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Please note: Images will appear in color online but will be printed in black and white.ArticleTitle Distinct invasion sources of common ragweed (Ambrosia artemisiifolia) in Eastern and Western EuropeArticle Sub-Title

Article CopyRight Springer Science+Business Media B.V.(This will be the copyright line in the final PDF)

Journal Name Biological Invasions

Corresponding Author Family Name GladieuxParticle

Given Name PierreSuffix

Division Laboratoire Ecologie, Systematique et Evolution

Organization Universite Paris-Sud

Address UMR8079, 91405, Orsay, France

Division

Organization CNRS

Address 91405, Orsay, France

Division

Organization AgroParisTech


Email [email protected]

Author Family Name GiraudParticle

Given Name TatianaSuffix




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Organization CNRS


Division



Email

Author Family Name KissParticle

Given Name LeventeSuffix

Division

Organization Plant Protection Institute of the Hungarian Academy of Sciences

Address H-1525 Budapest, P.O. Box 102, Budapest, Hungary

Email

Author Family Name GentonParticle

Given Name Benjamin J.Suffix




Division

Organization CNRS


Division



Email

Author Family Name JonotParticle

Given Name OdileSuffix




Division

Organization CNRS


Division



Email

Author Family Name ShykoffParticle

Given Name Jacqui A.Suffix




Division

Organization CNRS


Division



Email

ScheduleReceived 26 January 2010

Revised

Accepted 14 September 2010

Abstract The common ragweed (Ambrosia artemisiifolia L.; Asteraceae) is a North American native that is invadingEurasia. Besides its economic impact on crop yield, it presents a major health problem because of its highlyallergenic pollen. The plant was imported inadvertently to Europe in the eighteenth century and has becomeinvasive in several countries. By analyzing French and North American populations, it was previously shownthat French populations were best described as a mixture of native sources and that range expansion in Franceprobably involved sequential bottlenecks. Here, our aim was to determine whether Eastern Europeanpopulations of A. artemisiifolia originated from the previously established French populations or fromindependent trans-Atlantic colonization events. We used nuclear microsatellite markers to elucidate therelationships among populations from Eastern and Western Europe in relation to populations from a broadsurvey across the native North American range. We found that A. artemisiifolia from Eastern Europe did notoriginate from the earlier established French populations but rather represents multiple independentintroductions 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 characterizedFrench and North American populations, but analyses of population structure clearly distinguish the twoEuropean groups. This suggests separate introductions in Eastern and Western Europe as well as divergentsources for these two invasions, possibly as a result of distinct rules for trade and exchange for Eastern Europeduring most of the twentieth century.

Keywords (separated by '-') Allergenic plant - Biological invasion - Invasive species - Multiple introductions - Population structure

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Journal: 10530

Article: 9880

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ORIGINAL PAPER1

2 Distinct invasion sources of common ragweed (Ambrosia

3 artemisiifolia) in Eastern and Western Europe

4 Pierre Gladieux • Tatiana Giraud •

5 Levente Kiss • Benjamin J. Genton •

6 Odile Jonot • Jacqui A. Shykoff

7 Received: 26 January 2010 / Accepted: 14 September 20108 � Springer Science+Business Media B.V. 2010

9 Abstract The common ragweed (Ambrosia artem-

10 isiifolia L.; Asteraceae) is a North American native

11 that is invading Eurasia. Besides its economic impact

12 on crop yield, it presents a major health problem

13 because of its highly allergenic pollen. The plant was

14 imported inadvertently to Europe in the eighteenth

15 century and has become invasive in several countries.

16 By analyzing French and North American popula-

17 tions, it was previously shown that French popula-

18 tions were best described as a mixture of native

19 sources and that range expansion in France probably

20 involved sequential bottlenecks. Here, our aim was to

21 determine whether Eastern European populations of

22 A. artemisiifolia originated from the previously

23 established French populations or from independent

24trans-Atlantic colonization events. We used nuclear

25microsatellite markers to elucidate the relationships

26among populations from Eastern and Western Europe

27in relation to populations from a broad survey across

28the native North American range. We found that

29A. artemisiifolia from Eastern Europe did not orig-

30inate from the earlier established French populations

31but rather represents multiple independent introduc-

32tions from other sources, or introductions from a not

33yet identified highly diverse native population. East-

34ern European populations show comparable amounts

35of genetic variability as do previously characterized

36French and North American populations, but analyses

37of population structure clearly distinguish the two

38European groups. This suggests separate introduc-

39tions in Eastern and Western Europe as well as

40divergent sources for these two invasions, possibly as

41a result of distinct rules for trade and exchange for

42Eastern Europe during most of the twentieth century.

