DNA, Chloroplast; DNA, Plant; Climate; DNA, Chloroplast/analysis; Ecosystem; Europe; Genetic Variation/physiology; Prunus/physiology; Rosaceae/genetics; Rosaceae/physiology; Genetics, Population; Black cherry; Invasive tree species; Microsatellites; Phylogeography; Population genetics; Prunus serotina var. serotina; Plant Science
Abstract :
[en] [en] BACKGROUND AND AIMS: Black cherry (Prunus serotina) is a North American tree that is rapidly invading European forests. This species was introduced first as an ornamental plant, then it was massively planted by foresters in many countries, but its origins and the process of invasion remain poorly documented. Based on a genetic survey of both native and invasive ranges, the invasion history of black cherry was investigated by identifying putative source populations and then assessing the importance of multiple introductions on the maintenance of gene diversity.
METHODS: Genetic variability and structure of 23 populations from the invasive range and 22 populations from the native range were analysed using eight nuclear microsatellite loci and five chloroplast DNA regions.
KEY RESULTS: Chloroplast DNA diversity suggests there were multiple introductions from a single geographic region (the north-eastern United States). A low reduction of genetic diversity was observed in the invasive range for both nuclear and plastid genomes. High propagule pressure including both the size and number of introductions shaped the genetic structure in Europe and boosted genetic diversity. Populations from Denmark, The Netherlands, Belgium and Germany showed high genetic diversity and low differentiation among populations, supporting the hypothesis that numerous introduction events, including multiple individuals and exchanges between sites, have taken place during two centuries of plantation.
CONCLUSIONS: This study postulates that the invasive black cherry has originated from east of the Appalachian Mountains (mainly the Allegheny plateau) and its invasiveness in north-western Europe is mainly due to multiple introductions containing high numbers of individuals.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Pairon, Marie ; Earth and Life Institute, Research group 'genetics, reproduction, populations', Université catholique de Louvain, Croix du Sud, Louvain-la-Neuve, Belgium
Petitpierre, Blaise; Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
Campbell, Michael; Penn State Erie Behredn College, School of Science, Erie, PA 16563, United States
Guisan, Antoine; Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
Broennimann, Olivier; Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
Baret, Philippe V; Earth and Life Institute, Research Group 'Genetics, Reproduction, Populations', Université Catholique de Louvain, 1348 Louvain-la-Neuve, Belgium
Jacquemart, Anne-Laure; Earth and Life Institute, Research Group 'Genetics, Reproduction, Populations', Université Catholique de Louvain, 1348 Louvain-la-Neuve, Belgium
Besnard, Guillaume; Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland ; Imperial College, Silwood Park Campus, Ascot, Berkshire SL5 7PY, United Kingdom
Language :
English
Title :
Multiple introductions boosted genetic diversity in the invasive range of black cherry (Prunus serotina; Rosaceae).
This study was supported by the Fonds Spéciaux de Recherche (FSR) of the Université catholique de Louvain (UCL), the Belgian Scientific Policy (BelSPo–InPlanBel) and the National Centre of Competence in Research (NCCR) Plant Survival, research programme of the Swiss National Science Foundation. Collection of some samples was partly funded by grants to K. O. Reinhart from Highlands Biological Station and from the AW Mellon Foundation. We are grateful for the kind collaboration of many foresters and scientists who helped us to collect leaves of Prunus serotina. Samples from France were provided by P. Geldreich, J. M. Ansolabehere, R. Rodriguez and J. Jaminon (Office National des Forêts), and G. Decocq (University of Picardie Jules Verne); from Germany by T. Heinken (University of Potsdam), U. Starfinger (Technische University of Berlin) and J. Meyer (Forestrevier Altenwalde); from The Netherlands by W. van der Putten (NIOO-KNAW) and A. Ehrenburg (Amsterdam Water Supply); from Italy by F. Caronni and L. Hildebrand (Parco Lombardo della Valle del Ticino) and S. Del Fabbro; from Denmark by E. Kjaer (Royal Veterinary and Agricultural University), N. P. Revsbech (University of Aarhus) and O. Raspé (Jardin botanique national de Belgique); from Poland by B. Suszka (Polish Academy of Sciences) and A. Halarewicz (University of Agriculture of Wroclaw); from the USA by G. Meyer (University of Wisconsin – Milwaukee Field Station), A. K. Buthod (Robert Bebb Herbarium, The University of Oklahoma), D. A. Lewis (Ada Hayden Herbarium, Iowa State University), L. Iverson (Northern Research Station, USDA Forest Service), R. B. Kaul and D. M. Sutherland (Bessey Herbarium University of Nebraska), T. S. Cochrane (University of Wisconsin–Madison Herbarium), K. O. Reinhart (United States Department of Agriculture, Agricultural Research Service), R. A. Klips (Ohio State University) and L. M. Bowe (Ozarks Regional Herbarium, Missouri State University). We thank L. Dhondt, C. Noël and D. Savova-Bianchi for technical help in the laboratory. We would like to thank O. Hardy, O. Raspé, U. Starfinger and two anonymous referees for helpful comments and revision of previous versions of the manuscript.
