Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-30T00:44:30.825Z Has data issue: false hasContentIssue false

Genetic comparison of introduced and native populations of common buckthorn (Rhamnus cathartica), a woody shrub introduced into North America from Europe

Published online by Cambridge University Press:  27 April 2020

Alexis Wafer
Affiliation:
Undergraduate Research Associate, Department of Biological Sciences, University of Cincinnati, OH, USA
Theresa M. Culley*
Affiliation:
Professor, Department of Biological Sciences, University of Cincinnati, OH, USA
Kala Stephens
Affiliation:
Undergraduate Research Associate, Department of Biological Sciences, University of Cincinnati, OH, USA
J. Ryan Stewart
Affiliation:
Professor, Department of Plant and Wildlife Sciences, Brigham Young University, Provo, UT, USA
*
Author for correspondence: Theresa M. Culley, Department of Biological Sciences, 614 Rieveschl Hall, University of Cincinnati, OH45221-0006. (Email: theresa.culley@uc.edu)

Abstract

Introduced from Europe to North America in the early 19th century as an ornamental shrub and for medicinal purposes, common buckthorn (Rhamnus cathartica L.) has since spread and naturalized throughout regions of the United States and Canada. The purpose of this study was to investigate levels of genetic variation and population differentiation in R.cathartica in its introduced range in North America compared with its native range in Europe to better understand patterns of spread. By analyzing introduced and native populations using microsatellite markers, we found that introduced populations generally exhibited similar or slightly lower levels of genetic variation compared with native populations, consistent with a slight bottleneck effect. Introduced populations contained many different genotypes, indicating genetic admixture, rather than one or few genotypes. In a few cases, populations had been misidentified in the field and were glossy buckthorn (Frangula alnus Mill.; syn. Rhamnus frangula L.). Overall, there was no substantial genetic differentiation detected between native and introduced populations of R. cathartica. Invasive spread in this species is likely due to its past horticultural history as well as adaptive biological traits such as competitive behavior, potential allelopathy, and seed dispersal via birds.

Type
Research Article
Copyright
© Weed Science Society of America, 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Associate Editor: Marie Jasieniuk, University of California, Davis