43Keywords Allergenic plant � Biological invasion �

44Invasive species � Multiple introductions �

45Population structure

46

47

48Introduction

49Species introductions involve demographic and

50genetic bottlenecks when colonists are few and

51represent only a subset of the genetic variation

A1 P. Gladieux (&) � T. Giraud � B. J. Genton �

A2 O. Jonot � J. A. Shykoff

A3 Laboratoire Ecologie, Systematique et Evolution,

A4 Universite Paris-Sud, UMR8079, 91405 Orsay, France

A5 e-mail: [email protected]

A6 P. Gladieux � T. Giraud � B. J. Genton �


A8 CNRS, 91405 Orsay, France

A9 P. Gladieux � T. Giraud � B. J. Genton �


A11 AgroParisTech, 91405 Orsay, France

A12 L. Kiss

A13 Plant Protection Institute of the Hungarian Academy

A14 of Sciences, H-1525 Budapest, P.O. Box 102, Budapest,

Hungary

123

Journal : Medium 10530 Dispatch : 23-9-2010 Pages : 12

Article No. : 9880 h LE h TYPESET

MS Code : BINV2030 h CP h DISK4 4

Biol Invasions

DOI 10.1007/s10530-010-9880-y

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52 available in populations in the native range (Husband

53 and Barrett 1991). However populations of introduced

54 and invasive plants do not always lose genetic

55 variation during invasion (see Bossdorf et al. 2005;

56 Dlugosch and Parker 2008; Puillandre et al. 2008 for

57 reviews). Some invasive populations originate from

58 multiple introductions, thereby amassing allelic vari-

59 ation from a broad range of different populations from

60 the native range (Bossdorf et al. 2005; Ciosi et al.

61 2008; Facon et al. 2005; Genton et al. 2005a; Hufbauer

62 and Sforza 2008; Lavergne and Molofsky 2007),

63 though multiple introductions do not always lead to an

64 increase in genetic variation (Durka et al. 2005).

65 Altogether, successful introductions, i.e. those leading

66 to naturalization and invasion of a new geographical

67 area, often appear to involve relatively small bottle-

68 necks, with the best predictor of establishment success

69 being propagule pressure, both in terms of number of

70 introductions and number of individuals released

71 (Simberloff 2009). Therefore many species that suc-

72 cessfully establish and invade are likely those that lost

73 least variation in the process, though invasions of

74 single genotypes are not unknown (Grimsby et al.

75 2007; Okada et al. 2009).

76 Invasive populations may also show altered genetic

77 structure compared to those in the native range, either

78 less, with homogenised mixes of representatives of

79 several differentiated populations (Le Roux et al.

80 2008), or more (Ciosi et al. 2008; Marrs et al. 2008),

81 with invasive populations being particular subsam-

82 ples of well mixed populations from the native range.

83 Studies that compare genetic structures of invasive

84 populations and populations in the native range can

85 help pinpoint the area of origin as well as elucidating

86 patterns of colonisation and pathways of spread (Le

87 Roux et al. 2006). Do invaders come from areas with

88 similar climatic characteristics? Have invaders fol-

89 lowed a stepping-stone from an initial unique

90 introduction (Amsellem et al. 2000)? Do newly

91 colonised populations at the front of the species

92 range originate from already established ones in the

93 invaded range (Genton et al. 2005a) or do they

94 represent independent colonization events from the

95 native range (Ciosi et al. 2008)? These questions are

96 relevant for practical purposes of risk assessment

97 and the efficacy of control measures but also will

98 provide important insights into the evolutionary

99 ecology of invasive and other species undergoing

100 range expansion.

101Here we investigate the genetic structure of

102populations of the invasive Ambrosia artemisiifolia

103L. (Asteraceae), a North American native that is

104invading Eurasia, found particularly in sunflower and

105corn fields, abandoned fields, disturbed areas and

106along roadsides (Bassett and Crompton 1975). This

107wind-pollinated monoecious annual plant is self-

108incompatible, thus showing an outcrossing mating

109system, even in colonizing populations (Friedman

110and Barrett 2008). During the past 15–20 years, the

111spread of common ragweed has become a major

112problem in some parts of France and a number of

113Eastern European countries, including Hungary,

114Croatia, Ukraine, Russia and Serbia (Kiss and Beres

1152007).

116The first Eurasian records of this species are from a

117herbarium specimen from Central France from 1863,

118and the species showed a gradual but continuous

119spread in this region, demonstrating continuous

120presence in the area of Lyon, France, which seems

121to be the focus of its current French distribution

122(Chauvel et al. 2006). The earliest recorded Eastern

123European records of this plant appear first 40 years

124later from Orsova, Romania, and about 20 years after

125that from the south-western part of Hungary (Kazinczi

126et al. 2008; Makra et al. 2005; Csontos et al. 2010). It

127is therefore possible that Eastern Europe was colo-

128nized from the already established French invasive

129populations, though an independent introduction from

130the native range of this species is also possible. Over

131the last 20 years additional populations have appeared

132and become established in the intervening areas of

133Switzerland, northern Italy and Austria, but these are

134thought to represent recent range expansion from one

135or the other long established centres of spread. The

136conquest of Eastern Europe, however, has been

137dramatically more rapid and complete than that of

138the West, with a larger occupied range and far denser

139populations, as revealed by pattern of airborne pollen

140density across Europe (Fig. 1; Makra et al. 2004;

141Makra et al. 2005). This then poses the question of

142whether the Eastern European invasion is caused by

143other more competitive genotypes or those better

144adapted to the conditions in Eastern Europe.

