Genetic differentiation and phenotypic plasticity jointly shape intraspecific trait variation, but their roles differ among traits. In short-lived plants, reproductive traits may be more genetically determined due to their impact on fitness, whereas vegetative traits may show higher plasticity to buffer short-term perturbations. Combining a multi-treatment greenhouse experiment with observational field data throughout the range of a widespread short-lived herb, Plantago lanceolata, we (1) disentangled genetic and plastic responses of functional traits to a set of environmental drivers and (2) assessed how genetic differentiation and plasticity shape observational trait-environment relationships. Reproductive traits showed distinct genetic differentiation that largely determined observational patterns, but only when correcting traits for differences in biomass. Vegetative traits showed higher plasticity and opposite genetic and plastic responses, masking the genetic component underlying field-observed trait variation. Our study suggests that genetic differentiation may be inferred from observational data only for the traits most closely related to fitness.

Agri Food and Biosciences Institute Belfast Northern Ireland UK

Biodiversity and Ecosystem Research Group Institut of Landscape Ecology University of Münster Germany

Biological Sciences University of Southampton Southampton UK

Botanic Garden Anastasie Fatu University Alexandru Ioan Cuza Iaşi Romania

CSIRO Land and Water EcoSciences Precinct Dutton Park Queensland Australia

Departamento de Biodiversidad Ecología y Evolución Universidad Complutense de Madrid Madrid Spain

Department of Agriculture Forest and Food Science University of Torino Grugliasco Italy

Department of Animal and Plant Sciences University of Sheffield Sheffield UK

Department of Biodiversity Conservation and Ecosystem Restoration Pyrenean Institute of Ecology Zaragoza Spain

Department of Biological Sciences Louisiana State University Baton Rouge Louisiana USA

Department of Biology Tufts University Medford Massachusetts USA

Department of Biology University of Turku Turku Finland

Department of Biology University of Virginia Charlottesville Virginia USA

Department of Biology University of York York UK

Department of Botany and Soroksár Botanical Garden Szent István University Budapest Hungary

Department of Botany Faculty of Science Charles University Prague Czech Republic

Department of Ecology and Evolutionary Biology University of California Irvine California USA

Department of Ecology Environment and Plant Sciences Stockholm University Stockholm Sweden

Department of Environmental Sciences Western Norway University of Applied Sciences Sogndal Norway

Department of Evolutionary Biology and Environmental Studies University of Zurich Zurich Switzerland

Department of Evolutionary Biology Ecology and Environmental Sciences Faculty of Biology University of Barcelona Barcelona Spain

Department of Geography King's College London London UK

Department of Integrative Biology University of Guelph Guelph Ontario Canada

Department of Natural Resource Sciences Thompson Rivers University Kamloops British Columbia Canada

Department of Physiological Diversity Helmholtz Centre for Environmental Research Leipzig Germany

Department of Plant and Microbial Biology North Carolina State University Raleigh North Carolina USA

Department of Plant Biology Ecology and Evolution Oklahoma State University Stillwater Oklahoma USA

Department of Plant Sciences and Biotechnology Georgikon Faculty University of Pannonia Keszthely Hungary

Department of Population Ecology Institute of Botany Czech Academy of Sciences Prague Czech Republic

Department of Zoology University of Oxford Oxford UK

Facultad de Ciencias de la Salud Universidad Alfonso 10 el Sabio Villanueva de la Cañada Madrid Spain

German Centre for Integrative Biodiversity Research Halle Jena Leipzig Leipzig Germany

Institut de Recerca de la Biodiversitat Universitat de Barcelona Barcelona Spain

Institute for Applied Ecology University of Canberra Canberra Australian Capital Territory Australia

Institute of Agricultural and Environmental Sciences Estonian University of Life Sciences Tartu Estonia

