Abstract
Biological invasions offer excellent systems to study the evolutionary processes involved in introductions of species to new ranges. Molecular markers can reveal invasion histories and the effects of introductions on amounts and structuring of genetic variation. We used five polymorphic microsatellite loci to elucidate genetic diversity and population structure between native range and introduced range populations of a prominent North American rangeland weed, Centaurea diffusa (Asteraceae). We found that the total number of alleles and the number of private alleles was slightly higher in the native Eurasian range, and that allelic richness did not differ between the ranges, indicating overall levels of diversity were similar in Eurasia and North America. It therefore seems unlikely that this invasion has been affected by genetic bottlenecks or founder effects. Indeed, results of assignment tests suggest that multiple introductions have contributed to North America’s C. diffusa invasion. Additionally, assignment tests show that both Eurasian and North American sites had a strong pattern of mixed genetic ancestry. This mixed assignment corresponded to a lack of geographic population structure among Eurasian samples. The lack of population structure in the native range conflicts with general expectations and findings to date for invasion genetics, and cautions that even species’ native ranges may show signs of recent ecological upheaval. Despite the mixed assignments, North American samples showed strong population structure, suggesting that the invasion has been characterized by long-range dispersal of genetically distinct propagules across the introduced range.
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Amsellam L, Noyer JL, Le Bourgeois T, Hossaert-McKey M (2000) Comparison of genetic diversity in 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
Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindiginous plants: a hypothesis. J Ecol 83:887–889
Bohonak AJ (2002) IBD (Isolation By Distance): a program for analyses of isolation by distance. J Hered 93:153–154
Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11
Brown AHD, Marshall DR (1981) Evolutionary changes accompanying colonization in plants. In: Scudder GEC, Reveal JL (eds) Evolution today, proceedings of the 2nd international congress of systematic and evolutionary biology. Hunt Institute for Botanical Documentation, Carnegie-Mellon University, Pittsburgh
DeWalt SJ, Hamrick JL (2004) Genetic variation of introduced Hawaiian and native Costa Rican populations of an invasive tropical shrub, Clidemia hirta (Melastomataceae). Am J Bot 91:1155–1162
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
Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97(13):7043–7050
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
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
Genton BJ, Shykoff A, Giraud T (2005) High genetic diversity in French invasive populations of common ragweed, Ambrosia artemisiifolia, as a result of multiple sources of introduction. Mol Ecol 14:4275–4285
Goolsby JA, Makinson JR, Hartley DM, Zonneveld R, Wright AD (2004) Pre-release evaluation and host range testing of Floracarus perrepae (Eriophyidae) genotypes for biological control of Old World climbing fern. In: Cullen JM, Briese DT, Kriticos DJ, Lonsdale WM, Morin L, Scott JK (eds) Proceedings of the XI international symposium on biological control of weeds. CSIRO Entomology, Canberra, Australia
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (Version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html. Cited 23 May 2007
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. Mol Ecol 14:4207–4219
Hufbauer RA, Sforza R (in press) Multiple introductions of invasive Centaureas inferred from cpDNA haplotypes. Divers Distrib
Husband BC, Barrett SCH (1991) Colonization history and population genetic structure of Eichornia paniculata in Jamaica. Heredity 66:287–296
Kliber A, Eckert CG (2005) Interaction between founder effect and selection during biological invasion in an aquatic plant. Evolution 59:1900–1913
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
Lang RF, Richard RD, Parker PE, Wendel L (2000) Release and establishment of diffuse and spotted knapweed biocontrol agents by USDA, APHIS, PPQ in the United States. Pan-Pac Entomol 76:197–218
LeJeune KD, Seastedt TR (2001) Centaurea species: the forb that won the West. Conserv Biol 15:1568–1574
Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142
Marrs RA, Hufbauer RA, Bogdanowicz SJ, Sforza R (2006) Nine polymorphic microsatellite markers in Centaurea stoebe L. (subspecies C. s. stoebe and C. s. micranthos (S. G. Gmelin ex Gugler) Hayek) and C. diffusa Lam. (Asteraceae). Mol Ecol Notes 6:837–840
Merila J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903
Müller-Scharer H, Schroeder D (1993) The biological-control of Centaurea spp in North America—do insects solve the problem. Pestic Sci 37:343–353
Neel JV (1973) Private genetic variants and frequency of mutation among South-American Indians. Proc Natl Acad Sci USA 70:3311–3315
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Neuffer B, Hurka H (1999) Colonization history and introduction dynamics of Capsella bursa-pastoris (Brassicaceae) in North America: isozymes and quantitative traits. Mol Ecol 8:1667–1681
Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155
Pauwels M, Saumitou-Laprade P, Holl AC, Petit D, Bonnin I (2005) Multiple origin of metallicolous populations of the pseudometallophyte Arabidopsis halleri (Brassicaceae) in central Europe: the cpDNA testimony. Mol Ecol 14:4403–4414
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Raymond M, Rousset F (1995) GENEPOP Version 1.2: population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103
Roché BF Jr, Roché CF (1999) Diffuse knapweed. In: Sheley RL, Petroff JK (eds) Biology and management of noxious rangeland weeds. Oregon State University Press, Corvalis, USA
Roderick GK, Navajas M (2003) Genotypes in novel environments: genetics and evolution in biological control. Nat Rev Genet 4:889–899
Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65
Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279
Therriault TW, Orlova MI, Docker MF, MacIsaac HJ, Heath DD (2005) Invasion genetics of a freshwater mussel (Dreissena rostriformis bugensis) in eastern Europe: high gene flow and multiple introductions. Heredity 95:16–23
Thompson DJ, Stout DG (1991) Duration of the juvenile period in C. diffusa (Centaurea diffusa). Can J Bot 69:368–371
Watson AK, Renney AJ (1974) The biology of Canadian weeds: 6. Centaurea diffusa and C. maculosa. Can J Plant Sci 54:687–701
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
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. Mol Ecol 14:3643–3656
Zenger KR, Richardson BJ, Vachot-Griffin. AM (2003) A rapid population expansion retains genetic diversity within European rabbits in Australia. Mol Ecol 12:789–794
Acknowledgments
This work was funded by the USDA-NRI and the Colorado State University Agricultural Experiment Station. The authors thank Dr. William C. Black IV, Steven Rauth, Amy Blair, and Dr. Rebecca Kao for suggestions that greatly improved this manuscript, and Dr. Andrew Norton and Dale Woods for collecting samples.
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Marrs, R.A., Sforza, R. & Hufbauer, R.A. When invasion increases population genetic structure: a study with Centaurea diffusa . Biol Invasions 10, 561–572 (2008). https://doi.org/10.1007/s10530-007-9153-6
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DOI: https://doi.org/10.1007/s10530-007-9153-6