References

Ahmad, R, Liow, P, Spencer, DF, Jasieniuk, M (2008) Molecular evidence for a single genetic clone of invasive Arundo donax in the United States. Aquat Bot 88:113120CrossRefGoogle Scholar
Allendorf, FW, Lundquist, LL (2003) Introduction: population biology, evolution and control of invasive species. Conserv Biol 17:2430CrossRefGoogle Scholar
Anonymous (2019) Identification Comparisons of Invasive Buckthorn to Native Plants in NE Minnesota. http://www.1854treatyauthority.org/images/IDComparisonsofInvasiveBuckthorn&HoneysuckletoNativePlantsinNEMN.pdf Accessed: April 30, 2020Google Scholar
Archibold, OW, Brooks, D, Delanoy, L (1997) An investigation of the invasive shrub European buckthorn, Rhamnus cathartica L. near Saskatoon, Saskatchewan. Can Field Nat 111:617621Google Scholar
Brodersen, C, Lavergne, S, Molofsky, J (2008) Genetic variation in photosynthetic characteristics among invasive and native populations of reed canarygrass (Phalaris arundinacea). Biol Invasions 10:13171325CrossRefGoogle Scholar
Cornuet, JM, Luikart, G (1997) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:20012014Google Scholar
Culley, T, Stewart, J (2010) Microsatellite primers in Rhamnus cathartica (Rhamnaceae) and applicability in related taxa to assess hybridization events. Am J Bot 97:e7e9CrossRefGoogle ScholarPubMed
Culley, TM, Stamper, TI, Stokes, RL, Brzyski, JR, Hardiman, NA, Klooster, MR, Merritt, BJ (2013) An efficient technique for primer development and application that integrates fluorescent labeling and multiplex PCR. Appl Plant Sci 1:1300027CrossRefGoogle ScholarPubMed
De Kort, H, Mergeay, J, Jacquemyn, H, Honnay, O (2016) Transatlantic invasion routes and adaptive potential in North American populations of the invasive glossy buckthorn, Frangula alnus. Ann Bot 118:10891099CrossRefGoogle ScholarPubMed
Dirr, MA (1998) Manual of Woody Landscape Plants: Their Identification, Ornamental Characteristics, Culture, Propagation and Uses. 5th ed. Champaign, IL: Stipes. 1187 pGoogle Scholar
Dlugosch, KM, Anderson, SR, Braasche, J, Cang, FA, Gillette, HD (2015) The devil is in the details: genetic variation in introduced populations and its contributions to invasion. Mol Ecol 24:20952111CrossRefGoogle Scholar
Doyle, JJ, Doyle, JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:1115Google Scholar
Dukes, JS, Pntius, J, Orwig, D, Garnas, JR, Rodgers, VL, Brazee, N, Cooke, B, Theoharides, KA, Stange, EE, Harrington, R, Ehrenfeld, J, Gurevitch, J, Lerdau, M, Stinson, K, Wick, R, Ayres, M (2009) Responses of insect rests, pathogens, and invasive plant species to climate change in the forests of northeastern North America: what can we predict? Can J For Res 39:231248CrossRefGoogle Scholar
Durka, W, Bossdorf, O, Prati, D, Auge, H (2005) Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol Ecol 14:16971706CrossRefGoogle Scholar
Estoup, A, Ravigné, V, Hufauer, R, Vitalis, R, Gautier, M, Facon, B (2016) Is there a genetic paradox of biological invasion. Annu Rev Ecol Syst 47:5172CrossRefGoogle Scholar
Gale, SW (2000) Control of the invasive exotic Rhamnus cathartica in temperate North American forests. St Paul: Department of Horticultural Science, University of Minnesota. http://hdl.handle.net/11299/60097. Accessed: April 30, 2020Google Scholar
Godwin, H (1936) Studies in ecology of Wicken Fen: III. The establishment and development of fen scrub (carr). J Ecol 28:82116CrossRefGoogle Scholar
Godwin, H (1943) Rhamnaceae – Rhamnus cathartica L., Frangula alnuc Miller (Rhamnus frangula L.) part of The Biological Flora of the British Isles. J Ecol 31:6676CrossRefGoogle Scholar
Hale, ML, Burg, TM, Steeves, TE (2012) Sampling for microsatellite-based population genetic studies: 25 to 30 individuals per population is enough to accurately estimate allele frequencies. PLoS ONE 7:e45170CrossRefGoogle ScholarPubMed
Heidorn, R (1990) Vegetation Management Guideline: Exotic Buckthorns. Springfield: Illinois Nature Preserves Commission: Vegetation Management Guide 1(5). 5 pGoogle Scholar
Heimpel, GE, Frelich, LE, Landis, DA, Hopper, KR, Hoelmer, KA, Sezen, Z, Asplen, MK, Wu, K (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol Invasions 12:29132931CrossRefGoogle Scholar
