Chloroplast DNA analysis of the invasive weed, Himalayan balsam (Impatiens glandulifera), in the British Isles

Clements, D. R., Feenstra, K. R., Jones, K. & Staniforth, R. The biology of invasive alien plants in Canada. 9. Impatiens glandulifera Royle. Can. J. Plant Sci. 88, 403–417. https://doi.org/10.4141/CJPS06040 (2008).

Article  Google Scholar 

2Cockel, C. P. & Tanner, R. A. Impatiens glandulifera Royle (Himalayan balsam) in A Handbook of Global Freshwater Invasive Species (ed Francis, R. A.) 67–77 (Earthscan, London, 2011).

Prentis, P. J. et al. Understanding invasion history: genetic structure and diversity of two globally invasive plants and implications for their management. Divers. Distrib. 15, 822–830. https://doi.org/10.1111/j.1472-4642.2009.00592.x (2009).

Article  Google Scholar 

Beerling, D. J. & Perrins, J. M. Impatiens glandulifera Royle (Impatiens roylei Walp). J. Ecol. 81, 367–382. https://doi.org/10.2307/2261507 (1993).

Article  Google Scholar 

Tanner, R. A. An Ecological Assessment of Impatiens glandulifera in its Introduced and Native Range and the Potential for its Classical Biological Control. Ph.D thesis thesis, Royal Holloway, University of London, London (2011).

Morgan, R. J. Impatiens: The Vibrant World of Busy Lizzies, Balsams, and Touch-Me-Nots (Timber Press, Oregon, 2007).

Google Scholar 

Hulme, P. E. & Bremner, E. T. Assessing the impact of Impatiens glandulifera on riparian habitats: partitioning diversity components following species removal. J. Appl. Ecol. 43, 43–50. https://doi.org/10.1111/j.1365-2664.2005.01102.x (2006).

Article  Google Scholar 

Tanner, R. A. et al. Impacts of an invasive non-native annual weed, Impatiens glandulifera, on above-and below-ground invertebrate communities in the United Kingdom. PLoS ONE 8, e67271. https://doi.org/10.1371/journal.pone.0067271 (2013).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Pattison, Z. et al. Positive plant–soil feedbacks of the invasive Impatiens glandulifera and their effects on above-ground microbial communities. Weed Res. 56, 198–207. https://doi.org/10.1111/wre.12200 (2016).

CAS  Article  Google Scholar 

Chittka, L. & Schürkens, S. Successful invasion of a floral market. Nature 411, 653. https://doi.org/10.1038/35079676 (2001).

ADS  CAS  Article  PubMed  Google Scholar 

Greenwood, P. & Kuhn, N. J. Does the invasive plant, Impatiens glandulifera, promote soil erosion along the riparian zone? An investigation on a small watercourse in northwest Switzerland. J. Soils Sed. 14, 637–650. https://doi.org/10.1007/s11368-013-0825-9 (2014).

Article  Google Scholar 

Tanner, R. A. et al. Puccinia komarovii var. glanduliferae var. nov.: a fungal agent for the biological control of Himalayan balsam (Impatiens glandulifera). Eur. J. Plant Pathol. 141, 247–266. https://doi.org/10.1007/s10658-014-0539-x (2015).

Article  Google Scholar 

Varia, S., Pollard, K. & Ellison, C. Implementing a novel weed management approach for Himalayan balsam: progress on biological control in the UK. Outlooks Pest Manage. 27, 198–203. https://doi.org/10.1564/v27_oct_02 (2016).

Article  Google Scholar 

Ellison, C. A., Pollard, K. M. & Varia, S. Potential of a coevolved rust fungus for the management of Himalayan balsam in the British Isles: first field releases. Weed Res. 60, 37–49. https://doi.org/10.1111/wre.12403 (2020).

