Biological Invasions

, Volume 16, Issue 1, pp 205–216 | Cite as

Genetic evidence for founder effects in the introduced range of houndstongue (Cynoglossum officinale)

  • Jennifer L. WilliamsEmail author
  • Lila Fishman
Original Paper


Phenotypic differentiation can occur between the native and introduced ranges of a species as a result of novel selective pressures, or by neutral processes and historical events. Our aim was to determine how underlying patterns of genetic diversity and potential population origin might have contributed to phenotypic differentiation between the native and introduced ranges of an herbaceous weed. We combined data from microsatellite markers from 16 native and 16 introduced populations of Cynoglossum officinale, a noxious weed of the western US, with previously published phenotypic data from common gardens to investigate genetic diversity in both ranges and relate population structure to phenotypic differentiation. Several lines of evidence suggest loss of genetic diversity during the introduction of C. officinale. Despite reduced diversity, introduced plants out-performed natives in a common garden in one environment. We found little evidence that population-level variation in diversity contributed to phenotypic variation (e.g. through inbreeding depression). Our results suggest that establishment, spread, and potentially adaptation of a species to a new range is not prevented by reductions in genetic diversity of the magnitude we observed. Further, we suggest that non-random filtering or biased introduction at the point of emigration may contribute to phenotypic divergence between ranges.


Common garden Cynoglossum officinale Founder effects Genetic diversity Houndstongue Invasive plant Native and introduced ranges Weed 



We thank Jennifer Andreas, Harald Auge, Tom de Jong, and Stefan Toepfer for collecting seeds, and Samantha Campbell for assisting in the greenhouse. We are grateful to Camille Barr for invaluable advice in the lab and to Mike Schwartz for statistical advice. Jake Alexander, Darren Johnson and Joanna Kelley provided helpful comments on the manuscript. Support for this study was provided by NSF grant DBI-0321329 to LF and to JW by an NSF Graduate Research Fellowship, NSF Doctoral Dissertation Improvement Grant DEB 05-08102 and from the National Center for Ecological Analysis and Synthesis, a Center Funded by NSF (Grant #EF-0553768), the University of California, Santa Barbara, and the State of California. Seeds were imported into the US under USDA-APHIS permit 37-86531.

Supplementary material

10530_2013_514_MOESM1_ESM.docx (98 kb)
Supplementary material 1 (DOCX 97kb)