King, M, Altdorff, S, Li, P, Galagedara, L, Holden, J, Unc, A (2018) Northward shift of the agricultural climate zone under 21st-century global climate change. Nature 8:7904Google ScholarPubMed
Klionsky, S, Amatangelo, K, Waller, D (2011) Above- and belowground impacts of European buckthorn (Rhamnus cathartica) on four native forbs. Restor Ecol 19:728736CrossRefGoogle Scholar
Knight, K, Kurylo, J, Endress, A, Stewart, J, Reich, P (2007) Ecology and ecosystem impacts of common buckthorn (Rhamnus cathartica): a review. Biol Invasions 9:925937CrossRefGoogle Scholar
Kurylo, J, Endress, A (2012) Rhamnus cathartica: notes on its early history in North America. Northeast Nat 19:601610CrossRefGoogle Scholar
Lavergne, S, Molofsky, J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:38833888CrossRefGoogle ScholarPubMed
Meyerson, LA, Viola, DV, Brown, RN (2010) Hybridization of invasive Phragmites australis with a native subspecies in North America. Biol Invasions 12:102111CrossRefGoogle Scholar
Nybom, H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:11431155CrossRefGoogle ScholarPubMed
Peakall, R, Smouse, PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6:288295CrossRefGoogle Scholar
Peakall, R, Smouse, PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:25372539CrossRefGoogle ScholarPubMed
Proven Winners (2019) Fine Line® Buckthorn Rhamnus frangula. https://www.provenwinners.com/plants/rhamnus/fine-line-buckthorn-rhamnus-frangula. Accessed: April 30, 2020Google Scholar
Quinn, L, Culley, T, Stewart, JR (2012) Genetic comparison of introduced and native populations of Miscanthus sinensis (Poaceae), a potential bioenergy crop. Grassland Sci 58:101111CrossRefGoogle Scholar
R Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical ComputingGoogle Scholar
Reichard, SH (1994) Assessing the potential of invasiveness in woody plants introduced to North America. Ph.D. thesis. Seattle: University of Washington. 205 pGoogle Scholar
Reichard, SH, White, P (2001) Horticulture as a pathway of invasive plant introductions in the United States. Biosci 51:103113CrossRefGoogle Scholar
Robarts, DWG, Wolfe, AD (2014) Sequence-related amplified polymorphism (SRAP)markers: a potential resource for studies in plant molecular biology. Appl Plant Sci 2:apps.1400017CrossRefGoogle ScholarPubMed
Roth, AM, Whitfeld, TJS, Lodge, AG, Eisenhauer, N, Frelich, LE, Reich, PB (2014) Invasive earthworms interact with abiotic conditions to influence the invasion of common buckthorn (Rhamnus cathartica). Oecologia 178:219230CrossRefGoogle Scholar
Sakai, AK, Allendorf, FW, Holt, JS, Lodge, DM, Molofsky, J, Kimberly, A, With, K, Baughman, S, Cabin, RJ, Cohen, JE, Ellstrand, NE, McCauley, DE, O’Neil, P, Parker, IM, Thompson, JN, Weller, SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305332CrossRefGoogle Scholar
Saltonstall, K, Castillo, HE, Blossey, B (2014) Confirmed field hybridization of native and introduced Phragmites australis (Poaceae) in North America. Am J Bot 101:211214CrossRefGoogle Scholar
Seltzner, S, Eddy, TL (2003) Allelopathy in Rhamnus cathartica, European buckthorn. Great Lakes Bot 42:5161Google Scholar
Stewart, JR, Graves, WR, Landes, RD (2006) Cold hardiness and vernal budbreak of Rhamnus caroliniana and the invasive Rhamnus cathartica. J Am Soc Hort Sci 131:345351CrossRefGoogle Scholar
Warren, RJ, Labatore, A, Candeias, M (2017) Allelopathic invasive tree (Rhamnus cathartica) alters native plant communities. Plant Ecol 218:12331241CrossRefGoogle Scholar
Wyckoff, PH, Shaffer, A, Hucka, B, Bombyk, M, Wipd, A (2014) No evidence of facilitation between invasive Rhamnus cathartica (European buckthorn) and invasive earthworms in west central Minnesota. Pedobiologia 57:311317CrossRefGoogle Scholar
Zhang, J, Yi, Q, Xing, F, Tang, C, Wang, L, Ye, W, Ng, II, Chan, TI, Chen, H, Liu, D (2018) Rapid shifts of peak flowering phenology in 12 species under the effects of extreme climate events in Macao. Nature 8:13950Google ScholarPubMed
Ziter, C, Turner, MG (2019) No evidence of co-facilitation between a non-native Asian earthworm (Amynthas tokioensis) and invasive common buckthorn (Rhamnus cathartica) in experimental mesocosms. Biol Invasions 21:111122CrossRefGoogle Scholar