Institute of Biology Martin Luther University Halle Wittenberg Halle Germany

Institute of Ecology and Earth Sciences University of Tartu Tartu Estonia

Madrona Stewardship Eugene Oregon USA

Manaaki Whenua Landcare Research Lincoln New Zealand

Max Planck Institute for Demographic Research Rostock Germany

Natural History Museum University of Oslo Oslo Norway

Norwegian Institute for Nature Research Oslo Norway

Organismal and Evolutionary Biology Research Program Faculty of Biological and Environmental Sciences University of Helsinki Helsinki Finland

Plant Evolutionary Ecology Institut of Evolution and Ecology University of Tübingen Tübingen Germany

School of Agriculture and Food Sciences University of Queensland Gatton Queensland Australia

School of Biological Earth and Environmental Sciences and Environmental Research Institute University College Cork Cork Ireland

School of Biological Sciences The University of Queensland St Lucia Queensland Australia

School of Biological Sciences Washington State University Vancouver Washington USA

School of BioSciences University of Melbourne Melbourne Victoria Australia

School of Life and Environmental Sciences University of Sydney Sydney New South Wales Australia

School of Natural Sciences Zoology Trinity College Dublin Dublin Ireland

The Morton Arboretum Lisle Illinois USA

The National Research Centre for the Working Environment Copenhagen Denmark

See more in PubMed

Acasuso-Rivero, C., Murren, C.J., Schlichting, C.D. & Steiner, U.K. (2019) Adaptive phenotypic plasticity for life-history and less fitness-related traits. Proceedings of the Royal Society B, 286, 20190653.

Adler, P.B., Salguero-Gomez, R., Compagnoni, A., Hsu, J.S., Ray-Mukherjee, J., Mbeau-Ache, C. & et al. (2014) Functional traits explain variation in plant life history strategies. Proceedings of the National Academy of Sciences of the United States of America, 111, 740-745.

Albert, C.H., Thuiller, W., Yoccoz, N.G., Douzet, R., Aubert, S. & Lavorel, S. (2010b) A multi-trait approach reveals the structure and the relative importance of intra- vs. interspecific variability in plant traits. Functional Ecology, 24, 1192-1201.

Albert, C.H., Thuiller, W., Yoccoz, N.G., Soudant, A., Boucher, F., Saccone, P. & et al. (2010a) Intraspecific functional variability: extent, structure and sources of variation. Journal of Ecology, 98, 604-613.

Alexander, J.M., van Kleunen, M., Ghezzi, R. & Edwards, P.J. (2012) Different genetic clines in response to temperature across the native and introduced ranges of a global plant invader. Journal of Ecology, 100, 771-781.

Alpert, P. & Simms, E.L. (2002) The relative advantages of plasticity and fixity in different environments: when is it good for a plant to adjust? Evolutionary Ecology, 16, 285-297.

Benito Garzón, M., Alía, R., Robson, T.M. & Zavala, M.A. (2011) Intra-specific variability and plasticity influence potential tree species distributions under climate change. Global Ecology and Biogeography, 20, 766-778.

Biere, A. (1995) Genotypic and plastic variation in plant size: effects on fecundity and allocation patterns in Lychnis flos-cuculi along a gradient of natural soil fertility. Journal of Ecology, 83, 629-642.

Bradshaw, A.D. (1965). Evolutionary significance of phenotypic plasticity in plants. In: Caspari, E.W. & Thoday, J.M. (Eds.), Advances in genetics. New York: Academic Press, pp. 115-155.

Bruelheide, H., Dengler, J., Purschke, O., Lenoir, J., Jiménez-Alfaro, B., Hennekens, S.M. et al. (2018) Global trait-environment relationships of plant communities. Nature Ecology and Evolution, 2, 1906-1917.

Buckley, Y.M., Blomberg, S., Crone, E.E., Csergő, A.M., Ehrlén, J., García, M.B. et al. (2019). Plantpopnet protocol V1.01 2015. https://doi.org/10.6084/m9.figshare.7982810.v7

Burnham, K.P. & Anderson, D.R. (2002) Model selection and multimodel inference: a practical information-theoretic approach. Berlin, Germany: Springer Science & Business Media.

