iberian Arabidopsis thaliana estimated in field and glasshouse conditions. The New Phytologist 197: 1332–1343. PubMed

Messier  J, McGill BJ, Lechowicz MJ. 2010. How do traits vary across ecological scales? A case for trait-based ecology. Ecology Letters 13: 838–848. PubMed

Picó  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 180: 1009–1021. PubMed PMC

Puy  J, Dvořáková H, Carmona CP, de Bello F, Hiiesalu I, Latzel V. 2018. Improved demethylation in ecological epigenetic experiments: Testing a simple and harmless foliar demethylation application. Methods in Ecology and Evolution 9: 744–753.

R Core Team. 2016. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Reich  PB, Knops J, Tilman D, et al.  2001. Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition. Nature 410: 809–812. PubMed

Reusch  TB, Ehlers A, Hämmerli A, Worm B. 2005. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proceedings of the National Academy of Sciences of the United States of America 102: 2826–2831. PubMed PMC

Richards  CL, Alonso C, Becker C, et al.  2017. Ecological plant epigenetics: Evidence from model and non-model species, and the way forward. Ecology Letters 20: 1576–1590. PubMed

Richards  CL, Bossdorf O, Pigliucci M. 2010. What role does heritable epigenetic variation play in phenotypic evolution? BioScience 60: 232–237.

Roscher  C, Schumacher J, Gubsch M, et al.  2012. Using plant functional traits to explain diversity–productivity relationships. PLoS ONE 7: e36760. PubMed PMC

Semchenko  M, Saar S, Lepik A. 2014. Plant root exudates mediate neighbour recognition and trigger complex behavioural changes. The New Phytologist 204: 631–637. PubMed

Siefert  A, Violle C, Chalmandrier L, et al.  2015. A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecology Letters 18: 1406–1419. PubMed

Sultan  SE, Stearns SC. 2005. Environmentally contingent variation: Phenotypic plasticity and norms of reaction. In: Hallgrimsson B, Hall B, eds. Variation. Boston: Elsevier Academic Press, 303–332.

Tobner  CM, Paquette A, Gravel D, Reich PB, Williams LJ, Messier C. 2016. Functional identity is the main driver of diversity effects in young tree communities. Ecology Letters 19: 638–647. PubMed

Turcotte  MM, Levine JM. 2016. Phenotypic plasticity and species coexistence. Trends in Ecology & Evolution 31: 803–813. PubMed

Verhoeven  KJ, Jansen JJ, van Dijk PJ, Biere A. 2010. Stress-induced DNA methylation changes and their heritability in asexual dandelions. The New Phytologist 185: 1108–1118. PubMed

Wright  IJ, Reich PB, Cornelissen JH, et al.  2005. Assessing the generality of global leaf trait relationships. The New Phytologist 166: 485–496. PubMed

Zhang  YY, Fischer M, Colot V, Bossdorf O. 2013. Epigenetic variation creates potential for evolution of plant phenotypic plasticity. The New Phytologist 197: 314–322. PubMed

Zhang  YY, Latzel V, Fischer M, Bossdorf O. 2018. Understanding the evolutionary potential of epigenetic variation: a comparison of heritable phenotypic variation in epiRILs, RILs, and natural ecotypes of Arabidopsis thaliana. Heredity 121: 257–265. PubMed PMC

Zhu  Y, Chen H, Fan J, et al.  2000. Genetic diversity and disease control in rice. Nature 406: 718–722. PubMed

Zuppinger-Dingley  D, Schmid B, Petermann JS, Yadav V, De Deyn GB, Flynn DF. 2014. Selection for niche differentiation in plant communities increases biodiversity effects. Nature 515: 108–111. PubMed

Closely related species differ in their traits, but competition induces high intra-specific variability