Skip to main content

Advertisement

Log in

One genotype dominates a facultatively outcrossing plant invasion

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Plant invasions are rarely homogenous. Processes such as selection, drift, gene flow, and founding events can rapidly shape the genetic diversity and spatial population structure of an invasion. We investigated the diversity, origins and population structure of Verbascum thapsus (common mullein), an introduced plant in North America. Despite this species being facultatively outcrossing, we found the invasion dominated by a single genotype (61% of plants were identical amplified fragment length polymorphism [AFLP] genotypes in the western USA). Fifty percent of the invasion populations were monotypic, and we found 32 genotypes overall in the 431 plants sampled from the invasion. In contrast, populations were much more diverse in the native Eurasian range, with 394 genotypes found in 479 plants. Further, we found an exact genetic match between the common genotype 1 in the USA and plants from Belgium and Germany. The identification of the most common and diverse invasive genotypes of common mullein allows their use in tests of management tools and further studies of mechanisms of this invasion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alba C, Hufbauer R (2012) Exploring the potential for climatic factors, herbivory, and co-occurring vegetation to shape performance in native and introduced populations of Verbascum thapsus. Biol Invasions 14:2505–2518

    Google Scholar 

  • Alba C, Bowers MD, Hufbauer R (2012) Combining optimal defense theory and the evolutionary dilemma model to refine predictions regarding plant invasion. Ecology 93:1912–1921

    PubMed  Google Scholar 

  • Alba C, Bowers MD, Blumenthal D, Hufbauer R (2011) Evolution of growth but not structural or chemical defense in Verbascum thapsus (common mullein) following introduction to North America. Biol Invasions 13:2379–2389

    Google Scholar 

  • Alba C, Moravcová L, Pyšek P (2016) Geographic structuring and transgenerational maternal effects shape germination in native, but not introduced, populations of a widespread plant invader. Am J Bot 103:837–844

    PubMed  Google Scholar 

  • Ansari S, Daehler CC (2010) Life history variation in a temperate plant invader, Verbascum thapsus along a tropical elevational gradient in Hawaii. Biol Invasions 12:4033–4047

    Google Scholar 

  • Barratt BIP, Moran VC, Bigler F, van Lenteren JC (2018) The status of biological control and recommendations for improving uptake for the future. Biocontrol 63:155–167

    Google Scholar 

  • Baskin JM, Baskin CC (1981) Seasonal changes in germination responses of buried seeds of Verbascum thapsus and V. blattaria and ecological implications. Can J Bot 59:1769–1775

    Google Scholar 

  • Bock DG, Caseys C, Cousens RD, Hahn MA, Heredia SM, Hübner S, Turner KG, Whitney KD, Rieseberg LH (2015) What we still don’t know about invasion genetics. Mol Ecol 24:2277–2297

    PubMed  Google Scholar 

  • Bonin A, Ehrich D, Manel S (2007) Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionists. Mol Ecol 16:3737–3758

    CAS  PubMed  Google Scholar 

  • Bossard CC, Randall JM, Hoshovsky-Marc C (2000) Invasive plants of California’s wildlands. University of California Press, Berkeley, pp 1–360

    Google Scholar 

  • Burton JE (1964) Methods and problems of weed control along highways. In: Procedures of the 20th North Central Weed Control Conference, 43:6

  • CABI (2019) Verbascum thapsus (common mullein). Invasive species compendium. https://www.cabi.org/isc/datasheet/56652

  • Cristofaro M, Roselli G, Marini F, de Lillo E, Petanovic RU, Vidovic B, Augé M, Rector BG (2020) Open field evaluation of Aculodes altamurgensis, a recently described eriophyid species associated with medusahead (Taeniatherum caput-medusae). Biocontrol Sci Tech. https://doi.org/10.1080/09583157.2019.1711021

    Article  Google Scholar 

  • Cuddihy LW, Stone CP (1990) Alteration of native Hawaiian vegetation: effects of humans, their activities and introductions. University of Hawaii, Cooperative National Park Resources Studies Unit, Honolulu, HI, pp 1–138

    Google Scholar 

  • Daehler CC (2005) Upper-montane plant invasions in the Hawaiian Islands: patterns and opportunities. Perspect Plant Ecol Evol Syst 7:203–216

    Google Scholar 

  • Darlington HT, Bessey EA, Megee CR (1940) Some important Michigan weeds. Michigan State College Agricultural Experiment Station Special Bulletin #304

  • de Lange WJ, van Wilgen BW (2010) An economic assessment of the contribution of biological control to the management of invasive alien plants and to the protection of ecosystem services in South Africa. Biol Invasions 12:4113–4124

