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.
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
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
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
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
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
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
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
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
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
Bossard CC, Randall JM, Hoshovsky-Marc C (2000) Invasive plants of California’s wildlands. University of California Press, Berkeley, pp 1–360
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
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
Daehler CC (2005) Upper-montane plant invasions in the Hawaiian Islands: patterns and opportunities. Perspect Plant Ecol Evol Syst 7:203–216
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
Dice L (1945) Measures of the amount of ecologic association between species. Ecology 26:297–302
Donnelly SE, Lortie CJ, Aarssen LW (1998) Pollination in Verbascum thapsus (Scrophulariaceae): the advantage of being tall. Am J Bot 85:1618–1625
Earl DA (2012) Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conserv Genet Resour 4:359–361
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
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
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
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
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
Gross KL, Werner PA (1978) Biology of Canadian Weeds. 28. Verbascum thapsus L. and Verbascum blattaria L. Can J Plant Sci 58:401–413
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
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
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
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
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
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
Maw MG (1980) Cucullia verbasci an agent for the biological control of common mullein (Verbascum thapsus). Weed Sci 28:27–30
Moran EV, Alexander JM (2014) Evolutionary responses to global change: lessons from invasive species. Ecol Lett 17:637–649
Murbeck SS (1933) Monographie der guttang verbascum. Acta Univ Lund 29:1–630
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
Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273
Odum S (1965) Germination of ancient seeds: floristical observations and experiments with archaeologically dated soil samples. Dansk Botanisk Arkiv 24:1–70
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
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
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
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
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
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
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
Rohlf FJ (1992) NTSYS-PC: Numerical taxonomy and multivariate analysis system. Exeter Software, Setauket
Schaffner U (2001) Host range testing of insects for biological weed control: how can it be better interpreted? Bioscience 51:951–959
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
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
Suckling M, Sforza RFH (2014) What magnitude are non-target impacts from weed biocontrol? PLoS ONE 9:1–12
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
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
Werner PA (1975) A seed trap for determining patterns of seed deposition in terrestrial plants. Can J Bot 53:810–813
Whittle CA, Otto SP, Johnston MO, Krochko JE (2009) Adaptive epigenetic memory of ancestral gtemperature regime in Arabidopsis thaliana. Botany 87:650–657
Young RT (1907) The forest formations of Boulder County, Colorado. Bot Gaz 44:321–352
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
Corresponding author
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.
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-021-02480-0