Biological Invasions

, Volume 12, Issue 12, pp 3973–3987 | Cite as

Patterns of genetic variation in invasive populations of Gunnera tinctoria: an analysis at three spatial scales

  • Mark FennellEmail author
  • Tommy Gallagher
  • Bruce Osborne
Original Paper


While there is evidence that the genetic structure of invasive populations may be distinct from native populations, it has proved difficult to establish the causes of any variation owing in part to the range of evolutionary processes involved. In order to assess differences in the genetic structure of invasive populations of Gunnera tinctoria, five native populations were compared to 23 geographically widely dispersed invasive populations using amplified fragment length polymorphic markers (AFLPs). In total, 221 individuals were sampled at three spatial scales: inter-regional, within-region, and at a high-resolution local scale. It was observed that there were high levels of genetic variation between most populations, that invasive populations were generally distinct from both native populations and from each other and that genetic variation away from founding populations can occur relatively quickly and within a small geographic area. Changes in the pattern of genetic variation observed in invasive populations strongly indicated that founder effects and genetic drift played a significant role in shaping their genetic structure. It was further concluded that gene flow had a homogenizing effect on the structure of invasive populations occurring in close proximity, increasing their allele content and potentially contributing to their successful establishment.


AFLP analysis Gunnera tinctoria Invasive species Non-adaptive evolution Population genetics Spatial scales 



This study was funded by a University College Dublin Research Demonstratorship awarded to Mark Fennell. We would like to thank Craig Hornby, Cristina Armstrong, Javier Atalah, Margherita Gioria, Luis Silva, Curtis Daehler and Kieran MacKevitt for sample collection; Tom Fennell and Joan Forsdyke for proof reading; and Karen Bacon for help with statistical analysis.


