To understand the biological effects of climate change, it is essential to take into account species' evolutionary responses to their changing environments. Ongoing climate change is resulting in species shifting their geographical distribution ranges poleward. We tested whether a successful range expanding plant has rapidly adapted to the regional conditions in its novel range, and whether adaptation could be driven by herbivores. Furthermore, we investigated if enemy release occurred in the newly colonized areas and whether plant origins differed in herbivore resistance. Plants were cloned and reciprocally transplanted between three experimental sites across the range. Effects of herbivores on plant performance were tested by individually caging plants with either open or closed cages. There was no indication of (regional) adaptation to abiotic conditions. Plants originating from the novel range were always larger than plants from the core distribution at all experimental sites, with or without herbivory. Herbivore damage was highest and not lowest at the experimental sites in the novel range, suggesting no release from enemy impact. Genotypes from the core were more damaged compared to genotypes from newly colonized areas at the most northern site in the novel range, which was dominated by generalist slug herbivory. We also detected subtle shifts in chemical defenses between the plant origins. Genotypes from the novel range had more inducible defenses. Our results suggest that plants that are expanding their range with climate change may evolve increased vigor and altered herbivore resistance in their new range, analogous to invasive plants.

Department of Botany Faculty of Science Charles University Prague Benátská 2 128 01 Prague 2 Czech Republic

Institute of Biology Leiden University P O Box 9505 2300 RA Leiden The Netherlands

Institute of Botany The Czech Academy of Sciences Zámek 1 252 43 Průhonice Czech Republic

Institute of Ecology Friedrich Schiller University Jena Dornburger Str 159 07743 Jena Germany

Molecular Interaction Ecology Department of Plant Science Radboud University P O Box 9010 6500 GL Nijmegen The Netherlands

Molecular Interactions Ecology German Centre for Integrative Biodiverisity Research Deutscher Platz 5e 04103 Leipzig Germany

Plant Ecology University of Tübingen Auf der Morgenstelle 5 72076 Tübingen Germany

Plant Evolutionary Ecology University of Tübingen Auf der Morgenstelle 5 72076 Tübingen Germany

Terrestrial Ecology Netherlands Institute of Ecology Droevendaalsesteeg 10 6708 PB Wageningen The Netherlands

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Abela-Hofbauerova I, Munzbergova Z. Increased performance of Cirsium arvense from the invasive range. Flora. 2011;206:1012–1019. doi: 10.1016/j.flora.2011.07.007. DOI

Alofs KM, Jackson DA. The abiotic and biotic factors limiting establishment of predatory fishes at their expanding northern range boundaries in Ontario, Canada. Glob Change Biol. 2015;21:2227–2237. doi: 10.1111/gcb.12853. PubMed DOI

Berg MP, Kiers ET, Driessen G, van der Heijden M, Kooi BW, Kuenen F, Liefting M, Verhoef HA, Ellers J. Adapt or disperse: understanding species persistence in a changing world. Glob Change Biol. 2010;16:587–598. doi: 10.1111/j.1365-2486.2009.02014.x. DOI

Bischoff A, Hurault B. Scales and drivers of local adaptation in Brassica nigra (Brassicaceae) populations. Am J Bot. 2013;100:1162–1170. doi: 10.3732/ajb.1200500. PubMed DOI

Bleeker W. Hybridization and Rorippa austriaca (Brassicaceae) invasion in Germany. Mol Ecol. 2003;12:1831–1841. doi: 10.1046/j.1365-294X.2003.01854.x. PubMed DOI

Bleeker W, Hurka H. Introgressive hybridization in Rorippa (Brassicaceae): gene flow and its consequences in natural and anthropogenic habitats. Mol Ecol. 2001;10:2013–2022. doi: 10.1046/j.1365-294X.2001.01341.x. PubMed DOI

Bleeker W, Matthies A. Hybrid zones between invasive Rorippa austriaca and native R. sylvestris (Brassicaceae) in Germany: ploidy levels and patterns of fitness in the field. Heredity. 2005;94:664–670. doi: 10.1038/sj.hdy.6800687. PubMed DOI

Blossey B, Nötzold R. Evolution of increased competitive ability in invasive nonindigenous plants-a hypothesis. J Ecol. 1995;83:887–889. doi: 10.2307/2261425. DOI