145Here we extend our previous investigation of the

146population structure of invasive populations in France

147(Genton et al. 2005a). We have previously shown

148that the French invasive populations of A. artemis-

149iifolia originated from a mixture of sources. French

P. Gladieux et al.

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150 populations showed even higher within-population

151 diversity than did native North American populations,

152 they contained mixes of rare alleles found in distinct

153 North American populations and assignment tests

154 failed to identify a single area of origin in North

155 America (Genton et al. 2005a). Chun et al. (2010)

156 showed that historical French populations, recon-

157 structed from herbarium specimens dating from the

158 late nineteenth to early twentieth century, appeared to

159 harbour lower allelic and genetic diversity than recent

160 populations. Altogether, this suggests that ragweed

161 seeds were introduced repeatedly, or as mixtures,

162 from different parts of North America to France.

163 However within France, ragweed populations at the

164 front of the invasion, far from the original area of

165 introduction near Lyon, France, are genetically less

166 diverse, indicating that ragweed range expansion

167 probably involves sequential bottlenecks from the

168 primary introduction rather than subsequent new

169 introductions (Genton et al. 2005a). Here we test

170 whether Eastern European ragweed populations could

171 have been founded from French populations involving

172 sequential bottlenecks or whether Eastern European

173 ragweed populations were introduced independently.

174 We analysed Eastern European populations of this

175 invasive plant using microsatellites to address the

176 following questions: (1) Were Eastern European

177 populations founded from French populations? Are

178 they characterised by a subset of the allelic diversity

179 already found in the French populations? (2) Did they

180 come independently from similar sources in North

181 America, characterized by a similar amount of vari-

182 ation and similar allelic profiles, or from elsewhere?

183 Here we compare our new data from Eastern European

184ragweed populations with data previously presented in

185Genton et al. (2005a).

186Methods

187Sampling and DNA extractions

188Ragweed populations were sampled in six localities

189in Eastern Europe (Fig. 1; Table 1). In each sampling

190site leaves were collected from 30 individual plants at

191approximately 1.5 m spacing, according to the sam-

192pling method of Genton et al. (2005a), air-dried, and

193kept as herbarium materials. DNA was extracted

194from 10 to 15 mg dried leaf tissue using DNeasy

195Plant Mini Kits (QIAGEN) and then stored at -20�C.

196Genetic data for a total of 12 North American and 10

197French ragweed populations, obtained in a previously

198published study (Genton et al. 2005a), were also included

199in this work. The American populations sampled were

200located east of the Rocky Mountains, mostly from the

201East Coast and Great Lakes region of the USA and

202Canada, areas with a long history of commercial

203exchange with Western Europe. The French ragweed

204populations sampled were located in the Rhone-Alpes,

205Provence-Alpes-Cote-d’Azur and Bourgogne regions.

206The designations, locations and other data of the

207American and French ragweed populations included in

208this study are given in Genton et al. (2005a).

209Microsatellite genotyping and analyses

210We used the five nuclear microsatellite loci recently

211developed for A. artemisiifolia (Genton et al. 2005b).

A B

Fig. 1 Annual counts of Ambrosia artemisiifolia pollen grains

(a) averaged over 1995–2007 (reproduced with permission

from Regula Gehrig, MeteoSwiss; source: EAN European

Aeroallergen Network) as a proxy for the local distribution and

abundance of this plant; sampling sites of A. artemisiifolia

(b) in Western Europe (previously presented in Genton et al.