  1. Allendorf FW, Lundkvist LL (2003) Population biology, evolution, and control of invasive species. Conserv Biol 17:24–30. doi: 10.1046/j.1523-1739.2003.01717.x CrossRefGoogle Scholar
  2. Armstrong C (2008) Development of control measures and distribution mapping of Gunnera tinctoria on Achill Island, Co. Mayo, Ireland. Dissertation, University College DublinGoogle Scholar
  3. Armstrong C, Osborne BA, Kelly J, Maguire CM (2009) Giant rhubarb (Gunnera tinctoria) invasive species action plan. Report prepared for NIEA and NPWS as part of Invasive Species Ireland. Accessed 6 March 2010
  4. Baker HG, Stebbins GL (eds) (1965) The genetics of colonizing species. In: Proceedings of the first international union of biological sciences symposia on general biology. Academic Press, New YorkGoogle Scholar
  5. Barrett SCH, Husband BC (1990) The genetics of plant migration and colonization. In: Brown AHD, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding, and genetic resources. Sinauer, Sunderland, pp 254–277Google Scholar
  6. Barrett SCH, Richardson BJ (1986) Genetic attributes of invading species. In: Groves RH, Burdon JJ (eds) Ecology of biological invasions: an Australian perspective. Australian Academy of Science, Australia, pp 21–33Google Scholar
  7. Bassam BJ, Gresshoff PM (2007) Silver staining DNA in polyacrylamide gels. Nature Protoc 2:2649–2654CrossRefGoogle Scholar
  8. Bonin A, Eheich D, Manel S (2007) Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionists. Mol Ecol 16:3737–3758. doi: 10.1111/j.1365-294X.2007.03435.x PubMedCrossRefGoogle Scholar
  9. Carson HL (1990) Increased genetic variance after a population bottleneck. Trends Ecol Evol 5:228–230CrossRefGoogle Scholar
  10. Chase MW, Hill HH (1991) Silica gel: an ideal material for field preservation of leaf samples for DNA studies. Taxon 40:215–220CrossRefGoogle Scholar
  11. Cheverud JM, Routman EJ (1996) Epistasis as a source of increased additive genetic variance at population bottlenecks. Evolution 50:1042–1051CrossRefGoogle Scholar
  12. Chun YJ, Nason JD, Moloney KA (2009) Comparison of quantitative and molecular genetic variation of native vs. invasive populations of purple loosestrife (Lythrum salicaria L., Lythraceae). Mol Ecol 18:3020–3035. doi: 10.1111/j.1365-294X.2009.04254.x PubMedCrossRefGoogle Scholar
  13. 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 185:1100–1107PubMedCrossRefGoogle Scholar
  14. Cox GW (2004) Alien species and evolution: the evolutionary ecology of exotic plants, animals, microbes, and interacting native species. Island Press, LondonGoogle Scholar
  15. Crawley MJ (1987) What makes a community invisible? In: Gray AJ, Crawley MJ, Edwards PJ (eds) Colonization, succession and stability. Blackwell Scientific Publications, Oxford, pp 429–453Google Scholar
  16. Crooks J, Soule ME (1999) Lag times in population explosions of invasive species: causes and implications. In: Sandlund OT, Schei SJ, Vikens A (eds) Invasive species and biodiversity management. Kluwer Academic Publishers, The Netherlands, pp 103–125Google Scholar
  17. Doyle GJ, Foss PJ (1986) A resurvey of the Clare Island flora. Ir Nat J 22:85–89Google Scholar
  18. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050PubMedCrossRefGoogle Scholar
  19. Ellstrand NC, Devlint B, Marshall DL (1989) Gene flow by pollen into small populations: data from experimental and natural stands of wild radish. Proc Natl Acad Sci USA 86:9044–9047PubMedCrossRefGoogle Scholar
  20. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonGoogle Scholar
  21. Epperson BK (1990) Spatial autocorrelation of genotypes under directional selection. Genetics 124:757–771PubMedGoogle Scholar
  22. Etisham-Ul-Haq M, Allnutt TR, Smith-Ramírez C, Gardnerk MF, Armesto JJ, Newton AC (2001) Patterns of genetic variation in in and ex situ populations of the threatened Chilean vine Berberidopsis corallina, detected using RAPD markers. Ann Bot 87:813–821. doi: 10.1006/anbo.2001.1420 CrossRefGoogle Scholar
  23. Genton BJ, Shykoff JA, 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. doi: 10.1111/j.1365-294X.2005.02750.x PubMedCrossRefGoogle Scholar
  24. Gioria M, Osborne BA (2008) The soil seed banks of two invasive plant species, Heracleum mantegazzianum and Gunnera tinctoria, in Ireland. In: Tokarska-Guzik B, Brock JH, Brundu G, Child L, Daehler CC, Pyšek P (eds) Plant invasions: human perception, ecological impacts and management. Backhuys, Leiden, pp 217–233Google Scholar
  25. Gioria M, Osborne BA (2009a) The impact of Gunnera tinctoria (Molina) Mirbel invasions on soil seed bank communities. J Plant Ecol 2:153–167. doi: 10.1093/jpe/rtp013 CrossRefGoogle Scholar
  26. Gioria M, Osborne BA (2009b) Similarities in the impact of three large invasive plant species on soil seed bank communities. Biol Inv. doi: 10.1007/s10530-009-9580-7
  27. Hammer O, Harper DAT, Ryan PD (2009) PAST: paleontological statistics software package for education and data analysis, Version 1.94b. www.http// Accessed 9 Nov 2009
  28. Hickey E, Osborne BA (2001) Effect of Gunnera tinctoria (Molina) Mirbel on semi-natural grassland habitats in the west of Ireland. In: Brundu G, Brock JH, Camarda I, Child L, Wade PM (eds) Plant invasions: species ecology and ecosystem management. Blackwell, Oxford, pp 105–114Google Scholar
  29. Jaccard P (1901) Distribution de la flore alpine dans le bassin des Dranses et dans quelques régions voisines. Bull Soc Vaudoise Sci Nat 37:241–272Google Scholar