Article  Google Scholar 

Ellison, C. A., Evans, H. C. & Ineson, J. The significance of intraspecies pathogenicity in the selection of a rust pathotype for the classical biological control of Mikania micrantha (mile-a-minute weed) in Southeast Asia. In Proceedings of the XI International Symposium on Biological Control of Weeds (eds Cullen, J. M. et al.) 102–107 (CSIRO Entomology, Canberra, 2004).

Google Scholar 

Smith, L. et al. The importance of cryptic species and subspecific populations in classic biological control of weeds: a North American perspective. Biocontrol 63, 417–425. https://doi.org/10.1007/s10526-017-9859-z (2018).

Article  Google Scholar 

Thrall, P. H. & Burdon, J. J. Host–pathogen life history interactions affect biological control success. Weed Technol. 18, 1269–1274. https://doi.org/10.1614/0890-037X(2004)018[1269:HLHIAB]2.0.CO;2 (2004).

Article  Google Scholar 

Gaskin, J. F. et al. Applying molecular-based approaches to classical biological control of weeds. Biol. Control 58, 1–21. https://doi.org/10.1016/j.biocontrol.2011.03.015 (2011).

CAS  Article  Google Scholar 

St. Quinton, J. M., Fay, M., Ingrouille, M. & Faull, J. Characterisation of Rubus niveus: a prerequisite to its biological control in oceanic islands. Biocontrol Sci. Technol. 21, 733–752. https://doi.org/10.1080/09583157.2011.570429 (2011).

Article  Google Scholar 

Goolsby, J. A., Van Klinken, R. D. & Palmer, W. A. Maximising the contribution of native-range studies towards the identification and prioritisation of weed biocontrol agents. Aust. J. Entomol. 45, 276–286. https://doi.org/10.1111/j.1440-6055.2006.00551.x (2006).

Article  Google Scholar 

Nissen, S. J., Masters, R. A., Lee, D. J. & Rowe, M. L. DNA-based marker systems to determine genetic diversity of weedy species and their application to biocontrol. Weed Sci. 43, 504–513. https://doi.org/10.1017/S0043174500081546 (1995).

CAS  Article  Google Scholar 

Gaskin, J. F., Zhang, D. Y. & Bon, M. C. Invasion of Lepidium draba (Brassicaceae) in the western United States: distributions and origins of chloroplast DNA haplotypes. Mol. Ecol. 14, 2331–2341. https://doi.org/10.1111/j.1365-294X.2005.02589.x (2005).

CAS  Article  PubMed  Google Scholar 

Morin, L. & Hartley, D. Routine use of molecular tools in Australian weed biological control programmes involving pathogens. In Proceeding of the XIIth International Symposium on Biological Control of Weeds (eds Julien, M. H. et al.) (CAB International, Wallingford, 2008).

Google Scholar 

Paterson, I. D., Downie, D. A. & Hill, M. P. Using molecular methods to determine the origin of weed populations of Pereskia aculeata in South Africa and its relevance to biological control. Biol. Control 48, 84–91. https://doi.org/10.1016/j.biocontrol.2008.09.012 (2009).

CAS  Article  Google Scholar 

Sutton, G., Paterson, I. & Paynter, Q. Genetic matching of invasive populations of the African tulip tree, Spathodea campanulata Beauv. (Bignoniaceae), to their native distribution: Maximising the likelihood of selecting host-compatible biological control agents. Biol. Control 114, 167–175. https://doi.org/10.1016/j.biocontrol.2017.08.015 (2017).

Article  Google Scholar 

Saltonstall, K. Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc. Natl. Acad. Sci. 99, 2445–2449 (2002).

ADS  CAS  Article  Google Scholar 

Trewick, S. A., Morgan-Richards, M. & Chapman, H. M. Chloroplast DNA diversity of Hieracium pilosella (Asteraceae) introduced to New Zealand: reticulation, hybridization, and invasion. Am. J. Bot. 91, 73–85 (2004).