2005a) and Eastern Europe (new to this study). F France; HU

Hungary; RO Romania; UA Ukraine; SCG Serbia and

Montenegro

Distinct invasion sources of common ragweed

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Table

1Origin,populationstructure

andmeasuresofgenetic

variationoftheEastern

Europeanragweedpopulationsanalysedin

thisstudy

Populations

Location

Latitude

Longitude

Aa

ARb

RSc

HEd

HOe

FISf

HW

testg

FST

h

HU-Bi

Biatorbagy,Hungary

47�460N

18�810E

10.6

8.2

9.7

0.80

0.19

0.76

***

HU-Bu

Budaors,Hungary

47�450N

18�960E

10.4

7.8

9.1

0.73

0.24

0.68

***

HU-K

Keszthely,Hungary

46�760N

17�250E

9.0

5.2

8.4

0.78

0.18

0.79

***

RO-E

Elesd,Romania

47�060N

22�410E

8.0

4.4

7.5

0.70

0.23

0.70

***

UA-K

Kiev,Ukraine

50�430N

30�510E

5.8

2.8

5.3

0.60

0.25

0.47

***

SCG-Z

Zenta,Serbia

andMontenegro

45�920N

20�070E

8.8

4.8

8.5

0.78

0.20

0.75

***

Mean±

SD

8.8

±1.7

5.5

±2.1

8.1

±1.5

0.73±

0.07

0.21±

0.03

0.69±

0.12

0.08±

0.05

aMeannumber

ofallelesper

locus

bMeannumber

ofrare

allelesper

locus

cAllelic

richness

dExpectedheterozygosity

eObserved

heterozygosity

fInbreedingcoefficient

gResultsofexactHardy-W

einbergtests

hWeirandCockerham

’sF-statisticsestimates

P. Gladieux et al.

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212 Polymerase chain reaction and allele resolution were

213 carried out according to Genton et al. (2005a).

214 Several samples from the study by Genton et al.

215 (2005a), having the full range of alleles previously

216 identified, were run on each gel to score allele sizes

217 consistently between the previous and the present

218 studies. New primers were designed for the locus

219 Amb15 because of difficulties in amplification using

220 the previous primers from Genton et al. (2005b). The

221 new primer pair (Amb15-F2: aatccattccccacatcctt and

222 Amb15-R2: gaggggttgggtcgagtaag) gave amplifica-

223 tions in a higher number of individuals.

224 Using FSTAT version 2.9.3.2 (Goudet 1995), we

225 estimated (1) the means ± SD over all loci of the

226 following genetic variation indices: allelic richness

227 (RS; El Mousadik and Petit 1996), observed hetero-

228 zygosities and expected heterozygosities, respec-

229 tively HO and HE (Nei 1987; the latter also referred

230 to as Nei’s gene diversity); (2) F-statistics (Weir and

231 Cockerham 1984). Deviations from Hardy-Weinberg

232 proportions were assessed using FSTAT (Goudet

233 1995) with P-values being corrected for table-wide

234 significance levels (a = 0.05) using the sequential

235 Bonferroni method (Rice 1989). We also computed

236 the means over all loci of the number of alleles

237 (A) and the number of rare alleles (AR), i.e. with

238 allelic frequencies below 0.1. Finally, we tested for

239 linkage disequilibria using Fisher exact tests in

240 FSTAT (Goudet 1995) with P-values being corrected

241 for table-wide significance levels (a = 0.05) using

242 the sequential Bonferroni method (Rice 1989).

243 Genetic distances among populationsweremeasured

244 with the POPULATIONS program (http://bioinformatics.

245 org/*tryphon/populations/), using the chord distance

246 of Cavalli-Sforza and Edwards (1967). The distance

247 matrix was submitted to a Principal Coordinate

248 Analysis (PCoA), as implemented in GENALEX (Peakall

249 and Smouse 2006).

250 Comparison of genetic diversity and population

251 differentiation

252 To compare the values of within-population genetic

253 variation indices (A, AR, HE, FIS) and population

254 differentiation (FST) between the native range, France

255 and Eastern Europe, we used FSTAT. For each index

256 FSTAT computes the average over loci and popula-

257 tions for each group and then the squared difference

258 between these two averages. Significance of this

259difference is then assessed using a permutation test:

260the whole sample is allocated at random to the three

261groups, keeping the number of populations constant

262in each group.

263To compare the means of numbers of null geno-

264types among French, North American and Eastern

265European populations, pairwise mean comparisons

266were carried out using Student t-tests with the soft-

267ware JMP (SAS Institute Inc, SAS Campus Drive,

268Cary NC). The locus Amb15 was not included in

269these comparisons because different primer pairs had

270been used for genotyping Eastern European popula-

271tions (see above), precisely because the number of

272null alleles was high using the first primer pair.

273Amb15 was however used in all other analyses as we

274could make the correspondence between the same

275alleles amplified using the two different primer pairs.

276Analyses of molecular variance (AMOVAs) were

277performed using ARLEQUIN version 3.0 (Excoffier

278et al. 2005), with variation being partitioned within-

279and among-populations, and distance among geno-

280types calculated as the number of different alleles.

281This method was preferred over the method that uses

282the squared number of repeat difference between

283genotypes to calculate distances (Slatkin 1995) to

284avoid biases due to departures from the stepwise

285model of microsatellite evolution.

286Population subdivision and assignment tests

287We used STRUCTURE version 2.3.1 (Pritchard et al.

2882000) to identify the source populations of Eastern

289European invasive populations and to examine pop-

290ulation subdivision. The model implemented allowed

291information on sampling location (LocPrior model;

292Hubisz et al. 2009), admixture, and correlation in

293allele frequencies (Falush et al. 2003). Burn-in length

294was set at 150,000 iterations followed by a run phase

295of 750,000 iterations. We employed a hierarchical

296approach to detect all layers of population structure

297(Coulon et al. 2008; Evanno et al. 2005; Rollins et al.