Burns, J.H., Blomberg, S.P., Crone, E.E., Ehrlén, J., Knight, T.M., Pichancourt, J.-B. et al. (2010) Empirical tests of life-history evolution theory using phylogenetic analysis of plant demography. Journal of Ecology, 98, 334-344.

Caruso, C.M., Maherali, H. & Martin, R.A. (2020) A meta-analysis of natural selection on plant functional traits. International Journal of Plant Sciences, 181, 44-55.

Cavers, P.B., Bassett, I.J. & Crompton, C.W. (1980) The biology of Canadian weeds. 47. Plantago lanceolata L. Canadian Journal of Plant Science, 60, 1269-1282.

Chevin, L.M. & Lande, R. (2015) Evolution of environmental cues for phenotypic plasticity. Evolution, 69, 2767-2775.

Clausen, J., Keck, D.D. & Hiesey, W.M. (1940). Experimental studies on the nature of species. I. Effect of varied environments on western North American plants. Publication 520. Washington DC: Carnegie Institution of Washington.

Clifford, H.T. (1962) Insect pollination of Plantago lanceolata L. Nature, 193, 196.

Conover, D.O., Duffy, T.A. & Hice, L.A. (2009) The covariance between genetic and environmental influences across ecological gradients: reassessing the evolutionary significance of countergradient and cogradient variation. Annals of the New York Academy of Sciences, 1168, 100-129.

Conover, D.O. & Schultz, E.T. (1995) Phenotypic similarity and the evolutionary significance of countergradient variation. Trends in Ecology & Evolution, 10, 248-252.

Des Roches, S., Post, D.M., Turley, N.E., Bailey, J.K., Hendry, A.P., Kinnison, M.T. et al. (2018) The ecological importance of intraspecific variation. Nature Ecology and Evolution, 2, 57-64.

DeWitt, T.J., Sih, A. & Wilson, D.S. (1998) Costs and limits of phenotypic plasticity. Trends in Ecology and Evolution, 13, 77-81.

Dwyer, J.M., Hobbs, R.J. & Mayfield, M.M. (2014) Specific leaf area responses to environmental gradients through space and time. Ecology, 95, 399-410.

Fick, S.E. & Hijmans, R.J. (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302-4315.

Franks, S.J., Weber, J.J. & Aitken, S.N. (2014) Evolutionary and plastic responses to climate change in terrestrial plant populations. Evolutionary Applications, 7, 123-139.

Frazee, J.E. & Marquis, R.J. (1994) Environmental contribution to floral trait variation in Chamaecrista fasciculata (Fabaceae: Caesalpinoideae). American Journal of Botany, 81, 206-215.

Frenne, P., Graae, B.J., Rodríguez-Sánchez, F., Kolb, A., Chabrerie, O., Decocq, G. et al. (2013) Latitudinal gradients as natural laboratories to infer species’ responses to temperature. Journal of Ecology, 101, 784-795.

Funk, J.L., Larson, J.E., Ames, G.M., Butterfield, B.J., Cavender-Bares, J., Firn, J. et al. (2017) Revisiting the Holy Grail: using plant functional traits to understand ecological processes. Biological Reviews, 92, 1156-1173.

García, M.B., Picó, F.X. & Ehrlén, J. (2008) Life span correlates with population dynamics in perennial herbaceous plants. American Journal of Botany, 95, 258-262.

GBIF.org. (2014). GBIF Occurrence Download 16 March 2014. https://doi.org/10.15468/dl.kqryr8

Gienapp, P., Teplitsky, C., Alho, J.S., Mills, J.A. & Merilä, J. (2008) Climate change and evolution: disentangling environmental and genetic responses. Molecular Ecology, 17, 167-178.