  30. Jones TH, Vaillancourt RE, Potts BM (2007) Detection and visualization of spatial genetic structure in continuous Eucalyptus globulus forest. Mol Ecol 16:697–707. doi: 10.1111/j.1365-294X.2006.03180.x PubMedCrossRefGoogle Scholar
  31. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. doi: 10.1111/j.1461-0248.2004.00684.x CrossRefGoogle Scholar
  32. Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:3883–3888PubMedCrossRefGoogle Scholar
  33. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391. doi: 10.1016/S0169-5347(02)02554-5 CrossRefGoogle Scholar
  34. LeRoux J (2008) What can genes tell us about invasive species? Quest 4:31–37Google Scholar
  35. Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277. doi: 10.1146/annurev.ecolsys.27.1.237 CrossRefGoogle Scholar
  36. Liscum E (1999) AFLP: studies on plant development. In: Innis M, Gelfand D, Sninsky J (eds) PCR methods manual. Academic Press, San Diego, pp 505–519Google Scholar
  37. Mack RN (1985) Invading plants: their potential contribution to population biology. In: White J (ed) Studies on plant demography: a festschrift for John L. Harper. Academic Press, London, pp 127–142Google Scholar
  38. Maron JL, Vilà M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280. doi: 10.1890/03-4027 CrossRefGoogle Scholar
  39. McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291. doi: 10.1016/S0169-5347(02)02478-3 CrossRefGoogle Scholar
  40. Merilä J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903. doi: 10.1046/j.1420-9101.2001.00348 CrossRefGoogle Scholar
  41. Mueller UG, Wolfenbarger LL (1999) AFLP genotyping and fingerprinting. Trends Ecol Evol 14:389–394PubMedCrossRefGoogle Scholar
  42. Naghavi MR, Mardi M, Pirseyedi SM, Kazemi M, Potki P, Ghaffari MR (2007) Comparison of genetic variation among accessions of Aegilops tauschii using AFLP and SSR markers. Genet Resour Crop Evol 54:237–240. doi: 10.1007/s10722-006-9143-z CrossRefGoogle Scholar
  43. Osborne BA, Bergman B (2009) Why does Gunnera do it and other angiosperms don’t? An evolutionary perspective of the Gunnera-Nostoc symbiosis. Microbiol Monogr 8:207–224. doi: 10.1007/978-3-540-75460-2 CrossRefGoogle Scholar
  44. Osborne BA, Sprent JI (2002) Ecology of the Nostoc-Gunnera symbiosis. In: Rai AN, Bergman B, Rassmussen U (eds) Cyanobacteria in Symbiosis. Kluwer Academic Publishers, Dordrecht, pp 233–252Google Scholar
  45. Osborne BA, Doris F, Cullen A, McDonald R, Campbell G, Steer M (1991) Gunnera tinctoria: an unusual nitrogen-fixing plant invader. Bioscience 41:224–235CrossRefGoogle Scholar
  46. Parisod C, Trippi C, Galland N (2005) Genetic variability and founder effect in the pitcher plant Sarracenia purpurea (Sarraceniaceae) in populations introduced into Switzerland: from inbreeding to invasion. Ann Bot 95:277–286. doi: 10.1093/aob/mci023 PubMedGoogle Scholar
  47. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi: 10.1111/j.1471-8286.2005.01155.x CrossRefGoogle Scholar
  48. Pich U, Schubert I (1993) Midiprep method for isolation of DNA from plants with a high content of polyphenolics. Nucleic Acids Res 21:3328–3330PubMedCrossRefGoogle Scholar
  49. Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294. doi: 10.1016/j.tplants.2008.03.004 PubMedCrossRefGoogle Scholar
  50. Preston CD, Pearman DA, Dines TD (eds) (2002) New atlas of the British and Irish flora: an atlas of the vascular plants of Britain, Ireland, the Isle of man and the Channel Islands. University Press, OxfordGoogle Scholar
  51. Rajagopal S, Pollux BJA, Peters JL, Cremers G, Moon-van der Staay SY, van Alen T, Eygensteyn J, van Hoek A, Palau A, de Vaate A, van der Velde G (2009) Origin of Spanish invasion by the zebra mussel, Dreissena polymorpha (Pallas, 1771) revealed by amplified fragment length polymorphism (AFLP) fingerprinting. Biol Inv 11:2147–2159. doi: 10.1007/s10530-009-9495-3 CrossRefGoogle Scholar
  52. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237CrossRefGoogle Scholar
  53. Schlaepfer DR, Glättli M, Fischer M, van Kleunen M (2009) A multi-species experiment in their native range indicates pre-adaptation of invasive alien plant species. New Phytol 185:1087–1099. doi: 10.1111/j.1469-8137.2009.03114.x PubMedCrossRefGoogle Scholar
  54. Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana, ILGoogle Scholar
  55. Switzer RC, Merril CR, Shifrin S (1979) A highly sensitive silver stain for detecting proteins and peptides in poly- acrylamide gels. Anal Biochem 98:231–237PubMedCrossRefGoogle Scholar
  56. Van Buskirk J, Willi Y (2006) The change in quantitative genetic variation with inbreeding. Evolution 60:2428–2434PubMedCrossRefGoogle Scholar
  57. Vekemans X, Beauwens T, Lemaire M, Roldan-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151PubMedCrossRefGoogle Scholar
  58. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414PubMedCrossRefGoogle Scholar
  59. Ward S (2006) Genetic analysis of invasive plant populations at different spatial scales. Biol Inv 8:541–552. doi: 10.1007/s10530-005-6443-8 CrossRefGoogle Scholar
  60. Wen-Kun H, Jian-Ying G, Fang-Hao W, Bi-Da G, Bing-Yan X (2007) AFLP analyses on genetic diversity and structure of Eupatorium adenophorum populations in China. J Agric Biotechnol 15:992–1000Google Scholar
  61. Williams PA, Ogle CC, Timmins SM, Cock GDL, Clarkson J (2005) Chilean rhubarb (Gunnera tinctoria): biology, ecology and conservation impacts in New Zealand. Department of Conservation, WellingtonGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.School of Biology and Environmental ScienceUniversity College DublinBelfield, Dublin 4Ireland

Personalised recommendations