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Genetic variation and population structure of the garden escaper Lupinus polyphyllus in Finland

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Abstract

Analysis of the amount and distribution of genetic variation can yield information about the number of introductions and history of an invasive species, which may be relevant for understanding the evolutionary potential and spread of invaders, as well as for creating best management practices for curbing them. We explored the genetic patterns and invasion history of the perennial, ornamental herb Lupinus polyphyllus Lindl. in Finland, where the species has spread rapidly during the past hundred years. Using 13 microsatellite loci, we determined the genetic variation of L. polyphyllus in 51 sites across a latitudinal gradient that reflected the invasion history of the species in this country. We found that the sampled populations were significantly genetically differentiated among sites, as indicated by the global FST value (0.19) and AMOVA results (16.7 % of total genetic variation occurred among sites), and this differentiation slightly increased with increasing geographic distance (r = 0.11, P = 0.006), indicating limited gene flow. Genetic variation of L. polyphyllus, measured as the average number of alleles per site or the average number of unshared alleles between pairs of individuals per site, was not associated with latitude. Our results suggest that the invasive populations of L. polyphyllus are genetically differentiated in Finland, but show no evidence of a loss of genetic variation during the invasion process. Overall, this pattern reflects human-mediated dispersal with multiple introductions from different sources rather than the natural spread of L. polyphyllus from a single or few sources in Finland.

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References

  • Aniszewski T, Kupari MH, Leinonen AJ (2001) Seed number, seed size and seed diversity in Washington lupin (Lupinus polyphyllus Lindl.). Ann Bot (Oxford) 87:77–82. doi:10.1006/anbo.2000.1300

    Article  Google Scholar 

  • Arias MC, Atteke C, Augusto SC, Bailey J, Bazaga P, Beheregaray LB, Benoit L, Blatrix R, Born C, Brito RM, Chen H-K, Covarrubias S, de Vega C, Djieto-Lordon C, Dubois M-P, Francisco FO, Garcia C, Goncalves PHP, Gonzalez C, Gutierrez-Rodriguez C, Hammer MP, Herrera CM, Itoh H, Kamimura S, Karaoglu H, Kojima S, Li S-L, Ling HJ, Matos-Maraávi PF, McKey D, Mezui-M’Eko J, Ornelas JF, Park RF, Pozo MI, Ramula S, Rigueiro C, Sandoval-Castillo J, Santiago LR, Seino MM, Song CB, Takeshima H, Vasemägi A, Wellings CR, Yan J, Yu-Zhou D, Zhang CR, Zhang TY (2013) Permanent genetic resources added to Molecular Ecology Resources Database 1 February 2013–31 March 2013. Molec Ecol Res 13:760–762. doi:10.1111/1755-0998.12121

  • Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Molec Ecol 11:155–165. doi:10.1046/j.0962-1083.2001.01436.x

    Article  Google Scholar 

  • Bellstedt DU, Pirie MD, Visser JC, de Villiers MJ, Gehrke B (2010) A rapid and inexpensive method for the direct PCR amplification of DNA from plants. Amer J Bot 97:E65–E68. doi:10.3732/ajb.1000181

    CAS  Google Scholar 

  • 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. doi:10.1007/s00442-005-0070-z

    Article  PubMed  Google Scholar 

  • Burdon JJ, Marshall DR (1981) Biological control and the reproductive mode of weeds. J Appl Ecol 18:649–658. doi:10.2307/2402423

    Article  Google Scholar 

  • de Vere N, Jongejans E, Plowman A, Williams E (2009) Population size and habitat quality affect genetic diversity and fitness in the clonal herb Cirsium dissectum. Oecologia 159:59–68. doi:10.1007/s00442-008-1203-y

    Article  PubMed  Google Scholar 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molec Ecol 17:431–449. doi:10.1111/j.1365-294X.2007.03538.x