    Google Scholar 

  • Dice L (1945) Measures of the amount of ecologic association between species. Ecology 26:297–302

    Google Scholar 

  • Donnelly SE, Lortie CJ, Aarssen LW (1998) Pollination in Verbascum thapsus (Scrophulariaceae): the advantage of being tall. Am J Bot 85:1618–1625

    CAS  PubMed  Google Scholar 

  • Earl DA (2012) Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Google Scholar 

  • EDDMapS (2021) Early detection and distribution mapping system. The University of Georgia—Center for Invasive Species and Ecosystem Health. http://www.eddmaps.org/

  • Endriss SB, Alba C, Norton AP, Pyšek P, Hufbauer RA (2018) Breakdown of a geographic cline explains high performance of introduced populations of a weedy invader. J Ecol 106:699–713

    Google Scholar 

  • Ersts PJ (2021) Geographic distance matrix generator (version 1.2.3). American Museum of Natural History, Center for Biodiversity and Conservation. http://biodiversityinformatics.amnh.org/open_source/gdmg

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gaskin JF, Schwarzländer M, Hinz HL, Williams L, Gerber E, Rector BG, Zhang D (2013) Genetic identity and diversity of perennial pepperweed (Lepidium latifolium) in its native and invaded ranges. Invasive Plant Sci Manag 6:268–280

    Google Scholar 

  • Gross KL, Werner PA (1978) Biology of Canadian Weeds. 28. Verbascum thapsus L. and Verbascum blattaria L. Can J Plant Sci 58:401–413

    Google Scholar 

  • Gross KL (1980a) Ecological consequences of differences in life history characteristics among four "biennial" plant species. PhD Thesis. Michigan State University (East Lansing)

  • Gross KL (1980) Colonization by Verbascum thapsus (mullein) of an old-field in Michigan- experiments on the effects of vegetation. J Ecol 68:919–927

    Google Scholar 

  • Gross KL (1985) Effects of irradiance and spectral quality on the germination of Verbascum thapsus L. and Oenothera biennis L. seeds. New Phytol 101:531–541

    PubMed  Google Scholar 

  • Gucker CL (2008) Verbascum thapsus. Fire Effects Information System. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fire Sciences Laboratory. https://www.fs.fed.us/database/feis/plants/forb/vertha/all.html

  • Hamrick JL, Godt MW (1996) Effects of life history traits on genetic diversity in plant species. Philosophical transactions of the royal society of London. Ser B Biol Sci 351:1291–1298

    Google Scholar 

  • Harms N, Shearer J, Cronin JT, Gaskin JF (2019) Geographic and genetic variation in susceptibility of Butomus umbellatus to foliar fungal pathogens. Biol Invasions. https://doi.org/10.1007/s10530-019-02109-3

    Article  Google Scholar 

  • Hillis DM, Moritz C, Mable BK (1996) Molecular systematics, 2nd edn. Sinauer, Sunderland, MA

  • Kivilaan A, Bandurski RS (1981) The one hundred-year period for Dr. Beal’s seed viability experiment. Am J Bot 68:1290–1292

    Google Scholar 

  • Kumschick S, Hufbauer RA, Alba C, Blumenthal DM (2013) Evolution of fast-growing and more resistant phenotypes in introduced common mullein (Verbascum thapsus). J Ecol 101:378–387

    Google Scholar 

  • Maw MG (1980) Cucullia verbasci an agent for the biological control of common mullein (Verbascum thapsus). Weed Sci 28:27–30

    Google Scholar 

  • Moran EV, Alexander JM (2014) Evolutionary responses to global change: lessons from invasive species. Ecol Lett 17:637–649

    PubMed  Google Scholar 

  • Murbeck SS (1933) Monographie der guttang verbascum. Acta Univ Lund 29:1–630

    Google Scholar 

  • Naranjo SE, Frisvold GB, Ellsworth PC (2019) Economic value of arthropod biological control. In: Onstad D, Crain P (eds) The economics of integrated pest management for insects. Springer, Dordrecht-Heidelberg-London-New York, pp 49–85

    Google Scholar 

  • Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273

    CAS  PubMed  Google Scholar 

  • Odum S (1965) Germination of ancient seeds: floristical observations and experiments with archaeologically dated soil samples. Dansk Botanisk Arkiv 24:1–70

    Google Scholar 

  • Parker IM, Rodriguez J, Loik ME (2003) An evolutionary approach to understanding the biology of invasions: local adaptation and general-purpose genotypes in the weed Verbascum thapsus. Conserv Biol 17:59–72

    Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pervukhina-Smith I, Sforza RF, Cristofaro M, Smith JF, Novak SJ (2020) Genetic analysis of invasive populations of Ventenata dubia (Poaceae): an assessment of propagule pressure and pattern of range expansion in the Western United States. Biol Invasions 22:3575–3592

    Google Scholar 

  • Pitcairn MJ (2000) Verbascum thapsus. In: Bossard CC, Randall JM, Hoshovsky MC (eds) Invasive plants of California’s wildlands. University of California Press, Berkeley, pp 321–326

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reinartz JA (1984) Life history variation of common mullein (Verbascum Thapsus): II. Plant size, biomass partitioning and morphology. The Journal of Ecology 1:913–925

    Google Scholar 

  • Rohlf FJ (1992) NTSYS-PC: Numerical taxonomy and multivariate analysis system. Exeter Software, Setauket

    Google Scholar 

  • Schaffner U (2001) Host range testing of insects for biological weed control: how can it be better interpreted? Bioscience 51:951–959

    Google Scholar 

  • Seipel T, Alexander JM, Daehler CC, Rew LJ, Edwards PJ, Dar PA, McDougall K, Naylor B, Parks C, Pollnac FW, Reshi ZA (2015) Performance of the herb Verbascum thapsus along environmental gradients in its native and non-native ranges. J Biogeogr 42(1):132–143

    Google Scholar 

  • Sotoodeh A, Attar F, Andalo C, Mirtadzadini M, Civeyrel L (2018) Focusing on three Verbascum L. taxa (Scrophulariaceae) of the Flora of Iran. Adansonia 40:171–182

    Google Scholar 

  • Suckling M, Sforza RFH (2014) What magnitude are non-target impacts from weed biocontrol? PLoS ONE 9:1–12

    Google Scholar 

  • Tropicos.org (2020) Missouri Botanical Garden. http://www.tropicos.org. Accessed 06 Nov 2020

  • USDA (2004) Eastern region invasive plants ranked by degree of invasiveness. In: Noxious weeds and non-native invasive plants. Section 3: Invasive plants. Milwaukee, WI: Eastern region (Producer). https://www.fs.fed.us/r9/wildlife/range/weed/Sec3B.htm

  • USDA NRCS (2021) The plants database. http://plants.usda.gov

  • 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 23:4407–4414

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner WL, Herbst DR, Sohmer SH (1999) Manual of the flowering plants of Hawai'i, revised edition. Volume 2. University of Hawai'i Press (Honolulu), 988

  • Ward SM, Gaskin JF, Wilson LM (2008) Ecological genetics of plant invasion: what do we know? Invasive Plant Sci Manag 1:98–109

    Google Scholar 

  • Werner PA (1975) A seed trap for determining patterns of seed deposition in terrestrial plants. Can J Bot 53:810–813

    Google Scholar 

  • Whittle CA, Otto SP, Johnston MO, Krochko JE (2009) Adaptive epigenetic memory of ancestral gtemperature regime in Arabidopsis thaliana. Botany 87:650–657

    CAS  Google Scholar 

  • Young RT (1907) The forest formations of Boulder County, Colorado. Bot Gaz 44:321–352

    Google Scholar 

Download references

Acknowledgements

The authors would like to individually thank Massimo Cristofaro and Francesca Marini (BBCA, Rome, Italy), Stephen Novak (Boise State University, Idaho, USA), Christina Alba (Denver Botanic Gardens, Colorado, USA), Cécile Chambon, Pierre Silva, and Christophe Maurel (France), who kindly help in collecting plant DNA included in this study. Thanks to K. Mann and J. Lassey for generating AFLP data. This research was made possible in part by funding from the Bureau of Land Management (Montana, South and North Dakota) Billings Office, Colorado State University’s Graduate Degree Program in Ecology (Small Research Grant to SBE), the USA National Science Foundation (DDIG 1501905 to SBE), the Colorado State University Agricultural Experiment Station to APN, and by the USDA National Institute of Food and Agriculture (Hatch project 1012868 to RAH).

Funding

No conflicts of interest have been declared. All data connected to this analysis are available in the manuscript supplementary files. All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by all. The first draft of the manuscript was written by JFG and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John F. Gaskin.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 3201 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gaskin, J.F., Endriss, S.B., Fettig, C.E. et al. One genotype dominates a facultatively outcrossing plant invasion. Biol Invasions 23, 1901–1914 (2021). https://doi.org/10.1007/s10530-021-02480-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-021-02480-0

Keywords

Navigation