CAS  Article  Google Scholar 

Love, H. M., Maggs, C. A., Murray, T. E. & Provan, J. Genetic evidence for predominantly hydrochoric gene flow in the invasive riparian plant Impatiens glandulifera (Himalayan balsam). Ann. Bot. 112, 1743–1750. https://doi.org/10.1093/aob/mct227 (2013).

Article  PubMed  PubMed Central  Google Scholar 

Hagenblad, J. et al. Low genetic diversity despite multiple introductions of the invasive plant species Impatiens glandulifera in Europe. BMC Genet. 16, 103. https://doi.org/10.1186/s12863-015-0242-8 (2015).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Nagy, A.-M. & Korpelainen, H. Population genetics of Himalayan balsam (Impatiens glandulifera): comparison of native and introduced populations. Plant Ecol. Divers. 8, 317–321. https://doi.org/10.1080/17550874.2013.863407 (2015).

Article  Google Scholar 

31Barrett, S. Genetic variation in weeds. In Biological control of weeds with plant pathogens (eds Charudattan, R. & Walker, H.) 73–98 (1982).

Burdon, J. & Marshall, D. Biological control and the reproductive mode of weeds. J. Appl. Ecol. https://doi.org/10.2307/2402423 (1981).

Article  Google Scholar 

Charudattan, R. Ecological, practical, and political inputs into selection of weed targets: what makes a good biological control target?. Biol. Control 35, 183–196. https://doi.org/10.1016/j.biocontrol.2005.07.009 (2005).

Article  Google Scholar 

Wickham, H. ggplot2: elegant graphics for data analysis (Springer, New York, 2016).

Google Scholar 

Dunnington, D. ggspatial: spatial data framework for ggplot2. https://cran.r-project.org/package=ggspatial (2018).

Pebesma, E. Simple features for R: standardized support for spatial vector data. R J. 10, 439–446. https://doi.org/10.32614/RJ-2018-009 (2018).

Article  Google Scholar 

South, A. R natural earth: world map data from natural earth. https://CRAN.R-project.org/package=rnaturalearth (2017).

South, A. rnaturalearthdata: world vector map data from Natural Earth used in ‘rnaturalearth’. https://CRAN.R-project.org/package=rnaturalearthdata (2017).

R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/ (2018).

QGIS Development Team. QGIS Geographic Information System. Open Source Geospatial Foundation Project. https://qgis.osgeo.org/ (2020).

Hasan, S. Search in Greece and Turkey for Puccinia chondrillina strains suitable to Australian forms of skeleton weed. In Proceeding of the VI International Symposium on Biological Control of Weeds (ed. Delfosse, E. S.) 625–632 (Canada Agriculture, Ottawa, 1985).

Google Scholar 

Kress, W. J. et al. Use of DNA barcodes to identify flowering plants. Proc. Natl. Acad. Sci. USA 102, 8369–8374. https://doi.org/10.1073/pnas.0503123102 (2005).

ADS  CAS  Article  PubMed  Google Scholar 

Birky, C. W. Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc. Natl. Acad. Sci. USA 92, 11331–11338. https://doi.org/10.1073/pnas.92.25.11331 (1995).

ADS  CAS  Article  PubMed  Google Scholar 

Provan, J., Powell, W. & Hollingsworth, P. M. Chloroplast microsatellites: new tools for studies in plant ecology and evolution. Trends Ecol. Evol. 16, 142–147. https://doi.org/10.1016/S0169-5347(00)02097-8 (2001).

CAS  Article  PubMed  Google Scholar 

Fry, C. The Plant Hunters (Andre Deutsch, London, 2017).

Google Scholar 

Jukonienė, I., Subkaitė, M. & Ričkienė, A. Herbarium data on bryophytes from the eastern part of Lithuania (1934–1940) in the context of science history and landscape changes. Botanica 25, 41–53. https://doi.org/10.2478/botlit-2019-0005 (2019).