Bandelt HJ, Forster P, Rohl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37-48.
Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F. 2000. GENETIX 4.03, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, Populations, Interactions CNRS UMR 5000, Université de Montpellier II, Montpellier, France.
Besnard G, Henry P, Wille L, Cooke D, Chapuis E. 2007. On the origin of the invasive olives (Olea europaea L., Oleaceae). Heredity 99: 608-619.
Bucharova A, van Kleunen M. 2009. Introduction history and species characteristics partly explain naturalization success of North American woody species in Europe. Journal of Ecology 97: 230-238.
Carlton JT. 1996. Pattern, process and prediction in marine invasion ecology. Biological Conservation 78: 97-106.
Chabrerie O, Verheyen K, Saguez R, Decocq G. 2008. Disentangling relationships between habitat conditions, disturbance history, plant diversity, and American black cherry (Prunus serotina Ehrh.) invasion in a European temperate forest. Diversity and Distributions 14: 204-212.
Corander J, Marttinen P. 2006. Bayesian identification of admixture events using multi-locus molecular markers. Molecular Ecology 15: 2833-2843.
Cornuet JM, Luikart G. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001-2014.
Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M. 1999. New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153: 1989-2000.
DAISIE. 2009. Handbook of alien species in Europe. Knoxville, TN: Springer.
Devos N, Tyteca D, Raspé O, Wesselingh RA, Jacquemart AL. 2003. Pattern of chloroplast diversity among western European Dactylorhiza species (Orchidaceae). Plant Systematics and Evolution 243: 85-97.
Dlugosch KM, Parker IM. 2008. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17: 431-449.
Eckert CG, Manicacci D, Barrett SCH. 1996. Genetic drift and founder effect in native versus introduced populations of an invading plant, Lythrum salicaria (Lythraceae). Evolution 50: 1512-1519.
Excoffier L, Laval G, Schneider S. 2005. ARLEQUIN ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47-50.
Facon B, Pointier JP, Jarne P, Sarda V, David P. 2008. High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Current Biology 18: 363-367.
Forman J. 2003. The introduction of American plant species into Europe: issues and consequences. In: Child L, Brock J, Brundu G, et al eds. Plant invasions: ecological threats and management solutions. Backhuys: Leiden, 17-33.
Gaskin JF, Zhang DY, Bon MC. 2005. Invasion of Lepidium draba (Brassicaceae) in the western United States: distributions and origins of chloroplast DNA haplotypes. Molecular Ecology 14: 2331-2341.
Goudet J. 1995. FSTAT (Version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86: 485-486.
Grapputo A, Boman S, Lindstrom L, Lyytinen A, Mappes J. 2005. The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Molecular Ecology 14: 4207-4219.
Hardy OJ, Vekemans X. 2002. SPAGEDI: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2: 618-620.
Hedrick PW. 2005. A standardized genetic differentiation measure. Evolution 59: 1633-1638.
Henry P, Le Lay G, Goudet J, Guisan A, Jahodova S, Besnard G. 2009. Reduced genetic diversity, increased isolation and multiple introductions of invasive Giant Hogweed in the western Swiss Alps. Molecular Ecology 18: 2819-2831.