2982009). Analyses were first conducted on the total

299dataset, using the region of origin of individuals as

300prior information to assist clustering. We then

301repeated analyses on each of the K groups inferred

302in the previous step, using the population of origin of

303individuals as prior information. We set the number

304of populations (K) from 1 to 8, but not higher, as the

305results for the first level of analysis showed that


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306 setting K values from 3 to 8 already led to clusters

307 without geographical coherence and with admixed

308 ancestry, which is typical of too high a cluster

309 number. For all levels of analysis, we performed 30

310 independent runs for each value of K. Results were

311 analysed with CLUMPP version 1.1.2 (Jakobsson and

312 Rosenberg 2007) using the Greedy algorithm for

313 1 B KB4 and the Fast-Greedy algorithm for K[ 4,

314 with random input order and 10,000 permutations.

315 Distinct modes among runs were identified by finding

316 sets of runs with less than 85% similarity in the G0

317 pairwise similarity matrix (‘modes’ refer to distinct

318 clustering solutions represented within the set of

319 replicate cluster analyses). CLUMPP was used again to

320 align outputs of the runs with the same clustering

321 mode and to provide average cluster membership

322 coefficients across aligned runs. The optimal K value

323 was determined using the method of Evanno et al.

324 (2005) based on the rate of change in the log

325 probability of data between successive K values.

326 Distribution of private alleles

327 Because rare alleles can be powerful in identifying

328 sources and routes of migrations, we also examined the

329 distribution of private alleles, i.e. alleles unique to a

330 single population or combination of populations.

331 We used the program ADZE (Szpiech et al. 2008),

332 which implements a rarefaction procedure for count-

333 ing alleles private to populations while adjusting for

334 differences in sample size across populations. We

335 calculated the mean number of private alleles, aver-

336 aging across loci, for each of three regional group-

337 ings of populations (North America, France, Eastern

338 Europe) and each of three combined sets of two

339 regional groupings. Calculations were performed using

340 a standardized sample size of n = 252 (126 individ-

341 uals times two chromosomes), corresponding to the

342 smallest number of observations per regional grouping

343 under consideration.

344 Results

345 Genetic diversity, F-statistics and Hardy

346 Weinberg equilibrium

347 The five nuclear microsatellite loci had a total of 95

348 alleles in the six Eastern European populations

349analysed. Diversity indices, F-statistics estimates

350(Weir and Cockerham 1984) and results of exact

351Hardy-Weinberg tests (Guo and Thompson 1992) are

352presented in Table 1 for Eastern European popula-

353tions and can be found in Genton et al. (2005a) for

354North American and French populations. Significant

355heterozygote deficiencies were detected in all popu-

356lations, yielding significant positive FIS values. These

357values were greater in Eastern European populations

358than in North American ones and in France (P\ 0.01,

359Fig. 2). Tests for linkage disequilibria were all non-

360significant. Genetic variation, measured as number of

361alleles, number of rare alleles or expected heterozy-

362gosity, was not significantly different among the

363native range, France and Eastern Europe (Fig. 3).

364To assess whether the higher level of FIS in Eastern

365European populations could be due to the presence of

366more null alleles, we compared the proportion of null

367genotypes (i.e. giving no amplification in one or a few

368loci but giving bands in other loci; thus being assumed

North America France Eastern Europe

0.8

0.6

0.4

0.2

0.0

FIS

Fig. 2 Mean of the inbreeding coefficient (FIS) in North

American, French and Eastern European populations of

Ambrosia artemisiifolia. Error bars represent standard error

across loci

1.0

0.8

0.6

0.2

0.0

10

8

6

4

2

0 North

AmericaFrance Eastern

Europe

0.4

12 A AR

HE

Fig. 3 Mean of allelic richness (A), number of rare alleles

(AR), and of the expected heterozygosity (HE), in North

American, French and Eastern European populations of

Ambrosia artemisiifolia. Error bars represent standard error

across loci

P. Gladieux et al.

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369 to be homozygotes for null alleles) among Eastern

370 European, French and North American populations.

371 Eastern European populations had a significant higher

372 mean proportion of null genotypes (mean ± SE =

373 15.9 ± 2.0), than French (mean ± SE = 8.5 ± 1.5)

374 or North American (mean ± SE = 10.2 ± 1.4) pop-

375 ulations, which did not differ significantly from each

376 other.

377 Comparison of variability distribution

378 among populations between North America,

379 Western Europe and Eastern Europe

380 We first performed an analysis of molecular variance

381 (AMOVA) on Eastern European populations to

382 divide the genetic variance into within- and among

383 population components. Results indicated that most

384 genetic variation in Eastern Europe was within, rather

385 than among, populations (Table 2), as was the case in

386 the native range and in France (Genton et al. 2005a).

