The seeds of invasion: enhanced germination in invasive European populations of black locust (Robinia pseudoacacia L.) compared to native American populations.
Robinia pseudoacacia; biological invasion; black locust; genetic differentiation; germination; life-history traits; phenotypic plasticity; quantitative genetics; seedlings; American Indians or Alaska Natives; Germination; Humans; Seeds; Trees; Robinia; American Natives; Ecology, Evolution, Behavior and Systematics; Plant Science; General Medicine
Abstract :
[en] Local adaptation and the evolution of phenotypic plasticity may facilitate biological invasions. Both processes can enhance germination and seedling recruitment, which are crucial life-history traits for plants. The rate, timing and speed of germination have recently been documented as playing a major role during the invasion process. Black locust (Robinia pseudoacacia L.) is a North American tree, which has spread widely throughout Europe. A recent study demonstrated that a few populations are the source of European black locust. Thus, invasive populations can be compared to native ones in order to identify genetic-based phenotypic differentiation and the role of phenotypic plasticity can thereby be assessed. A quantitative genetics experiment was performed to evaluate 13 juvenile traits of both native and invasive black locust populations (3000 seeds, 20 populations) subjected to three different thermal treatments (18 °C, 22 °C and 31 °C). The results revealed European populations to have a higher germination rate than the native American populations (88% versus 60%), and even when genetic distance between populations was considered. Moreover, this trait showed lower plasticity to temperature in the invasive range than in the native one. Conversely, other studied traits showed high plasticity to temperature, but they responded in a similar way to temperature increase: the warmer the temperature, the higher the growth rate or germination traits values. The demonstrated genetic differentiation between native and invasive populations testifies to a shift between ranges for the maximum germination percentage. This pattern could be due to human-mediated introduction of black locust.
Bouteiller, X P ; BIOGECO, INRAE, Univ. Bordeaux, Cestas, France
Moret, F; BIOGECO, INRAE, Univ. Bordeaux, Cestas, France
Ségura, R; BIOGECO, INRAE, Univ. Bordeaux, Cestas, France
Klisz, M; Department of Silviculture and Genetics, Forest Research Institute, Raszyn, Poland
Martinik, A; Faculty of Forestry and Wood Technology, Mendel University in Brno, Brno, Czech Republic
Monty, Arnaud ; Université de Liège - ULiège > TERRA Research Centre > Biodiversité et Paysage
Pino, J; Centre for Ecological Research and Forestry Applications (CREAF), Universitat Autònoma de Barcelona, Bellaterra (Barcelona), Spain
van Loo, M; Department of Forest Growth, Silviculture and Genetics, Research Centre for Forests (BFW), Vienna, Austria
Wojda, T; Department of Silviculture and Genetics, Forest Research Institute, Raszyn, Poland
Porté, A J; BIOGECO, INRAE, Univ. Bordeaux, Cestas, France
Mariette, S; BIOGECO, INRAE, Univ. Bordeaux, Cestas, France
Language :
English
Title :
The seeds of invasion: enhanced germination in invasive European populations of black locust (Robinia pseudoacacia L.) compared to native American populations.