Hereford, J. (2009) A quantitative survey of local adaptation and fitness trade-offs. The American Naturalist, 173, 579-588.

Hilde, C.H., Gamelon, M., Saether, B.-E., Gaillard, J.-M., Yoccoz, N.G. & Pélabon, C. (2020) The demographic buffering hypothesis: evidence and challenges. Trends in Ecology and Evolution, 35, 6.

Hooker, J.D. (1867) Handbook of the New Zealand flora. Part 2. London: Reeve & Co.

Hughes, A.R., Inouye, B.D., Johnson, M.T.J., Underwood, N. & Vellend, M. (2008) Ecological consequences of genetic diversity. Ecology Letters, 11, 609-623.

Hulme, P.E. & Barrett, S.C.H. (2013) Integrating trait- and niche-based approaches to assess contemporary evolution in alien plant species. Journal of Ecology, 101, 68-77.

Iversen, C.M., McCormack, M.L., Powell, A.S., Blackwood, C.B., Freschet, G.T., Kattge, J. et al. (2017) A global fine-root ecology database to address below-ground challenges in plant ecology. New Phytologist, 215, 15-26.

Johnson, J.B. & Omland, K.S. (2004) Model selection in ecology and evolution. Trends in Ecology and Evolution, 19, 101-108.

Kattge, J., Bönisch, G., Díaz, S., Lavorel, S., Prentice, I.C., Leadley, P. et al. (2020) TRY plant trait database - enhanced coverage and open access. Global Change Biology, 26, 119-188.

Kattge, J., Díaz, S., Lavorel, S., Prentice, I.c., Leadley, P., Bönisch, G. et al. (2011) TRY - a global database of plant traits. Global Change Biology, 17, 2905-2935.

Keller, S.R., Sowell, D.R., Neiman, M., Wolfe, L.M. & Taylor, D.R. (2009) Adaptation and colonization history affect the evolution of clines in two introduced species. New Phytologist, 183, 678-690.

Kriticos, D.J., Webber, B.L., Leriche, A., Ota, N., Macadam, I., Bathols, J. & et al. (2012) CliMond: global high-resolution historical and future scenario climate surfaces for bioclimatic modelling. Methods in Ecology and Evolution, 3, 53-64.

Lacey, E.P., Roach, D.A., Herr, D., Kincaid, S. & Perrott, R. (2003) Multigenerational effects of flowering and fruiting phenology in Plantago lanceolata. Ecology, 84, 2462-2475.

Le Bagousse-Pinguet, Y., Börger, L., Quero, J.L., García-Gómez, M., Soriano, S., Maestre, F.T. & et al. (2015) Traits of neighbouring plants and space limitation determine intraspecific trait variability in semi-arid shrublands. Journal of Ecology, 103, 1647-1657.

Liancourt, P., Spence, L.A., Song, D.S., Lkhagva, A., Sharkhuu, A., Boldgiv, B. et al. (2013) Plant response to climate change varies with topography, interactions with neighbors, and ecotype. Ecology, 94, 444-453.

Liao, H., D'Antonio, C.M., Chen, B., Huang, Q. & Peng, S. (2016) How much do phenotypic plasticity and local genetic variation contribute to phenotypic divergences along environmental gradients in widespread invasive plants? A meta-analysis. Oikos, 125, 905-917.

MacColl, A.D.C. (2011) The ecological causes of evolution. Trends in Ecology and Evolution, 26, 514-522.

Magnani, F. (2009) Phenotypic variability: underlying mechanisms and limits do matter. New Phytologist, 184, 277-279. https://www.jstor.org/stable/27735776

Maitner, B.S., Boyle, B., Casler, N., Condit, R., Donoghue, J., Durán, S.M. et al. (2018) The BIEN R package: a tool to access the Botanical Information and Ecology Network (BIEN) database. Methods in Ecology and Evolution, 9, 373-379.