387 The percentage of variation attributed to among-

388 population differentiation was 8.79% in Eastern

389 Europe (Table 2), i.e. higher than in France (4.81%)

390 and in North America (6.39%).

391 Distribution of private alleles

392 The number of private alleles was calculated for

393 regional groupings of populations and their combina-

394 tions (Fig. 4). At the scale of regions, estimates were

395 higher in Eastern Europe (mean ± SE = 5.29 ±

396 2.50) than in France (mean ± SE = 1.84 ± 0.95)

397and North America (mean ± SE = 0.73 ± 0.51). In

398analyses on combinations of regions, private allele

399richness was higher in the North America/France

400combination (mean ± SE = 4.14 ± 2.03) than in the

401North America/Eastern Europe (mean ± SE = 1.45

402± 0.72) and France/Eastern Europe (mean ± SE =

4031.28 ± 0.72) combinations. The fact that the propor-

404tion of private alleles is the highest in North America

405and France when these regions are combined while it

406is the lowest when regions are analysed individu-

407ally suggests that North American and European

408populations are more similar to each other in terms of

409allelic profiles than they are to Eastern European

410populations.

411Genetic relationships among populations

412Chord genetic distances were calculated among pop-

413ulations, and the resulting distance matrix was sub-

414jected to PCoA (Fig. 5). The first principal coordinate

415(explaining 41.7% of total variation) partitioned

416populations into two groups with populations from

417France and North America in one group, and popu-

418lations from Eastern Europe in the other. The second

419and third principal coordinates (explaining 15.1 and

42012.9% of total variation, respectively) did not reveal

421any obvious further correspondence between genetic

422distances and the geographical origin of populations.

423The only remarkable feature that emerges from the

424decomposition of variance along these axes is that the

425third coordinate separated the Ukrainian population

426from other Eastern European populations.

Table 2 Results of the

analyses of molecular

variance (AMOVA)

Distance among multilocus

genotypes is computed as

the number of different

alleles

Source of variation d. f. Sum of squares Percentage

of variation

P-value

Eastern Europe

Among populations 5 32 8.79 \10-6

Within Populations 350 328 91.21 \10-6

Total 355 360

North America



Total 559 859

France



Total 497 739


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427 In STRUCTURE analyses, the modal value of the

428 DK statistic was found at K = 2, with North American

429 and French populations in one cluster, and Eastern

430 European populations in another (Fig. 6). Only a few

431 individuals contradicted this pattern of clustering and

432 had mixed membership in the two clusters or were not

433 assigned to the cluster containing individuals from the

434 region from which they were sampled. Generally,

435 levels above K = 2 produced no new clusters corre-

436 sponding to geographical structuring among North

437 American and French genotypes, but instead intro-

438 duced some heterogeneity in membership coefficients.

439 Within Eastern European populations, no particular

440geographical pattern of clustering was detected, except

441that all individuals from Ukraine had consistently

442high membership in the same cluster and ended up

443individualizing in a separate cluster when K reached 6

444(not shown). In the next level of analyses, we searched

445for possible additional layers of structure by repeat-

446ing analyses on both of the K = 2 groups inferred in

447the previous step, using ‘populations’—and not

448‘regions’—as prior information to assist clustering.

449In analyses of Eastern European samples, the modal

450value of DK was found at K = 2, with a secondary

451peak at K = 5. At K = 2, one cluster corresponded to

452individuals from Ukraine, and the other clusters

453grouped individuals from all other populations (not

454shown). At K = 5, individuals from populations from

455Serbia-Montenegro, Romania, and Ukraine (i.e. SCG-

456Z, RO-E, UA-K) had high membership proportions in

457separate clusters, individuals from Hungarian popula-

458tions HU-Bi and HU-Bu had high membership in the

459same cluster, and individuals from Hungarian popu-

460lation HU-K had roughly equal membership in multi-

461ple clusters (Fig. 6). In analyses of French and North

462American samples, the modal value of DK was

463observed for K = 6, but neither K = 6 nor any other

464value of K yielded an obvious pattern of geographical

465clustering (Fig. 6). In support of a lack of population

466structure, average log posterior probabilities of data

467forK = 1 andK = 2 were very close (on average over

468runs from the main mode: Ln(P) = -10,512.2 and

469Ln(P) = -10,512.9 for K = 1 and K = 2, respec-

470tively), suggesting that a model with multiple popu-

471lations is not significantly better than a model with a

472single population to represent data from French and

473North American samples.