We would like to thank all those who helped with sample collection: Dr Gideon Bradburd (Michigan State University) for support in America (XPB fieldwork), Marianne Corréard (INRAE—Avignon, France), Dr Volker Schneck (Thuenen Institute of Forest Genetics), Dr Santiago Gonzalez‐Martinez (INRAE—Bordeaux, France) who helped organise sampling in Spain, and Alexandra Quenu and Sébastien Irola (SMABVC, France) who helped locate black locust populations in Aquitaine, France. We are also grateful to Dr Amy Zanne (George Washington University, USA) for logistical help, Dr Shinichi Nakagawa (University of New South Wales, Australia) for reviewing code for the Bayesian mixed model incorporating genetic distances, and Dr Frédéric Barraquand (University of Bordeaux, France) for help with Bayesian mixed effect models. MK and TW acknowledge support of a grant from the General Directorate of State Forests in Poland (BLP‐386). This study was financially supported by the Forest and Nature Management Research Unit of Gembloux Agro‐BioTech, BioGeCo INRA‐Univ Bordeaux Research Unit, Special Research Fund of the University of Liège, Société Française d’Ecologie, French Agence de l’Eau, ANR‐10‐EQPX‐16 Xyloforest, EU COST Action FP1403 ‘Non‐Native Tree Species for European Forests—Experiences, Risks and Opportunities’ and Transnational Access to Research Infrastructure activity in the 7th Framework Program of the EC under the Trees4Future project (no.284181). Special thanks to Philippe Lejeune for supporting the collaborative project. We also thank Thomas Guillemaud, Gérard Largier, Eric Petit and Leopoldo Sanchez for useful comments on a previous version of this manuscript. Finally, we are very grateful to Niek Scheepens and two anonymous reviewers who significantly contributed to improving the manuscript.We would like to thank all those who helped with sample collection: Dr Gideon Bradburd (Michigan State University) for support in America (XPB fieldwork), Marianne Corre?ard (INRAE?Avignon, France), Dr Volker Schneck (Thuenen Institute of Forest Genetics), Dr Santiago Gonzalez-Martinez (INRAE?Bordeaux, France) who helped organise sampling in Spain, and Alexandra Quenu and Se?bastien Irola (SMABVC, France) who helped locate black locust populations in Aquitaine, France. We are also grateful to Dr Amy Zanne (George Washington University, USA) for logistical help, Dr Shinichi Nakagawa (University of New South Wales, Australia) for reviewing code for the Bayesian mixed model incorporating genetic distances, and Dr Fre?de?ric Barraquand (University of Bordeaux, France) for help with Bayesian mixed effect models. MK and TW acknowledge support of a grant from the General Directorate of State Forests in Poland (BLP-386). This study was financially supported by the Forest and Nature Management Research Unit of Gembloux Agro-BioTech, BioGeCo INRA-Univ Bordeaux Research Unit, Special Research Fund of the University of Li?ge, Socie?te? Fran?aise d?Ecologie, French Agence de l?Eau, ANR-10-EQPX-16 Xyloforest, EU COST Action FP1403 ?Non-Native Tree Species for European Forests?Experiences, Risks and Opportunities? and Transnational Access to Research Infrastructure activity in the 7th Framework Program of the EC under the Trees4Future project (no.284181). Special thanks to Philippe Lejeune for supporting the collaborative project. We also thank Thomas Guillemaud, Ge?rard Largier, Eric Petit and Leopoldo Sanchez for useful comments on a previous version of this manuscript. Finally, we are very grateful to Niek Scheepens and two anonymous reviewers who significantly contributed to improving the manuscript.
Barrett S.C.H., Colautti R.I., Eckert C.G. (2008) Plant reproductive systems and evolution during biological invasion. Molecular Ecology, 17, 373–383.
Beckmann M., Bruelheide H., Erfmeier A. (2011) Germination responses of three grassland species differ between native and invasive origins. Ecological Research, 26, 763–771.
Blair A.C., Wolfe L.M. (2004) The evolution of an invasive plant: an experimental study with Silene latifolia. Ecology, 85, 3035–3042.
Bonner F.T., Karrfalt R.P. (2008) The woody plant seed manual. Agriculture handbook, U.S. Department of Agriculture, Forest Service, Washington, DC, USA.
Bouteiller X.P., Barraquand F., Garnier-géré P., Harmand N., Laizet Y., Raimbault A., Segura R., Lassois L., Monty A., Verdu C., Mariette S., Porté A.J. (2018) No evidence for genetic differentiation in juvenile traits between Belgian and French populations of the invasive tree Robinia pseudoacacia. Plant Ecology and Evolution, 151, 5–17.
Bouteiller X.P., Porté A.J., Mariette S., Monty A. (2017) Using automated sanding to homogeneously break seed dormancy in black locust (Robinia pseudoacacia L., Fabaceae). Seed Science Research, 27, 1–8.
Bouteiller X.P., Verdu C.F., Aikio E., Bloese P., Dainou K., Delcamp A., De Thier O., Guichoux E., Mengal C., Monty A., Pucheu M., van Loo M., Josée P.A., Lassois L., Mariette S. (2019) A few north Appalachian populations are the source of European black locust. Ecology and Evolution.
Broennimann O., Treier U.A., Müller-Schärer H., Thuiller W., Peterson A.T., Guisan A. (2007) Evidence of climatic niche shift during biological invasion. Ecology Letters, 10, 701–709.