Brown CD, Vellend M. Non-climatic constraints on upper elevational plant range expansion under climate change. Proc R Soc B. 2014;281:20141779. doi: 10.1098/rspb.2014.1779. PubMed DOI PMC

Brown PD, Tokuhisa JG, Reichelt M, Gershenzon J. Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochem. 2003;62:471–481. doi: 10.1016/S0031-9422(02)00549-6. PubMed DOI

Bruelheide H, Scheidel U. Slug herbivory as a limiting factor for the geographical range of Arnica montana. J Ecol. 1999;87:839–848. doi: 10.1046/j.1365-2745.1999.00403.x. DOI

Buchner R. Approach to determination of HPLC response factors for glucosinolates. In: Wathelet JP, editor. Glucosinolates in rapeseed. Dordrecht: Martinus Nijhoff Publishers; 1987. pp. 50–58.

Buckley J, Bridle JR. Loss of adaptive variation during evolutionary responses to climate change. Ecol Lett. 2014;17:1316–1325. doi: 10.1111/ele.12340. PubMed DOI

Buschmann H, Edwards PH, Dietz H. Variation in growth pattern and response to slug damage among native and invasive provenances of four perennial Brassicaceae species. J Ecol. 2005;93:322–334. doi: 10.1111/j.1365-2745.2005.00991.x. DOI

Chen IC, Hill JK, Ohlemuller R, Roy DB, Thomas CD. Rapid range shifts of species associated with high levels of climate warming. Science. 2011;333:1024–1026. doi: 10.1126/science.1206432. PubMed DOI

Cipollini D, Lieurance DM. Expression and costs of induced defense traits in Alliaria petiolata, a widespread invasive plant. Basic Appl Ecol. 2012;13:432–440. doi: 10.1016/j.baae.2012.06.007. DOI

Cipollini D, Mbagwu J, Barto K, Hillstrom C, Enright S. Expression of constitutive and inducible chemical defenses in native and invasive populations of Alliaria petiolata. J Chem Ecol. 2005;31:1255–1267. doi: 10.1007/s10886-005-5284-3. PubMed DOI

Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ. Is invasion success explained by the enemy release hypothesis? Ecol Lett. 2004;7:721–733. doi: 10.1111/j.1461-0248.2004.00616.x. DOI

Doorduin LJ, Vrieling K. A review of the phytochemical support for the shifting defence hypothesis. Phytochem Rev. 2011;10:99–106. doi: 10.1007/s11101-010-9195-8. PubMed DOI PMC

Dostalek T, Muenzbergova Z, Kladivova A, Macel M. Plant–soil feedback in native vs. invasive populations of a range expanding plant. Plant Soil. 2016;399:209–220. doi: 10.1007/s11104-015-2688-x. DOI

Ellstrand NC, Schierenbeck KA. Hybridization as a stimulus for the evolution of invasiveness in plants? Euphytica. 2006;148:35–46. doi: 10.1007/s10681-006-5939-3. PubMed DOI PMC

Engelkes T, Morrien E, Verhoeven KJF, Bezemer TM, Biere A, Harvey JA, McIntyre LM, Tamis WLM, van der Putten WH. Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature. 2008;456:946–948. doi: 10.1038/nature07474. PubMed DOI

Engelkes T, Wouters B, Bezemer TM, Harvey JA, van der Putten WH. Contrasting patterns of herbivore and predator pressure on invasive and native plants. Basic Appl Ecol. 2012;13:725–734. doi: 10.1016/j.baae.2012.10.005. DOI

Falk KL, Kastner J, Bodenhausen N, Schramm K, Paetz C, Vassao DG, Reichelt M, Von Knorre D, Bergelson J, Erb M, Gershenzon J, Meldau S. The role of glucosinolates and the jasmonic acid pathway in resistance of Arabidopsis thaliana against molluscan herbivores. Mol Ecol. 2014;23:1188–1203. doi: 10.1111/mec.12610. PubMed DOI PMC

Felker-Quinn E, Schweitzer JA, Bailey JK. Meta-analysis reveals evolution in invasive plant species but little support for Evolution of Increased Competitive Ability (EICA) Ecol Evol. 2013;3:739–751. doi: 10.1002/ece3.488. PubMed DOI PMC

