Abstract
The common ragweed (Ambrosia artemisiifolia L.; Asteraceae) is a North American native that is invading Eurasia. Besides its economic impact on crop yield, it presents a major health problem because of its highly allergenic pollen. The plant was imported inadvertently to Europe in the eighteenth century and has become invasive in several countries. By analyzing French and North American populations, it was previously shown that French populations were best described as a mixture of native sources and that range expansion in France probably involved sequential bottlenecks. Here, our aim was to determine whether Eastern European populations of A. artemisiifolia originated from the previously established French populations or from independent trans-Atlantic colonization events. We used nuclear microsatellite markers to elucidate the relationships among populations from Eastern and Western Europe in relation to populations from a broad survey across the native North American range. We found that A. artemisiifolia from Eastern Europe did not originate from the earlier established French populations but rather represents multiple independent introductions from other sources, or introductions from a not yet identified highly diverse native population. Eastern European populations show comparable amounts of genetic variability as do previously characterized French and North American populations, but analyses of population structure clearly distinguish the two European groups. This suggests separate introductions in Eastern and Western Europe as well as divergent sources for these two invasions, possibly as a result of distinct rules for trade and exchange for Eastern Europe during most of the twentieth century.
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References
Amsellem L, Noyer JL, Le Bourgeois T, Hossaert-McKey M (2000) Comparison of genetic diversity of the invasive weed Rubus alceifolius Poir. (Rosaceae) in its native range and in areas of introduction, using amplified fragment length polymorphism (AFLP) markers. Mol Ecol 9:443–455
Bassett IJ, Crompton CW (1975) The biology of Canadian weeds. 11. Ambrosia artemisiifolia L. and A. psilostachya DC. Can J Plant Sci 55:463–476
Bossdorf O, Auge H, Lafuma L, Rogers W, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11
Cavalli-Sforza L, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 32:550–570
Chauvel B, Dessaint F, Cardinal-Legrand C, Bretagnolle F (2006) The historical spread of Ambrosia artemisiifolia L. in France from herbarium records. J Biogeogr 33:665–673
Chun YJ, Fumanal B, Laitung B, Bretagnolle F (2010) Gene flow and population admixture as the primary post-invasion processes in common ragweed (Ambrosia artemisiifolia) populations in France. New Phytol 185:1100–1107
Ciosi M, Miller NJ, Kim KS, Giordano R, Estoup A, Guillemaud T (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17:3614–3627
Coulon A, Fitzpatrick JW, Bowman R, Stith BM, Makarewich CA, Stenzler LM, Lovette IJ (2008) Congruent population structure inferred from dispersal behaviour and intensive genetic surveys of the threatened Florida scrub-jay (Aphelocoma coerulescens). Mol Ecol 17:1685–1701
Csontos P, Vitalos M, Barina Z, Kiss L (2010) Early distribution and spread of Ambrosia artemisiifolia in Central and Eastern Europe. Bot Helv 120:75–78
Dlugosch KM, Parker IM (2008) Founding events in species invasion: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449
Durka W, Bossdorf O, Prati D, Auge H (2005) Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol Ecol 14:1697–1706
El Mousadik A, Petit R (1996) High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa (L.) Skeels) endemic to Morocco. Theor Appl Genet 92:832–839
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Facon B, Jarne P, Pointier J-P, David P (2005) Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance. J Evol Biol 18:524–535
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164:1567–1587
Friedman J, Barrett SCH (2008) High outcrossing in the annual colonizing species Ambrosia artemisiifolia (Asteraceae). Ann Bot 101:1303–1309
Genton BJ, Shykoff JA, Giraud T (2005a) High genetic diversity in French invasive populations of common ragweed Ambrosia artemisiifolia as a consequence of multiple sources of introduction. Mol Ecol 14:4275–4285
Genton BJ, Jonot O, Thévenet D, Fournier E, Blatrix R, Vautrin D, Solignac M, Giraud T (2005b) Isolation of five polymorphic microsatellite loci, using an enrichment protocol, in the invasive weed Ambrosia artemisiifolia (Asteraceae). Mol Ecol Notes 5:381–383