Caño L., Escarré J., Fleck I., Blanco-Moreno J.M., Sans F.X. (2008) Increased fitness and plasticity of an invasive species in its introduced range: a study using Senecio pterophorus. Journal of Ecology, 96, 468–476.
Cierjacks A., Kowarik I., Joshi J., Hempel S., Ristow M., Von Der Lippe M., Weber E. (2013) Biological Flora of the British Isles: Robinia pseudoacacia. Journal of Ecology, 101, 1623–1640.
Cobbett W. (1825) The woodlands. William Cobbett, London, UK.
Colautti R.I., Barrett S.C.H. (2013) Rapid adaptation to climate facilitates range expansion of an invasive plant. Science, 342, 364–366.
DAISIE (2006) Delivering alien invasive species in Europe. Springer, Dordrecht, the Netherlands.
DAISIE (2009) Hulme P., Nentwig W., Pys\̌ek P., Vilà M. (Eds), Handbook of alien species in Europe. Springer, Dordrecht, the Netherlands.
de Crève S.-J., Coeur J.H. (1786) Mémoire sur la culture et les usages du faux Acacia dans les États-Unis de 1’Amérique septentrionale. Paris, France.
De Frenne P., Graae B.J., Kolb A., Brunet J., Chabrerie O., Cousins S.A.O., Decocq G., Dhondt R., Diekmann M., Eriksson O., Heinken T., Hermy M., Jõgar Ü., Saguez R., Shevtsova A., Stanton S., Zindel R., Zobel M., Verheyen K. (2010) Significant effects of temperature on the reproductive output of the forest herb Anemone nemorosa L. Forest Ecology and Management, 259, 809–817.
DeWalt S.J., Denslow J.S., Hamrick J.L. (2004) Biomass allocation, growth, and photosynthesis of genotypes from native and introduced ranges of the tropical shrub Clidemia hirta. Oecologia, 138, 521–531.
Donohue K., Dorn L., Griffith C., Kim E., Aguilera A., Polisetty C.R., Schmitt J. (2005) The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing. Evolution, 59, 758–770.
Donohue K., Rubio de Casas R., Burghardt L., Kovach K., Willis C.G. (2010) Germination, postgermination adaptation, and species ecological ranges. Annual Review of Ecology, Evolution, and Systematics, 41, 293–319.
ESRI (2018) ArcGIS desktop: release 10.6.1. Environmental Systems Research Institute, Redlands, CA.
Engel K., Tollrian R., Jeschke J.M. (2011) Integrating biological invasions, climate change, and phenotypic plasticity. Communicative and Integrative Biology, 4, 247–250.
Erfmeier A., Bruelheide H. (2005) Invasive and native Rhododendron ponticum populations: is there evidence for genotypic differences in germination and growth? Ecography, 28, 417–428.
Eriksson O., Ehrlén J. (2008) Seedling recruitment and population ecology. 239–254.
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.
Forest Research (2015) Seed storage and pretreatment for Robinia pseudoacacia. Available from http://www.forestry.gov.ukAccessed (accessed10 February 2015).
François de Neufchateau N. (1807) Lettre sur le robinier. Galland, Paris, France.
French K., Robinson S.A., Lia J. (2017) Thermotolerance capacities of native and exotic coastal plants will lead to changes in species composition under increased heat waves. Conservation Physiology, 5, 1–10.
Genty B., Briantais J.-M., Baker N.R. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta—General Subjects, 990, 87–92.
Ghalambor C.K., McKay J.K., Carroll S.P., Reznick D.N. (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology, 21, 394–407.
Gillard M., Grewell B.J., Deleu C., Thiébaut G. (2017) Climate warming and water primroses: germination responses of populations from two invaded ranges. Aquatic Botany, 136, 155–163.
Gioria M., Pys\̌ek P. (2016) Early bird catches the worm: germination as a critical step in plant invasion. Biological Invasions, 19, 1055–1080.
Godoy O., Valladares F., Castro-Díez P. (2012) The relative importance for plant invasiveness of trait means, and their plasticity and integration in a multivariate framework. New Phytologist, 195, 912–922.
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.