    Article  CAS  Google Scholar 

  • Forsman A (2014) Effects of genotypic and phenotypic variation on establishment are important for conservation, invasion, and infection biology. Proc Natl Acad Sci USA 111:302–307. doi:10.1073/pnas.1317745111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fremstad E (2010) NOBANIS—Invasive Alien Species Fact Sheet—Lupinus polyphyllus. In: Online Database of the European Network on Invasive Alien Species—NOBANIS. Available at: www.nobanis.org. Accessed 17 June 2015

  • Fremstad E, Elven R (2002) Perennial lupins in Fennoscandia. Wild and cultivated lupins from the Tropics to the Poles. In: van Santen E, Hill GD (eds) Proceedings of the 10th International Lupin Conference, Laugarvatn, Iceland, 19-24 June 2002, International Lupin Association, Canterbury, 178–183

  • Haynes J, Mesler M (1984) Pollen foraging by bumblebees: foraging patterns and efficiency on Lupinus polyphyllus. Oecologia 61:249–253. doi:10.1007/BF00396768

    Article  Google Scholar 

  • 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. Biol Inv 18:2819–2831. doi:10.1111/j.1365-294X.2009.04237.x

    CAS  Google Scholar 

  • Hofhanzlová E, Fér T (2009) Genetic variation and reproduction strategy of Gentiana pannonica in different habitats. Flora 204:99–110. doi:10.1016/j.flora.2008.01.004

    Article  Google Scholar 

  • Holderegger R, Kamm U, Gugerli F (2006) Adaptive vs. neutral genetic diversity: implications for landscape genetics. Landscape Ecol 21:797–807. doi:10.1007/s10980-005-5245-9

    Article  Google Scholar 

  • Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914

    Article  Google Scholar 

  • Jantunen J, Saarinen K, Valtonen A (2005) Niitettyjen tienpientareiden kasvillisuus. Vuoden 2005 tulokset. Raportti 4. Etelä-Karjalan Allergia- ja Ympäristöinstituutti, Joutseno, p 26

  • Kelager A, Pedersen JS, Bruun HH (2013) Multiple introductions and no loss of genetic diversity: invasion history of Japanese Rose, Rosa rugosa, in Europe. Biol Invas 15:1125–1141. doi:10.1007/s10530-012-0356-0

    Article  Google Scholar 

  • Kleist A, Herrera-Reddy AM, Sforza R, Jasieniuk M (2014) Inferring the compex oirigns of horticultural invasives: french broom in California. Biol Invas 16:887–901. doi:10.1007/s10530-013-0546-4

    Article  Google Scholar 

  • Kolb A, Durka W (2013) Reduced genetic variation mainly affects early rather than late life-cycle stages. Biol Conserv 159:367–374. doi:10.1016/j.biocon.2012.11.019

    Article  Google Scholar 

  • Kubešová M, Moravcová L, Suda J, Jarošík V, Pyšek P (2010) Naturalized plants have smaller genomes than their non-invading relatives: a flow cytometric analysis of the Czech alien flora. Preslia 82:81–96

    Google Scholar 

  • Kudoh H, Shibaike H, Takasu H, Wigham DF, Kawano S (1999) Genet structure and determinants of clonal structure in a temperate deciduous woodland herb, Uvularia perfoliata. J Ecol 87:244–257. doi:10.1046/j.1365-2745.1999.00355.x

    Article  Google Scholar 

  • Lachmuth S, Durka W, Schurr FM (2010) The making of a rapid plant invader: genetic diversity and differentiation in the native and invaded range of Senecio inaequidens. Molec Ecol 19:3952–3967. doi:10.1111/j.1365-294X.2010.04797.x

    Article  Google Scholar 

  • 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. doi:10.1073/pnas.0607324104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li S-L, Vasemägi A, Ramula S (2016) Genetic variation facilitates seedling establishment but not population growth rate of a perennial invader. Ann Bot (Oxford) 117:187–194. doi: 10.1093/aob/mcv145