474Discussion

475Invasion history of European ragweed

476Overall population genetic variability of A. artemis-

477iifolia, measured as expected heterozygosity or allelic

478richness, was similar in North America, Eastern and

479Western Europe. We found no evidence for the loss of

480genetic variation via sequential bottlenecks observed

481for other invasions (e.g. Amsellem et al. 2000; Henry

482et al. 2009; Puillandre et al. 2008). Therefore, in

483contrast to what was found in France, where popula-

484tions at the current invasion front in the Bourgogne

0

1

2

3

4

5

6

7

8


Me

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va

te a

llele

s

0

1

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3

4

5

6

7

North America and France

North America and Eastern Europe

France and Eastern Europe

Me

an

nu

mb

er

of

pri

va

te a

llele

s

A

B

Fig. 4 Mean number of alleles private to regional groupings

of populations (a) and their combinations (b). Estimates are

based on a standardized sample size of 252 chromosomes (126

plants times two chromosomes). Error bars represent standard

error across loci

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-0.06 -0.04 -0.02 0.00 0.02 0.04 0.06 0.08

-0.0

4-0

.02

0.0

00

.02

0.0

40

.06

First Principal Coordinate

Second P

rincip

al C

oord

inate

NA-AL

NA-CO

NA-IL

NA-MO

NA-NY

NA-OH

NA-ON1

NA-ON2

NA-QC

NA-SC

NA-TN

NA-WI

F-BOURG1

F-BOURG2

F-PACA1

F-PACA2

F-PACA3

F-RA1

F-RA2

F-RA3F-RA4

F-RA5HU-Bi

HU-K

SCG-Z

RO-E

UA-K

HU-Bu

-0.06 -0.04 -0.02 0.00 0.02 0.04 0.06 0.08

-0.1

0-0

.05

0.0

00

.05

0.1

00

.15

0.2

0

First Principal Coordinate

Third P

rincip

al C

oord

inate

NA-AL

NA-CO

NA-IL

NA-MONA-NY

NA-OH

NA-ON1

NA-ON2

NA-QC

NA-SC

NA-TN

NA-WI

F-BOURG1

F-BOURG2

F-PACA1

F-PACA2

F-PACA3

F-RA1

F-RA2

F-RA3

F-RA4

F-RA5

HU-K

SCG-Z

RO-E

UA-K

HU-Bu

Fig. 5 Principal coordinate analysis of chord distance among

populations. The first, second and third principal coordinates

account for 41.7, 15.1 and 12.9% of the variation, respectively.

NA North America; F France; HU Hungary; RO Romania; UA

Ukraine; SCG Serbia and Montenegro

NA

-AL

NA

-CO

NA

-IL

NA

-MO

NA

-NY

NA

-OH

NA

-ON

1

NA

-ON

2

NA

-QC

NA

-SC

NA

-TN

NA

-WI

F-B

OU

RG

1

F-B

OU

RG

2

F-P

AC

A1

F-P

AC

A2

F

-PA

CA

3

F-R

A1

F-R

A2

F-R

A3

F-R

A4

F-R

A5

HU

-Bi

HU

-K

SC

G-Z

RO

-E

UA

-K

HU

-Bu


NA

-AL

NA

-CO

NA

-IL

NA

-MO

NA

-NY

NA

-OH

NA

-ON

1

NA

-ON

2

NA

-QC

NA

-SC

NA

-TN

NA

-WI

F-B

OU

RG

1

F-B

OU

RG

2

F-P

AC

A1

F-P

AC

A2

F

-PA

CA

3

F-R

A1

F-R

A2

F-R

A3

F-R

A4

F-R

A5

HU

-Bi

HU

-K

SC

G-Z

RO

-E

UA

-K

HU

-Bu

Fig. 6 Population structure of Ambrosia artemisiifolia inferred

using the STRUCTURE program. The number of predefined

clusters was K = 2 for the analysis of the total dataset.

Subsequent hierarchical analyses (indicated by arrows)

assumed K = 6 clusters for French and North American

samples, and K = 5 clusters for Eastern European samples.

Each individual is represented by a thin vertical line that is

partitioned into two components according to the inferred

membership in the two genetic clusters. Black lines separate

genotypes from distinct populations. Vertical axis represents

the membership proportions to the K clusters assumed, obtained

using the CLUMPP program by averaging memberships across all

runs corresponding to the main clustering mode. NA North

America; F France; HU Hungary; RO Romania; UA Ukraine;

SCG Serbia and Montenegro


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485 and PACA regions originate from the original popu-

486 lations of introduction in the East of Lyon (Genton

487 et al. 2005a), Eastern European populations appear

488 not to have originated from colonists from these older

489 established French populations. Nor did Eastern

490 European populations originate from a single source

491 among the native populations sampled. The high

492 genetic variability observed in Eastern European

493 populations suggests either multiple sources of intro-

494 duction, or introduction from a highly diverse source

495 that we failed to sample (Muirhead et al. 2008).

496 Multiple introductions have been inferred for many

497 plant introductions studied to date (Bossdorf et al.

498 2005; Dlugosch and Parker 2008; Hufbauer and

499 Sforza 2008), including the introduction of this same

500 species to Western Europe (Genton et al. 2005a).