Hough AF. 1965. Black cherry (Prunus serotina Ehrh.). In: Fowells HA. ed. Silvics of forest trees of the United States. Agriculture Handbook No. 271. Washington DC: US Department of Agriculture, 539-545.
Hufbauer RA, Sforza R. 2008. Multiple introductions of two invasive Centaurea taxa inferred from cpDNA haplotypes. Diversity and Distribution 14: 252-261.
Le Roux JJ,Wieczorek AM, Meyer JY. 2008. Genetic diversity and structure of the invasive tree Miconia calvescens in Pacific islands. Diversity and Distributions 14: 935-948.
Lockwood JL, Cassey P, Blackburn T. 2005. The role of propagule pressure in explaining species invasions. Trends in Ecology & Evolution 20: 223-228.
Luikart G, Allendorf FW, Cornuet JM, Sherwin WB. 1998. Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity 89: 238-247.
McCauley DE, Smith RA, Lisenby JD, Hsieh C. 2003. The hierarchical spatial distribution of chloroplast DNA polymorphism across the introduced range of Silene vulgaris. Molecular Ecology 12: 3227-3235.
McVaugh R. 1951. A revision of the north American black cherries (Prunus serotina Ehrh., and relatives). Brittonia 7: 279-315.
Marquis D. 1990. Prunus serotina Ehrh. black cherry. In: Burns RM, Honkala BH. eds. Silvics of North America. Vol.2. Hardwoods. Washington, DC: US Department of Agriculture, Forest Service, 594-604.
Meekins JF, Ballard HE, McCarthy BC. 2001. Genetic variation and molecular biogeography of a North American invasive plant species (Alliaria petiolata, Brassicaceae). International Journal of Plant Sciences 162: 161-169.
Michalakis Y, Excoffier L. 1996. A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142: 1061-1064.
Muys B, Maddelein D, Lust N. 1992. Ecology, practice and policy of black cherry (Prunus serotina Ehrh.) management in Belgium. Silva Gandavensis 27: 28-45.
Nei M. 1972. Genetic distance between populations. American Naturalist 106: 283-292.
Nei M. 1987. Molecular evolutionary genetics. New York, NY: Columbia University Press.
Neuffer B, Hurka H. 1999. Colonization history and introduction dynamics of Capsella bursa-pastoris (Brassicaceae) in North America: isozymes and quantitative traits. Molecular Ecology 8: 1667-1681.
Novak SJ, Mack RN. 1993. Genetic variation in Bromus tectorum (Poaceae): comparison between native and introduced populations. Heredity 71: 167-176.
Novak SJ, Mack RN. 2001. Tracing plant introduction and spread: genetic evidence from Bromus tectorum (Cheatgrass). BioScience 51: 114-122.
Okada M, Lyle M, Jasieniuk M. 2009. Inferring the introduction history of the invasive apomictic grass Cortaderia jubata using microsatellite markers. Diversity and Distributions 15: 148-157.
Paetkau D, Calvert W, Stirling I, Strobeck C. 1995. Microsatellite analysis of population structure in Canadian polar bears. Molecular Ecology 4: 347-354.
Pairon MC. 2007. Ecology and population genetics of an invasive forest tree species: Prunus serotina Ehrh. PhD Dissertation, Université catholique de Louvain.
Pairon MC, Jacquemart AL. 2005. Disomic segregation of microsatellites in the tetraploid Prunus serotina Ehrh. (Rosaceae). Journal of the American Society for Horticultural Science 130: 729-734.
Pairon M, Chabrerie O, Mainer Casado C, Jacquemart AL. 2006a. Sexual regeneration traits linked to black cherry (Prunus serotina Ehrh.) invasiveness. Acta Oecologica 30: 238-247.
Pairon MC, Jonard M, Jacquemart AL. 2006b. Modeling seed dispersal of black cherry, an invasive forest tree: how microsatellites may help? Canadian Journal of Forest Research 36: 1385-1394.
Pairon MC, Potter D, Jacquemart AL. 2008. Detection and characterization of genome-specific microsatellite markers in the allotetraploid Prunus serotina. Journal of the American Society for Horticultural Science 133: 390-395.