Hirsch H., Hensen I., Wesche K., Renison D., Wypior C., Hartmann M., von Wehrden H. (2016) Non-native populations of an invasive tree outperform their native conspecifics. AoB PLANTS, 8, 1–11. https://doi.org/10.1093/aobpla/plw071
Hirsch H., Richardson D.M., Le Roux J.J. (2017) Introduction to the special issue: tree invasions: towards a better understanding of their complex evolutionary dynamics. AoB PLANTS, 9, 1–8. https://doi.org/10.1093/aobpla/plx014
Hirsch H., Wypior C., Wehrden H., Von W.K., Renison D., Hensen I. (2012) Germination performance of native and non-native Ulmus pumila populations. NeoBiota, 68, 53–68.
Hodgins K.A., Rieseberg L. (2011) Genetic differentiation in life-history traits of introduced and native common ragweed (Ambrosia artemisiifolia) populations. Journal of Evolutionary Biology, 24, 2731–2749.
Hulme P.E. (2008) Phenotypic plasticity and plant invasions: is it all Jack? Functional Ecology, 22, 3–7.
Huntley J.C. (1990) Robinia pseudoacacia L. black locust. In: Burns R. M., Honkala B. H. technical coordinators. Silvics of North America. Volume 2. Hardwoods. Agricculture Handbook 654. U.S. Department of Agriculture, Forest Service, Washington, DC, USA, pp. 755–761.
Hyldgaard B., Brix H. (2012) Intraspecies differences in phenotypic plasticity: invasive versus non-invasive populations of Ceratophyllum demersum. Aquatic Botany, 97, 49–56.
Iverson L.R., Prasad A.M. (1998) Predicting abundance of 80 tree species following climate change in the Eastern United States. Ecological Monographs, 68, 465–485.
Jastrzębowski S., Ukalska J., Kantorowicz W., Klisz M., Wojda T., Sułkowska M. (2017) Effects of thermal-time artificial scarification on the germination dynamics of black locust (Robinia pseudoacacia L.) seeds. European Journal of Forest Research, 136, 471–479.
Kaufman S.R., Smouse P.E. (2001) Comparing indigenous and introduced populations of Melaleuca quinquenervia (Cav.) Blake: response of seedlings to water and pH levels. Oecologia, 127, 487–494.
Keller S.R., Taylor D.R. (2008) History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecology Letters, 11, 852–866.
Kew Royal Botanic Garden (2015) Seed information database. Kew, London, UK.
Kruschke J.K. (2015) Doing Bayesian data analysis: a tutorial with R, JAGS, and Stan, 2nd edn. Academic Press, Boston, MA, USA.
Lamarque L.J., Lortie C.J., Porté A.J., Delzon S. (2014) Genetic differentiation and phenotypic plasticity in life-history traits between native and introduced populations of invasive maple trees. Biological Invasions, 17, 1109–1122.
Lamarque L.J., Porté A.J., Eymeric C., Lasnier J.B., Lortie C.J., Delzon S. (2013) A test for pre-adapted phenotypic plasticity in the invasive tree Acer negundo L. PLoS One, 8, e74239.
Lee C.E. (2002) Evolutionary genetics of invasive species. Trends in Ecology & Evolution, 17, 386–391.
Leiblein-Wild M.C., Kaviani R., Tackenberg O. (2014) Germination and seedling frost tolerance differ between the native and invasive range in common ragweed. Oecologia, 174, 739–750.
Leimu R., Fischer M. (2008) A meta-analysis of local adaptation in plants. PLoS One, 3, 1–8.
Leinonen T., McCairns R.J.S., O’Hara R.B., Merilä J. (2013) Qst-Fst comparisons: evolutionary and ecological insights from genomic heterogeneity. Nature Reviews Genetics, 14, 179–190.
Li X.-M., She D.-Y., Zhang D.-Y., Liao W.-J. (2014) Life history trait differentiation and local adaptation in invasive populations of Ambrosia artemisiifolia in China. Oecologia, 177, 669–677.
Linhart Y.B., Grant M.C. (1996) Evolutionary significance of local genetic differentiation in plants. Annual Review of Ecology and Systematics, 27, 237–277.
Little E.L. (1971). Atlas of United States trees. vol. 1. In: Conifers and important hardwoods. U.S. Department of Agriculture, Miscellaneous Publication 1146. Washington, DC, USA, p. 9, 313 maps.
Maron J.L., Vilà M., Bommarco R., Elmendorf S., Beardsley P. (2004) Rapid evolution of an invasive plant. Ecological Monographs, 74, 261–280.