Fortuna TM, Eckert S, Harvey JA, Vet LEM, Müller C, Gols R. Variation in plant defences among populations of a range-expanding plant: consequences for trophic interactions. New Phyt. 2014;204:989–999. doi: 10.1111/nph.12983. PubMed DOI

Gols R, Wagenaar R, Bukovinszky T, van Dam NM, Dicke M, Bullock JM, Harvey JA. Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids. Ecology. 2008;89:1616–1626. doi: 10.1890/07-0873.1. PubMed DOI

Gonzalez-Megias A, Menendez R, Roy D, Brereton T, Thomas CD. Changes in the composition of British butterfly assemblages over two decades. Glob Change Biol. 2008;14:1464–1474. doi: 10.1111/j.1365-2486.2008.01592.x. DOI

Gu X, Siemann E, Zhu L, Gao SX, Wang Y, Ding JQ. Invasive plant population and herbivore identity affect latex induction. Ecol Entomol. 2014;39:1–9. doi: 10.1111/een.12054. DOI

Hickling R, Roy DB, Hill JK, Fox R, Thomas CD. The distributions of a wide range of taxonomic groups are expanding polewards. Glob Change Biol. 2006;12:450–455. doi: 10.1111/j.1365-2486.2006.01116.x. DOI

Huberty M, Tielbörger K, Harvey JA, Müller C, Macel M. Chemical defenses (glucosinolates) of native and invasive populations of the range expanding invasive plant Rorippa austriaca. J Chem Ecol. 2014;40:363–370. doi: 10.1007/s10886-014-0425-1. PubMed DOI

Jakobs G, Weber E, Edwards PJ. Introduced plants of the invasive Solidago gigantea (Asteraceae) are larger and grow denser than conspecifics in the native range. Divers Distrib. 2004;10:11–19. doi: 10.1111/j.1472-4642.2004.00052.x. DOI

Joshi J, Vrieling K. The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett. 2005;8:704–714. doi: 10.1111/j.1461-0248.2005.00769.x. DOI

Joshi J, Schmid B, Caldeira MC, Dimitrakopoulos PG, Good J, Harris R, Hector A, Huss-Danell K, Jumpponen A, Minns A, Mulder CPH, Pereira JS, Prinz A, Scherer-Lorenzen M, Siamantziouras ASD, Terry AC, Troumbis AY, Lawton JH. Local adaptation enhances performance of common plant species. Ecol Lett. 2001;4:536–544. doi: 10.1046/j.1461-0248.2001.00262.x. DOI

Karban R, Baldwin IT. Induced repsonses to herbivory. Chicago: The University of Chicago Press; 1997.

Kawecki TJ, Ebert D. Conceptual issues in local adaptation. Ecol Lett. 2004;7:1225–1241. doi: 10.1111/j.1461-0248.2004.00684.x. DOI

Keil P (1999) Ecology of agriophytes Angelica archangelica ssp. litoralis, Bidens frondosa and Rorippa austriaca on river banks for the Ruhr region, Germany. Dissertationes Botanicae, Band 231. J. Camer Verlag, Berlin

Kirkpatrick M, Barton NH. Evolution of a species’ range. Am Nat. 1997;150:1–23. doi: 10.1086/286054. PubMed DOI

Lakeman-Fraser P, Ewers RM. Enemy release promotes range expansion in a host plant. Oecologia. 2013;172:1203–1212. doi: 10.1007/s00442-012-2555-x. PubMed DOI

Lankau RA. Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phyt. 2007;175:176–184. doi: 10.1111/j.1469-8137.2007.02090.x. PubMed DOI

Leimu R, Fischer M. A meta-analysis of local adaptation in plants. PLoS One. 2008;3:e4010. doi: 10.1371/journal.pone.0004010. PubMed DOI PMC

Lin TT, Klinkhamer PGL, Vrieling K. Parallel evolution in an invasive plant: effect of herbivores on competitive ability and regrowth of Jacobaea vulgaris. Ecol Let. 2016;18:668–676. doi: 10.1111/ele.12445. PubMed DOI

Macel M, Lawson CS, Mortimer SR, Smilauerova M, Bischoff A, Crémieux L, Dolezal J, Edwards AR, Lanta V, Bezemer TM, van der Putten WH, Igual JM, Rodriguez-Barrueco C, Müller-Schärer H, Steinger T. Climate vs. soil factors in local adaptation of two common plant species. Ecology. 2007;88:424–433. doi: 10.1890/0012-9658(2007)88[424:CVSFIL]2.0.CO;2. PubMed DOI