    Article  Google Scholar 

  • Meier CI, Reid BL, Sandoval O (2013) Effects of the invasive plant Lupinus polyphyllus on vertical accretion of fine sediment and nutrient availability in bars of the gravel-bed Paloma river. Limnologica 43:381–387. doi:10.1016/j.limno.2013.05.004

    Article  CAS  Google Scholar 

  • Obbard DJ, Harris SA, Pannell JR (2006) Simple allelic-phenotype diversity and differentiation statistics for allopolyploids. Heredity 97:296–303. doi:10.1038/sj.hdy.6800862

    Article  CAS  PubMed  Google Scholar 

  • Pohtio I, Teräs I (1995) Bumblebee visits to different colour morphs of the Washington lupine, Lupinus polyphyllus. Entomol Fenn 6:139–151

    Google Scholar 

  • R Development Core Team (2013) The R project for statistical computing. Available at: http://www.r-project.org

  • Ramula S (2014) Linking vital rates to invasiveness of a perennial herb. Oecologia 174:1255–1264. doi:10.1007/s00442-013-2869-3

    Article  PubMed  Google Scholar 

  • Ramula S, Pihlaja K (2012) Plant communities and the reproductive success of native plants after the invasion of an ornamental herb. Biol Invas 14:2079–2090. doi:10.1007/s10530-012-0215-z

    Article  Google Scholar 

  • Rapp W (2009) Invasive plant management in Glacier Bay National Park and Preserve: Summer 2009 field season report. U.S. National Park Service, Glacier Bay National Park and Preserve, Gustavus

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464. doi:10.1016/j.tree.2007.07.002

    Article  PubMed  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annual Rev Ecol Syst 32:302–332. doi:10.1146/annurev.ecolsys.32.081501.114037

    Article  Google Scholar 

  • Sõber V, Ramula S (2013) Seed number and environmental conditions do not explain seed size variability for the invasive herb Lupinus polyphyllus. Pl Ecol 214:883–892. doi:10.1007/s11258-013-0216-8

    Article  Google Scholar 

  • Vallejo-Marin M, Lye GC (2013) Hybridisation and genetic diversity of introduced Mimulus (Phrymaceae). Heredity 110:111–122. doi:10.1038/hdy.2012.91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valtonen A, Jantunen J, Saarinen K (2006) Flora and lepidoptera fauna adversely affected by invasive Lupinus polyphyllus along road verges. Conserv Biol 133:389–396. doi:10.1016/j.biocon.2006.06.015

    Article  Google Scholar 

  • Vyšniauskiené R, Ranceliené V, Žvingila D, Patamsyté J (2011) Genetic diversity of invasive alien species Lupinus polyphyllus population in Lithuania. Agriculture 98:383–390

    Google Scholar 

  • Wang XY, Shen DW, Jiao J, Xu NN, Yu S, Zhou XF, Shi MM, Chen XY (2012) Genotypic diversity enhances invasive ability of Spartina alterniflora. Molec Ecol 21:2542–2551. doi:10.1111/j.1365-294X.2012.05531.x

    Article  CAS  Google Scholar 

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Acknowledgments

We thank the staff at the TEG-lab for practical help during the genetic analysis, and the Emil Aaltonen Foundation for funding.

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Correspondence to Satu Ramula.

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This study was funded by the Emil Aaltonen Foundation (a project grant to SR).

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The authors declare that they have no conflict of interest.

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Handling editor: Christoph Oberprieler.

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Supplementary material 1 (PDF 31 kb)

Supplementary material 2 (PDF 12 kb)

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Online Resource 1. Details for multiplex PCR used in this study.

Online Resource 2. Pairwise genetic distances of the sampled sites in relation to geographic distances.

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Li, SL., Vasemägi, A. & Ramula, S. Genetic variation and population structure of the garden escaper Lupinus polyphyllus in Finland. Plant Syst Evol 302, 399–407 (2016). https://doi.org/10.1007/s00606-015-1273-3

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