Article  Google Scholar 

Janssens, S. B. et al. Rapid radiation of Impatiens (Balsaminaceae) during Pliocene and Pleistocene: result of a global climate change. Mol. Phylogen. Evol. 52, 806–824. https://doi.org/10.1016/j.ympev.2009.04.013 (2009).

CAS  Article  Google Scholar 

Barreto, R. W., Ellison, C. A., Seier, M. K. & Evans, H. C. Biological control of weeds with plant pathogens: four decades on. In Integrated Pest Management: Principles and Practice (eds Abrol, D. P. & Shankar, U.) 299–350 (CAB International, Wallingford, 2012).

Google Scholar 

Kniskern, J. & Rausher, M. D. Two modes of host–enemy coevolution. Popul. Ecol. 43, 3–14. https://doi.org/10.1007/PL00012012 (2001).

Article  Google Scholar 

Evans, H. C., Greaves, M. P. & Watson, A. K. Fungal biocontrol agents of weeds. In Fungi as Biocontrol Agents: Progress, Problems and Potential (eds Butt, T. M. et al.) 169–192 (CABI Publishing, Wallingford, 2001).

Google Scholar 

Cullen, J. M., Kable, P. F. & Catt, M. Epidemic spread of a rust imported for biological control. Nature 244, 463–464 (1973).

Article  Google Scholar 

Hasan, S. A new strain of the rust fungus Puccinia chondrillina for biological control of skeleton weed in Australia. Ann. Appl. Biol. 99, 119–124. https://doi.org/10.1111/j.1744-7348.1981.tb05137.x (1981).

Article  Google Scholar 

Charudattan, R. & Dinoor, A. Biological control of weeds using plant pathogens: accomplishments and limitations. Crop Protect. 19, 691–695. https://doi.org/10.1016/S0261-2194(00)00092-2 (2000).

Article  Google Scholar 

Fröhlich, J. et al. Biological control of mist flower (Ageratina riparia, Asteraceae): transferring a successful program from Hawai’i to New Zealand. In Proceeding of the X International Symposium on Biological Control of Weeds (ed. Spencer, N.) 51–57 (Montana State University, Montana, 2000).

Google Scholar 

Ellison, C. A. & Cock, M. J. W. Classical biological control of Mikania micrantha: the sustainable solution. In Invasive Alien Plants: Impacts on Development and Options for Management (eds Ellison, C. A. et al.) 162–190 (CABI, Wallingford, 2017).

Google Scholar 

Roderick, G. K. & Navajas, M. Genes in new environments: genetics and evolution in biological control. Nat. Rev. Genet. 4, 889–899. https://doi.org/10.1038/nrg1201 (2003).

CAS  Article  PubMed  Google Scholar 

Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874. https://doi.org/10.1093/molbev/msw054 (2016).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033 (2014).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542. https://doi.org/10.1093/sysbio/sys029 (2012).

Article  PubMed  PubMed Central  Google Scholar 

Tanabe, A. S. Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol. Ecol. Resour. 11, 914–921. https://doi.org/10.1111/j.1755-0998.2011.03021.x (2011).

Article  PubMed  Google Scholar 

Akaike, H. A new look at the statistical model identification. IEEE Trans. Automat. Control 19, 716–723. https://doi.org/10.1109/TAC.1974.1100705 (1974).

ADS  MathSciNet  Article  MATH  Google Scholar 

Rambaut, A., Suchard, M., Xie, D. & Drummond, A. Tracer v1.6. https://tree.bio.ed.ac.uk/software/tracer/ (2016).

Rambaut, A. FigTree ver. 1.4.3. https://tree.bio.ed.ac.uk/software/figtree (2016).

Clement, M., Posada, D. & Crandall, K. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9, 1657–1660. https://doi.org/10.1046/j.1365-294x.2000.01020.x (2000).

CAS  Article  PubMed  Google Scholar