Genetic evidence for plural introduction pathways of the invasive weed Paterson’s curse (Echium plantagineum L.) to southern Australia
Autoři:
Xiaocheng Zhu aff001; David Gopurenko aff002; Miguel Serrano aff003; Mark A. Spencer aff004; Petrus J. Pieterse aff005; Dominik Skoneczny aff006; Brendan J. Lepschi aff007; Manuel J. Reigosa aff008; Geoff M. Gurr aff001; Ragan M. Callaway aff009; Leslie A. Weston aff001
Působiště autorů:
Graham Centre for Agricultural Innovation (Charles Sturt University and NSW Department of Primary Industries), Charles Sturt University, Wagga Wagga, Australia
aff001; NSW Department of Primary Industries, Wagga Wagga Agricultural Institute, Wagga Wagga, Australia
aff002; Department of Botany, Faculty of Pharmacy, University of Santiago de Compostela, Santiago de Compostela, Spain
aff003; Department of Life Sciences, Natural History Museum, London, United Kingdom
aff004; Department of Agronomy, Stellenbosch University, Private bag X1, Matieland, South Africa
aff005; Department of Biochemistry and Molecular Biology, University of Melbourne, Melbourne, Australia
aff006; Australian National Herbarium, Centre for Australian National Biodiversity Research, Canberra, Australia
aff007; Department of Plant Biology and Soil Science, Faculty of Biology, University of Vigo, Vigo, Pontevedra, Spain
aff008; Division of Biological Sciences, University of Montana, Missoula, Montana, United States of America
aff009
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222696
Souhrn
Paterson’s curse (Echium plantagineum L. (Boraginaceae)), is an herbaceous annual native to Western Europe and northwest Africa. It has been recorded in Australia since the 1800’s and is now a major weed in pastures and rangelands, but its introduction history is poorly understood. An understanding of its invasion pathway and subsequent genetic structure is critical to the successful introduction of biological control agents and for provision of informed decisions for plant biosecurity efforts. We sampled E. plantagineum in its native (Iberian Peninsula), non-native (UK) and invaded ranges (Australia and South Africa) and analysed three chloroplast gene regions. Considerable genetic diversity was found among E. plantagineum in Australia, suggesting a complex introduction history. Fourteen haplotypes were identified globally, 10 of which were co-present in Australia and South Africa, indicating South Africa as an important source population, likely through contamination of traded goods or livestock. Haplotype 4 was most abundant in Australia (43%), and in historical and contemporary UK populations (80%), but scarce elsewhere (< 17%), suggesting that ornamental and/or other introductions from genetically impoverished UK sources were also important. Collectively, genetic evidence and historical records indicate E. plantagineum in southern Australia exists as an admixture that is likely derived from introduced source populations in both the UK and South Africa.
Klíčová slova:
Biology and life sciences – Genetics – Plant genetics – Heredity – Genetic mapping – Haplotypes – Plant science – Evolutionary biology – People and places – Population biology – Geographical locations – Europe – Population genetics – Africa – South Africa – Oceania – Australia – Earth sciences – Geography – Ecology and environmental sciences – Phylogeography – Biogeography – Species colonization – Invasive species
Zdroje
1. Pimentel D. Biological invasions: economic and environmental costs of alien plant, animal, and microbe species. Boca Raton: CRC Press; 2002. 384 p.
2. Cristescu ME. Genetic reconstructions of invasion history. Mol Ecol. 2015;24(9):2212–25. Epub 2015/02/24. doi: 10.1111/mec.13117 25703061.
3. Mooney HA, Cleland EE. The evolutionary impact of invasive species. PNAS. 2001;98(10):5446–51. doi: 10.1073/pnas.091093398 11344292
4. Novak SJ, Mack RN. Tracing Plant Introduction and Spread: Genetic Evidence from Bromus tectorum (Cheatgrass): Introductions of the invasive grass Bromus tectorum worldwide were broadly similar and closely tied to patterns of European human immigration. BioScience. 2001;51(2):114–22. doi: 10.1641/0006-3568(2001)051[0114:Tpiasg]2.0.Co;2
5. Wilson JR, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM. Something in the way you move: dispersal pathways affect invasion success. Trends Ecol Evol. 2009;24(3):136–44. Epub 2009/01/31. doi: 10.1016/j.tree.2008.10.007 19178981.