Marsico TD, Hellmann JJ. Dispersal limitation inferred from an experimental translocation of Lomatium (Apiaceae) species outside their geographic ranges. Oikos. 2009;118:1783–1792. doi: 10.1111/j.1600-0706.2009.17698.x. DOI

Menendez R, Gonzalez-Megias A, Lewis OT, Shaw MR, Thomas CD. Escape from natural enemies during climate-driven range expansion: a case study. Ecol Entomol. 2008;33:413–421. doi: 10.1111/j.1365-2311.2008.00985.x. DOI

Moran EV, Alexander JM. Evolutionary responses to global change: lessons from invasive species. Ecol Let. 2014;17:637–649. doi: 10.1111/ele.12262. PubMed DOI

Moshgani M, Kolvoort E, de Jong TJ. Pronounced effects of slug herbivory on seedling recruitment of Brassica cultivars and accessions, especially those with low levels of aliphatic glucosinolates. Basic Appl Ecol. 2014;15:607–615. doi: 10.1016/j.baae.2014.08.011. DOI

Nylund GM, Pereyra RT, Wood HL, Johannesson K, Pavia H. Increased resistance towards generalist herbivory in the new range of a habitat-forming seaweed. Ecosphere. 2012

Pankova H, Raabova J, Münzbergova Z. Mycorrhizal symbiosis and local adaptation in Aster amellus: a field transplant experiment. PLoS One. 2014;9(7):e93967. doi: 10.1371/journal.pone.0093967. PubMed DOI PMC

Parker JD, Burkepile DE, Hay ME. Opposing effects of native and exotic herbivores on plant invasions. Science. 2006;311:1459–1461. doi: 10.1126/science.1121407. PubMed DOI

Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature. 2003;421:37–42. doi: 10.1038/nature01286. PubMed DOI

Renwick JA, Radke C, Sachdev-Gupta K, Städler E. Leaf surface chemicals stimulating oviposition by Pieris rapae (Lepidoptera: Pieridae) on cabbage. Chemoecol. 1992;3:33–38. doi: 10.1007/BF01261454. DOI

Sexton JP, McIntyre PJ, Anger AL, Rice KJ. Evolution and ecology of species range limits. Ann Rev Ecol Evol Sys. 2009;40:415–436. doi: 10.1146/annurev.ecolsys.110308.120317. DOI

Tamis WLM, Van der Meijden R, Runhaar J, Bekker JM, Ozinga WA, Odé B, Hoste I. Standaardlijst van de Nederlandse flora 2003. Gorteria. 2004;30:101–195.

Torchin ME, Lafferty KD, Kuris AM. Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invasions. 2001;3:333–345. doi: 10.1023/A:1015855019360. DOI

Van der Putten WH, Macel M, Visser ME. Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Phil Trans R Soc B. 2010;365:2025–2034. doi: 10.1098/rstb.2010.0037. PubMed DOI PMC

Verhoeven KJF, Macel M, Wolfe LM, Biere A. Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proc R Soc B. 2011;278:2–8. doi: 10.1098/rspb.2010.1272. PubMed DOI PMC

Willis AJ, Thomas MB, Lawton JH. Is the increased vigour of invasive weeds explained by a trade-off between growth and herbivore resistance? Oecologia. 1999;120:632–640. doi: 10.1007/s004420050899. PubMed DOI

Zheng YL, Feng YL, Zhang LK, Callaway M, Valiente-Banuet A, Luo DQ, Liao ZY, Lei YB, Barclay GF, Silva-Pereyra C. Integrating novel chemical weapons and evolutionary increased competitive ability in success of a tropical invader. New Phyt. 2015;205:1350–1359. doi: 10.1111/nph.13135. PubMed DOI

Züst T, Heichinger C, Grossniklaus U, Harrington R, Kliebenstein DJ, Turnbull LA. Natural enemies drive geographic variation in plant defenses. Science. 2012;338:116–119. doi: 10.1126/science.1226397. PubMed DOI

Data on Herbivore Performance and Plant Herbivore Damage Identify the Same Plant Traits as the Key Drivers of Plant-Herbivore Interaction

Duration of the conditioning phase affects the results of plant-soil feedback experiments via soil chemical properties