501 Analyses of the distribution of genetic variability

502 brought additional insights to the history of the

503 ragweed invasion. AMOVA, PCoA and STRUCTURE

504 analyses revealed contrasted patterns of population

505 structure in the introduced range: while populations

506 from France appeared less differentiated than popu-

507 lations from the native range, a higher level of

508 geographical structure was observed among Eastern

509 European populations. These differences may be

510 related to the population structure in the native range

511 and the genetic makeup of founding propagules. The

512 shallow population structure of introduced French

513 populations suggests that they were all founded by

514 genetically similar sources, either by a single intro-

515 duction of mixed propagules followed by dissemina-

516 tion, or by multiple introductions coming from similar

517 mixtures of sources (Genton et al. 2005a). Such a

518 transformation of among population genetic variation

519 into within population genetic variation due to several

520 introductions from similar multiple sources has been

521 reported in several other cases of biological invasions

522 with multiple introductions (e.g. Kolbe et al. 2004;

523 Lavergne and Molofsky 2007). By contrast, the higher

524 population structure observed in Eastern European

525 populations of A. artemisiifolia may correspond to the

526 introduction of genetically differentiated propagules

527 resulting from independent samplings either from

528 similar highly diverse populations or from separate

529 differentiated populations. Such a pattern of higher

530 population structure in the invasive range has been

531 reported for several organisms (e.g. Ciosi et al. 2008;

532 Marrs et al. 2008), though it seems less frequent than

533 the opposite pattern (Bossdorf et al. 2005).

534Different origins and structure for Eastern

535and Western European invasive ragweed

536populations

537Several lines of evidence indicate that the Eastern and

538Western European invasive ragweed populations orig-

539inate, at least in part, from separate mixes of different

540native populations. Analyses of population structure

541revealed that Western and Eastern European popula-

542tions were differentiated, and French populations of

543A. artemisiifolia appeared genetically much more

544similar to the sampled North American populations

545than did Eastern European populations, as indicated by

546the number of alleles private to the combination of

547French and North American populations, patterns of

548genetic distance among populations and assignment

549tests. The higher FIS values in Eastern Europe further

550support their distinctness. The plant is self incompat-

551ible and outcrossing in its native area (Friedman and

552Barrett 2008) and we have no indication of a break-

553down of self incompatibility and shift in reproductive

554mode in Eastern Europe. Furthermore we found a

555higher proportion of null genotypes in these popula-

556tions, so the significant FIS values point strongly to the

557existence of null alleles caused by mutations in the

558flanking regions of themicrosatellites that are expected

559to evolve more slowly than repeat number, implying a

560longer history of independent evolution. Because the

561microsatellite markers were cloned from French pop-

562ulations (Genton et al. 2005b), genetically distant

563populations should harbour more null alleles. The fact

564that more null alleles seem to be present in Eastern

565Europe than in North America and France thus further

566indicate that Eastern European populations are genet-

567ically distinct from both the sampled North American

568and French ones. We also note that a scenario in which

569Eastern European populations originate, at least in part,

570from different native populations than those analysed

571by Genton et al. (2005a) is likely given the geopolitics

572of the latter half of the twentieth century that facilitated

573neither commercial nor human exchanges between

574Eastern Europe andNorthAmerica orWestern Europe.

575Conclusion

576Introductions from multiple sources and separate

577introductions to different sites have previously been

578reported in the literature (see introduction), but the

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579 pattern found for A. artemisiifolia is rarer, with two

580 separate introductions on the same continent, different

581 levels of population structure in different parts of the

582 invasive range, and introductions from different but

583 multiple sources each (see another example with the

584 invasive grass Bromus tectorum (Novak and Mack

585 2001). This results in a similar level of variability in

586 introduced and native populations, possibly yielding a

587 considerable potential for rapid evolution in invasive

588 populations. Nonetheless, we have little evidence for

589 post-introduction adaptive evolution in this species.

590 Genton et al. (2005c) investigated changes of intro-

591 duced populations compared to native ones, but found

592 no evidence for any evolutionary loss of defence

593 against natural enemies despite strong enemy release

594 in Europe, though there may have been an evolution-

595 ary change in the phenology of introduced popula-

596 tions, reflecting adaptation to higher latitudes in the

597 introduced range.

598 Another remarkable aspect of the invasion of

599 A. artemisiifolia in Europe is the possible role of the

600 political context in the genetic structure and diversity

601 on the invaded range. The wars and their consequences

602 may indeed have set the stage for the introduction of

603 genetically different sources in Western and Eastern

604 Europe. The locations of the populations that gave rise

605 to the Eastern populations remain to be identified.

606 Acknowledgments We are grateful to Tunde Jankovics and607 Vera Hayova for their help in collecting ragweed samples, to608 Bernard Clot from Meteoswiss, and we thank anonymous609 reviewers for their suggestions. TG acknowledges a grant ANR610 07-BDIV-003. A part of this work was supported by grants of611 the Hungarian Scientific Research Fund (OTKA T046841 and612 IN67377).

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