  1. 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 Associates, Sunderland, MA, pp 254–277Google Scholar
  2. Blair AC, Wolfe LM (2004) The evolution of an invasive plant: an experimental study with Silene latifolia. Ecology 85:3035–3042CrossRefGoogle Scholar
  3. Boorman LA, Fuller RM (1984) The comparative ecology of two sand dune biennials: Lactuca virosa L. and Cynoglossum officinale L. New Phytol 69:609–629CrossRefGoogle Scholar
  4. Bossdorf O, Auge H, Lafuma L et al (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11PubMedCrossRefGoogle Scholar
  5. Chun YJ, Nason JD, Moloney KA (2009) Comparison of quantitative and molecular genetic variation of native versus invasive populations of purple loosestrife (Lythrum salicaria L., Lythraceae). Mol Ecol 18:3020–3035PubMedCrossRefGoogle Scholar
  6. Chun YJ, Le Corre V, Bretagnolle F (2011) Adaptive divergence for a fitness-related trait among invasive Ambrosia artemisiifolia in France. Mol Ecol 20:1378–1388PubMedCrossRefGoogle Scholar
  7. De Clerck-Floate R, Wikeem B (2009) Influence of release size on establishment and impact of a root weevil for the biocontrol of houndstongue (Cynoglossum officinale). Biocontrol Sci Tech 19:169–183CrossRefGoogle Scholar
  8. de Jong TJ, Klinkhamer PGL, Boorman LA (1990) Biological flora of the British Isles: Cynoglossum officinale L. J Ecol 78:1123–1144CrossRefGoogle Scholar
  9. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449PubMedCrossRefGoogle Scholar
  10. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  11. Durka W, Bossdorf O, Prati D et al (2005) Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol Ecol 14:1697–1706PubMedCrossRefGoogle Scholar
  12. Enßlin A, Sandner TM, Matthies D (2011) Consequences of ex situ cultivation of plants: genetic diversity, fitness and adaptation of the monocarpic Cynoglossum officinale L. in botanic gardens. Biol Conserv 144:272–278CrossRefGoogle Scholar
  13. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  14. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedCentralGoogle Scholar
  15. Fishman L, Willis JH (2005) A novel meiotic drive locus almost completely distorts segregation in Mimulus (monkeyflower) hybrids. Genetics 169:347–353PubMedCrossRefGoogle Scholar
  16. Gao H, Williamson S, Bustamante CD (2007) A Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176:1635–1651PubMedCrossRefGoogle Scholar
  17. Gaskin JF, Zhang D-Y, Bon M-C (2005) Invasion of Lepidium draba (Brassicaceae) in the western United States: distributions and origins of chloroplast DNA haplotypes. Mol Ecol 14:2331–2341PubMedCrossRefGoogle Scholar
  18. Genton BJ, Shykoff J, 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 14:4275–4285PubMedCrossRefGoogle Scholar
  19. Gladieux P, Giraud T, Kiss L et al (2011) Distinct invasion sources of common ragweed (Ambrosia artemisiifolia) in Eastern and Western Europe. Biol Invasions 13:933–944CrossRefGoogle Scholar
  20. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from
  21. Goudet J (2005) Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186CrossRefGoogle Scholar
  22. Hardesty BD, Le Roux JJ, Rocha OJ et al (2012) Getting here from there: testing the genetic paradigm underpinning introduction histories and invasion success. Divers Distrib 18:147–157CrossRefGoogle Scholar
  23. Keller SR, Taylor DR (2008) History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecol Lett 11:852–866PubMedCrossRefGoogle Scholar
  24. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204PubMedCrossRefGoogle Scholar
  25. Korbecka G, Wolff K (2004) Characterization of nine microsatellite loci in Cynoglossum officinale (Boraginaceae). Mol Ecol Notes 4:229–230CrossRefGoogle Scholar
  26. Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Nat Acad Sci 104:3883–3888PubMedCrossRefGoogle Scholar
  27. Mack RN (2003) Global plant dispersal, naturalization and invasion: pathways, modes and circumstances. In: Ruiz GM, Carlton JT (eds) Invasive species: vectors and management strategies. Island Press, Washington, DC, pp 3–30Google Scholar
  28. Maron JL, Vilà M, Bommarco R et al (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280CrossRefGoogle Scholar
  29. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  30. Novak SJ, Mack RN (2005) Genetic bottlenecks in alien plant species: influence of mating systems and introduction dynamics. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland, MA, pp 201–228Google Scholar
  31. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  32. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  33. R Core Development Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  34. Richards CL, Bossdorf O, Muth NZ et al (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993PubMedCrossRefGoogle Scholar
  35. Upadhyaya MK, Tilsner HR, Pitt MD (1988) The biology of Canadian weeds. 87. Cynoglossum officinale L. Can J Plant Sci 68:763–774CrossRefGoogle Scholar
  36. van der Meijden E, Klinkhamer PGL, de Jong TJ et al (1992) Meta-population dynamics of biennial plants: how to exploit temporary habitats. Acta Botanica Neerlandica 41:249–270Google Scholar
  37. Vrieling K, Saumitou-Laprade P, Cuguen J et al (1999) Direct and indirect estimates of the selfing rate in small and large individuals of the bumblebee pollinated Cynoglossum officinale L (Boraginaceae). Ecol Lett 2:331–337CrossRefGoogle Scholar
  38. Wares JP, Hughes AR, Grosberg RK (2005) Mechanisms that drive evolutionary change: insights from species introductions and invasions. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland, MA, pp 229–257Google Scholar
  39. Williams JL (2009) Flowering life-history strategies differ between the native and introduced ranges of a monocarpic perennial. Am Nat 174:660–672PubMedCrossRefGoogle Scholar
  40. Williams JL, Auge H, Maron JL (2008) Different gardens, different results: native and introduced populations exhibit contrasting phenotypes across common gardens. Oecologia 157:239–248PubMedCrossRefGoogle Scholar
  41. Xu C-Y, Julien MH, Fatemi M et al (2010) Phenotypic divergence during the invasion of Phyla canescens in Australia and France: evidence for selection-driven evolution. Ecol Lett 13:32–44PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Division of Biological SciencesUniversity of MontanaMissoulaUSA
  2. 2.Department of GeographyUniversity of British ColumbiaVancouverCanada

Personalised recommendations