Genton BJ, Kotanen PM, Cheptou P-O, Adolphe C, Shykoff JA (2005c) Enemy release but no evolutionary loss of defence in a plant invasion: an intercontinental reciprocal experiment. Oecologia 146:404–414
Goudet J (1995) Fstat (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Grimsby JL, Tsirelson D, Gammon MA, Kesseli R (2007) Genetic diversity and clonal vs. sexual reproduction in Fallopia spp. (Polygonaceae). Am J Bot 94:957–964
Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics 48:361–372
Henry P, Le Lay G, Goudet J, Guisan A, Jahodová S, Besnard G (2009) Reduced genetic diversity, increased isolation and multiple introductions of invasive giant hogweed in the western Swiss Alps. Mol Ecol 18:2819–2831
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332
Hufbauer RA, Sforza R (2008) Multiple introductions of two invasive Centaurea taxa inferred from cpDNA haplotypes. Divers Distrib 14:252–261
Husband BC, Barrett SCH (1991) Colonization history and population genetic structure of Eichhornia paniculata in Jamaica. Heredity 66:287–296
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806
Kazinczi G, Béres I, Novák R, Bíró K, Pathy Z (2008) Common ragweed (Ambrosia artemisiifolia): A review with special regards to the results in Hungary. I. Taxonomy, origin and distribution, morphology, life cycle and reproduction strategy. Herbologia 9:55–91
Kiss L, Béres I (2007) Anthropogenic factors behind the recent population expansion of common ragweed (Ambrosia artemisiifolia L.) in Eastern Europe: is there a correlation with political transitions? J Biogeogr 33:2156–2157
Kolbe JJ, Glor RE, Schettino LRG, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181
Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:3883–3888
Le Roux JJ, Wieczorek AM, Ramadan MM, Tran CT (2006) Resolving the native provenance of invasive fireweed (Senecio madagascariensis Poir.) in the Hawaiian Islands as inferred from phylogenetic analysis. Divers Distrib 12:694–702
Le Roux JJ, Wieczorek AM, Meyer J-Y (2008) Genetic diversity and structure of the invasive tree Miconia calvescens in Pacific Islands. Divers Distrib 14:935–948
Makra L, Juhász M, Borsos E, Béczi R (2004) Meteorological variables connected with airborne ragweed pollen in Southern Hungary. Int J Biometeorol 49:37–47
Makra L, Juhász M, Béczi R, Borsos E (2005) The history and impacts of airborne Ambrosia (Asteraceae) pollen in Hungary. Grana 44:57–64
Marrs RA, Sforza R, Hufbauer RA (2008) When invasion increases population genetic structure: a study with Centaurea diffusa. Biol Invasions 10:561–572
Muirhead JR, Gray DK, Kelly DW, Ellis SM, Heath DD, Macisaac HJ (2008) Identifying the source of species invasions: sampling intensity vs. genetic diversity. Mol Ecol 17:1020–1035
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
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. Divers Distrib 15:148–157
Peakall ROD, Smouse PE (2006) Genalex 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Puillandre N, Dupas S, Dangles O, Zeddam J-L, Capdevielle-Dulac C, Barbin K, Torres-Leguizamon M, Silvain J-F (2008) Genetic bottleneck in invasive species: the potato tuber moth adds to the list. Biol Invasions 10:319–333
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Rollins LA, Woolnough AP, Wilton AN, Sinclair R, Sherwin WB (2009) Invasive species can’t cover their tracks: using microsatellites to assist management of starling (Sturnus vulgaris) populations in Western Australia. Mol Ecol 18:1560–1573
Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102
Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequency. Genetics 139:457–462
Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Acknowledgments
We are grateful to Tünde Jankovics and Vera Hayova for their help in collecting ragweed samples, to Bernard Clot from MeteoSwiss, and we thank anonymous reviewers for their suggestions. TG acknowledges a grant ANR 07-BDIV-003 and LK an Invited Professorship from University Paris-Sud. A part of this work was supported by grants of the Hungarian Scientific Research Fund (OTKA T046841 and IN67377).
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Gladieux, P., Giraud, T., Kiss, L. et al. Distinct invasion sources of common ragweed (Ambrosia artemisiifolia) in Eastern and Western Europe. Biol Invasions 13, 933–944 (2011). https://doi.org/10.1007/s10530-010-9880-y
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DOI: https://doi.org/10.1007/s10530-010-9880-y