Peakall R, Smouse PE. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288-295.
Petit RJ, Hampe A. 2006. Some evolutionary consequences of being a tree. Annual Review of Ecology, Evolution, and Systematics 37: 187-214.
Petit RJ, Kremer A,Wagner DB. 1993. Finite island model for organelle and nuclear genes in plants. Heredity 71: 630-641.
Petit RJ, Bialozyt R, Garnier-Gere P, Hampe A. 2004. Ecology and genetics of tree invasions: from recent introductions to Quaternary migrations. Forest Ecology and Management 197: 117-137.
Petitpierre B, Pairon M, Broennimann O, Jacquemart AL, Guisan A, Besnard G. 2009. Plastid DNA polymorphisms in Prunus serotina var. serotina (Rosaceae), a North American tree invading Europe. European Journal of Forest Research 128: 431-436.
Pimentel D, Zuniga R, Morrison D. 2005. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52: 273-288. (Pubitemid 40307254)
Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A. 2004. GENECLASS2: a software for genetic assignment and first-generation migrant detection. Journal of Heredity 95: 536-539.
Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ. 2008. Adaptive evolution in invasive species. Trends in Plant Science 13: 288-294.
Prentis PJ, Sigg DP, Raghu S, Dhileepan K, Pavasovic A, Lowe AJ. 2009. Understanding invasion history: genetic structure and diversity of two globally invasive plants and implications for their management. Diversity and Distributions 15: 822-830.
Rousset F. 2008. GENEPOP 2007: A complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8: 103-106.
SAS Institute. 1999. SAS User's guide, version 8. Cary, NC: SAS Institute Inc.
Schlaepfer DR, Edwards PJ, Widmer A, Billeter R. 2008. Phylogeography of native ploidy levels and invasive tetraploids of Solidago gigantea. Molecular Ecology 17: 5245-5256.
Simberloff D. 2003. Confronting introduced species: a form of xenophobia? Biological Invasions 5: 179-192.
Spencer CC, Neigel JE, Leberg PL. 2000. Experimental evaluation of the usefulness of microsatellite DNA for detecting demographic bottlenecks. Molecular Ecology 9: 1517-1528.
Starfinger U. 1997. Introduction and naturalization of Prunus serotina in Central Europe. In: Brock J, Wade M, Pysek P, Green D. eds. Plant invasions: studies from North America and Europe. Leiden: Backhuys Publishers, 161-171.
Starfinger U, Kowarik I, Rode M, Schepker H. 2003. From desirable ornamental plant to pest to accepted addition to the flora? The perception of an alien tree species through centuries. Biological Invasions 5: 323-335.
Suarez AV, Tsutsui ND. 2008. The evolutionary consequences of biological invasions. Molecular Ecology 17: 351-360.
Theoharides KA, Dukes JS. 2007. Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytologist 176: 256-273.
Vanhellemont M, Verheyen K, De Keersmaeker L, Vandekerkhove K, Hermy M. 2009. Does Prunus serotina acts as an aggressive invader in areas with a low propagule pressure? Biological Invasions 11: 1451-1462.
Vanhellemont M, Wauters L, Baeten L, et al. 2010. Prunus serotina unlashed: invader dominance after 70 years of forest development. Biological Invasions 12: doi 10.1007/s10530-009-9529-x.
Verheyen K, Vanhellemont M, Stock T, Hermy M. 2007. Predicting patterns of invasion by black cherry (Prunus serotina Ehrh.) in Flanders (Belgium) and its impact on the forest understorey community. Diversity and Distributions 13: 487-497.
Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E. 1998. Quantifying threats to imperiled species in the United States. BioScience 48: 607-615.
Williams DA, Overholt WA, Cuda JP, Hughes CR. 2005. Chloroplast and microsatellite DNA diversities reveal the introduction history of Brazilian peppertree (Schinus terebinthifolius) in Florida. Molecular Ecology 14: 3643-3656.
Wilson JRU, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM. 2009. Something on the way you move: dispersal pathways affect invasion success. Trends in Ecology & Evolution 24: 136-144.
With K. 2002. The landscape ecology of invasive spread. Conservation Biology 16: 1192-1203.