Monty A., Bizoux J. P., Escarré J., Mahy G. (2013) Rapid plant invasion in distinct climates involves different sources of phenotypic variation. PLoS One, 8, e55627.
Monty A., Lebeau J., Meerts P., Mahy G. (2009) An explicit test for the contribution of environmental maternal effects to rapid clinal differentiation in an invasive plant. Journal of Evolutionary Biology, 22, 917–926.
Nicolescu V.N., Rédei K., Mason W.L., Vor T., Pöetzelsberger E., Bastien J.C., Brus R., Benc\̌ať T., Đodan M., Cvjetkovic B., Andras\̌ev S., La Porta N., Lavnyy V., Mandžukovski D., Petkova K., Roženbergar D., Wąsik R., Mohren G.M.J., Monteverdi M.C., Musch B., Klisz M., Perić S., Keça L., Bartlett D., Hernea C., Pástor M. (2020) Ecology, growth and management of black locust (Robinia pseudoacacia L.), a non-native species integrated into European forests. Journal of Forestry Research, 31, 1081–1101.
O’Hara R.B., Merilä J. (2005) Bias and precision in QST estimates: problems and some solutions. Genetics, 171, 1331–1339.
Oduor A.M.O., Leimu R., van Kleunen M. (2016) Invasive plant species are locally adapted just as frequently and at least as strongly as native plant species. Journal of Ecology, 104, 957–968.
Pigliucci M., Murren C.J., Schlichting C.D. (2006) Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology, 209, 2362–2367.
Plummer M. (2005) JAGS: just another Gibbs sampler. In: Proceedings of the 3rd International Workshop on Distributed Statistical Computing (DSC 2003).
Postma F.M., Ågren J. (2016) Early life stages contribute strongly to local adaptation in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA, 113:7590–7595.
Prentice I.C., Cramer W., Harrison S., Leemans R., Monserud R., Solomon A. (1992) A global biome model based on plant physiology and dominance, soil properties and climate. Journal of Biogeography, 19, 117–134.
Puchałka R., Dyderski M.K., Vítková M., Sádlo J., Klisz M., Netsvetov M., Prokopuk Y., Matisons R., Mionskowski M., Wojda T., Koprowski M., Jagodziński A.M. (2021) Black locust (Robinia pseudoacacia L.) range contraction and expansion in Europe under changing climate. Global Change Biology, 27, 1587–1600. https://doi.org/10.1111/gcb.15486
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from https://www.R-project.org/
R Development Core Team (2013) R software. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
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.
Richardson D.M., Rejmánek M. (2011) Trees and shrubs as invasive alien species—a global review. Diversity and Distributions, 17, 788–809.
Santiso X., López L., Gilbert K.J., Barreiro R., Whitlock M.C., Retuerto R. (2015) Patterns of genetic variation within and among populations in Arbutus unedo and its relation with selection and evolvability. Perspectives in Plant Ecology, Evolution and Systematics, 17, 185–192.
Shouman S., Mason N., Kichey T., Closset-Kopp D., Heberling J.M., Kobeissi A., Decocq G. (2017) Functional shift of sycamore maple (Acer pseudoplatanus) towards greater plasticity and shade tolerance in its invasive range. Perspectives in Plant Ecology, Evolution and Systematics, 29, 30–40.
Su Y., Yajima M. (2012) R2jags: a package for running jags from R. Available from https://CRANR-projectorg/package=R2jags
Valladares F., Sanchez-Gomez D., Zavala M.A. (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. Journal of Ecology, 94, 1103–1116.
Walck J.L., Hidayati S.N., Dixon K.W., Thompson K., Poschlod P. (2011) Climate change and plant regeneration from seed. Global Change Biology, 17, 2145–2161.
Woodward F.I. (1987) Climate and plant distribution. Cambridge University Press, Cambridge, UK.
Xu C., Tang S., Fatemi M., Gross C., Julien M.H., Curtis C., Van Klinken R.D. (2015) Population structure and genetic diversity of invasive Phyla canescens: implications for the evolutionary potential. Ecosphere, 6, Art162.
Zou J., Rogers W.E., Siemann E. (2007) Differences in morphological and physiological traits between native and invasive populations of Sapium sebiferum. Functional Ecology, 21, 721–730.