Maron, J.L., Vilà, M., Bommarco, R., Elmendorf, S. & Beardsley, P. (2004) Rapid evolution of an invasive plant. Ecological Monographs, 74, 261-280.

Matesanz, S., Gianoli, E. & Valladares, F. (2010) Global change and the evolution of phenotypic plasticity in plants. Annals of the New York Academy of Sciences, 1206, 35-55.

Matesanz, S. & Ramírez-Valiente, J.A. (2019) A review and meta-analysis of intraspecific differences in phenotypic plasticity: implications to forecast plant responses to climate change. Global Ecology and Biogeography, 28, 1682-1694.

McDonald, J.L., Franco, M., Townley, S., Ezard, T.H.G., Jelbert, K. & Hodgson, D.J. (2017) Divergent demographic strategies of plants in variable environments. Nature Ecology and Evolution, 1, 1-6.

Merilä, J. & Hendry, A.P. (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evolutionary Applications, 7, 1-14.

Meyers, S.C. & Liston, A. (2008) The biogeography of Plantago ovata Forssk. (Plantaginaceae). International Journal of Plant Sciences, 169, 954-962.

Montague, J.L., Barrett, S.C.H. & Eckert, C.G. (2008) Re-establishment of clinal variation in flowering time among introduced populations of purple loosestrife (Lythrum salicaria, Lythraceae). Journal of Evolutionary Biology, 21, 234-245.

Moran, E.V., Hartig, F. & Bell, D.M. (2016) Intraspecific trait variation across scales: implications for understanding global change responses. Global Change Biology, 22, 137-150.

Morris, W.F. & Doak, D.F. (2005) How general are the determinants of the stochastic population growth rate across nearby sites? Ecological Monographs, 75, 119-137.

Münzbergová, Z., Hadincová, V., Skálová, H. & Vandvik, V. (2017) Genetic differentiation and plasticity interact along temperature and precipitation gradients to determine plant performance under climate change. Journal of Ecology, 105, 1358-1373.

Oleksyn, J., Reich, P.B., Zytkowiak, R., Karolewski, P. & Tjoelker, M.G. (2003) Nutrient conservation increases with latitude of origin in European Pinus sylvestris populations. Oecologia, 136, 220-235.

Palacio-López, K. & Gianoli, E. (2011) Invasive plants do not display greater phenotypic plasticity than their native or non-invasive counterparts: a meta-analysis. Oikos, 120, 1393-1401.

Pfister, C.A. (1998) Patterns of variance in stage-structured populations: evolutionary predictions and ecological implications. Proceedings of the National Academy of Sciences of the United States of America, 95, 213-218.

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

Preite, V., Stöcklin, J., Armbruster, G.F.J. & Scheepens, J.F. (2015) Adaptation of flowering phenology and fitness-related traits across environmental gradients in the widespread Campanula rotundifolia. Evolutionary Ecology, 29, 249-267.

Quinn, G.P. & Keough, M.J. (2002) Experimental design and data analysis for biologists. Cambridge, UK: Cambridge University Press.

R Core Team (2017) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Reich, P b, Wright, I j, Cavender-Bares, J., Craine, J m, Oleksyn, J., Westoby, M. & et al. (2003) The evolution of plant functional variation: traits, spectra, and strategies. International Journal of Plant Sciences, 164, S143-S164.

Revelle, W. (2018) psych: Procedures for Personality and Psychological Research. V.1.8.3. Evanston, IL: Northwestern University https://CRAN.R-project.org/package=psych

Richards, C.L., Bossdorf, O., Muth, N.Z., Gurevitch, J. & Pigliucci, M. (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters, 9, 981-993.

Roach, D.A. (2003) Age-specific demography in Plantago: variation among cohorts in a natural plant population. Ecology, 84, 749-756.

Roach, D.A. & Wulff, R.D. (1987) Maternal effects in plants. Annual Review of Ecology and Systematics, 18, 209-235.

Rosche, C., Hensen, I., Schaar, A., Zehra, U., Jasieniuk, M., Callaway, R.M. et al. (2019) Climate outweighs native vs. nonnative range-effects for genetics and common garden performance of a cosmopolitan weed. Ecological Monographs, 89, e01386.

Roybal, C.M. & Butterfield, B.J. (2019) Species-specific trait-environment relationships among populations of widespread grass species. Oecologia, 189, 1017-1026.

Sagar, G.R. & Harper, J.L. (1964) Plantago Major L., P. Media L. and P. Lanceolata L. The Journal of Ecology, 52, 189-221.

Santangelo, J.S., Johnson, M.T.J. & Ness, R.W. (2018) Modern spandrels: the roles of genetic drift, gene flow and natural selection in the evolution of parallel clines. Proceedings of the Royal Society B: Biological Sciences, 285, 20180230.

Scheiner, S.M. (1993) Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics, 24, 35-68.

Schlichting, C.D. & Levin, D.A. (1984) Phenotypic plasticity of annual Phlox: tests of some hypotheses. American Journal of Botany, 71, 252-260.

Shefferson, R.P. & Roach, D.A. (2012) The triple helix of Plantago lanceolata: genetics and the environment interact to determine population dynamics. Ecology, 93, 793-802.

Sih, A. (2004) A behavioural ecological view of phenotypic plasticity. In: deWitt, T.J. & Scheiner, S.M. (Eds.) Phenotypic plasticity: functional and conceptual processes. New York: Oxford University Press, pp. 112-126.

Silvertown, J., Franco, M. & Menges, E. (1996) Interpretation of elasticity matrices as an aid to the management of plant populations for conservation. Conservation Biology, 10, 591-597.

Smith, A.L., Hodkinson, T.R., Villellas, J., Catford, J.A., Csergő, A.M., Blomberg, S.P. et al. (2020) Global gene flow releases invasive plants from environmental constraints on genetic diversity. Proceedings of the National Academy of Sciences of the United States of America, 117, 4218-4227.

Stearns, S.C. & Kawecki, T.J. (1994) Fitness sensitivity and the canalization of life-history traits. Evolution, 48, 1438-1450.

Sultan, S.E. (1995) Phenotypic plasticity and plant adaptation. Acta Botanica Neerlandica, 44, 363-383.

van de Pol, M., Bailey, L.D., McLean, N., Rijsdijk, L., Lawson, C.R. & Brouwer, L. (2016) Identifying the best climatic predictors in ecology and evolution. Methods in Ecology and Evolution, 7, 1246-1257.

Villellas, J. & García, M.B. (2017) Intrinsic and extrinsic drivers of recruitment across the distribution range of a seed-dimorphic herb. Plant Ecology, 218, 529-539.

Violle, C., Enquist, B.J., McGill, B.J., Jiang, L., Albert, C.H., Hulshof, C. et al. (2012) The return of the variance: Intraspecific variability in community ecology. Trends in Ecology and Evolution, 27, 244-252.

Violle, C., Navas, M.-L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I. & et al. (2007) Let the concept of trait be functional! Oikos, 116, 882-892.

Violle, C., Reich, P.B., Pacala, S.W., Enquist, B.J. & Kattge, J. (2014) The emergence and promise of functional biogeography. Proceedings of the National Academy of Sciences of the United States of America, 111, 13690-13696.

Weiner, J., Campbell, L.G., Pino, J. & Echarte, L. (2009) The allometry of reproduction within plant populations. Journal of Ecology, 97, 1220-1233.

Winn, A.A. & Gross, K.L. (1993) Latitudinal variation in seed weight and flower number in Prunella vulgaris. Oecologia, 93, 55-62.

Woods, E.C., Hastings, A.P., Turley, N.E., Heard, S.B. & Agrawal, A.A. (2012) Adaptive geographical clines in the growth and defense of a native plant. Ecological Monographs, 82, 149-168.