6. Faulkner KT, Robertson MP, Rouget M, Wilson JRU. Understanding and managing the introduction pathways of alien taxa: South Africa as a case study. Biol Invasions. 2016;18(1):73–87. doi: 10.1007/s10530-015-0990-4
7. Estoup A, Guillemaud T. Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol. 2010;19(19):4113–30. doi: 10.1111/j.1365-294X.2010.04773.x 20723048
8. Tatem AJ, Hay SI, Rogers DJ. Global traffic and disease vector dispersal. PNAS. 2006;103(16):6242–7. doi: 10.1073/pnas.0508391103 16606847
9. Work TT, McCullough DG, Cavey JF, Komsa R. Arrival rate of nonindigenous insect species into the United States through foreign trade. Biol Invasions. 2005;7(2):323. doi: 10.1007/s10530-004-1663-x
10. Barker BS, Andonian K, Swope SM, Luster DG, Dlugosch KM. Population genomic analyses reveal a history of range expansion and trait evolution across the native and invaded range of yellow starthistle (Centaurea solstitialis). Mol Ecol. 2017;26(4):1131–47. doi: 10.1111/mec.13998 WOS:000394999200014. 28029713
11. Keller SR, Gilbert KJ, Fields PD, Taylor DR. Bayesian inference of a complex invasion history revealed by nuclear and chloroplast genetic diversity in the colonizing plant, Silene latifolia. Mol Ecol. 2012;21(19):4721–34. doi: 10.1111/j.1365-294X.2012.05751.x WOS:000309234300008. 22943057
12. Michaelides SN, While GM, Zajac N, Uller T. Widespread primary, but geographically restricted secondary, human introductions of wall lizards, Podarcis muralis. Mol Ecol. 2015;24(11):2702–14. doi: 10.1111/mec.13206 25891955
13. Darling JA, Bagley MJ, Roman JOE, Tepolt CK, Geller JB. Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Mol Ecol. 2008;17(23):4992–5007. doi: 10.1111/j.1365-294X.2008.03978.x 19120987
14. Lawson Handley L-J, Estoup A, Evans DM, Thomas CE, Lombaert E, Facon B, et al. Ecological genetics of invasive alien species. BioControl. 2011;56(4):409–28. doi: 10.1007/s10526-011-9386-2
15. Shaik RS, Zhu X, Clements DR, Weston LA. Understanding invasion history and predicting invasive niches using genetic sequencing technology in Australia: case studies from Cucurbitaceae and Boraginaceae. Conservation Physiology. 2016. doi: 10.1093/conphys/cow030 27766152
16. de Bolòs O, Bonada JV. Flora dels països catalans: Pirolàcies-compostes. Barcelona: Barcino; 1995. 1227 p.
17. Loudon JC. Loudon's hortus britannicus: a catalogue of all the plants indigenous, cultivated in, or introduced to Britain. London: Printed for Longman, Rees, Orme, Brown, and Green; 1830. 576 p.
18. Kloot PM. The naturalization of Echium plantagineum L. in Australia. Australian Weeds. 1982;1(4):29–31.
19. Retief E, Van Wyk AE. The genus Echium (Boraginaceae) in southern Africa. Bothalia. 1998;28(2):167–77. WOS:000077555500005.
20. Zhu X, Weston PA, Skoneczny D, Gopurenko D, Meyer L, Lepschi BJ, et al. Ecology and genetics affect relative invasion success of two Echium species in southern Australia. Scientific Reports. 2017;7:srep42792. doi: 10.1038/srep42792 28211478
21. Henderson L. Alien Weeds and Invasive Plants: A Complete Guide to Declared Weeds and Invaders in South Africa, Including Another 36 Species Invasive in that Region: Plant Protection Research Institute; 2001. 300 p.
22. USDA. Weed Risk Assessment for Echium plantagineum L. (Boraginaceae)-Paterson's Curse: United States Department of Agriculture; 2017 [cited 2019 July 5th].
23. Piggin CM. The biology of Australian weeds. 8. Echium plantagineum L. Journal of the Australian Institute of Agricultural Science. 1982;48(1):3–16. WOS:A1982PZ88700001.
24. NRM SatSTCA. Paterson's Curse 2009 [25th January 2016]. Available from: http://www.nrmsouth.org.au/wp-content/uploads/2014/10/patersons_curse.pdf
25. Skoneczny D, Weston PA, Zhu X, Gurr GM, Callaway RM, Weston LA. Metabolomic profiling of pyrrolizidine alkaloids in foliar of two Echium spp. invaders in Australia–a case of novel weapons? International Journal of Molecular Sciences. 2015;16(11):26721–37. doi: 10.3390/ijms161125979 26561809
26. Weston P, Weston L, Hildebrand S. Metabolic profiling in Echium plantagineum: presence of bioactive pyrrolizidine alkaloids and napthoquinones from accessions across southeastern Australia. Phytochem Rev. 2013;12(4):831–7. doi: 10.1007/s11101-013-9306-4
27. Weston LA, Weston PA, McCully M. Production of bioactive naphthoquinones by roots of Paterson's Curse (Echium plantagineum L.)–implications for invasion success? In: Adkins S, McFadden R, editors. 23rd Asian-Pacific Weed Science Society Conference; Cairns, Australia2011. p. 576–84.
28. Zhu X, Skoneczny D, Weidenhamer JD, Mwendwa JM, Weston PA, Gurr GM, et al. Identification and localization of bioactive naphthoquinones in the roots and rhizosphere of Paterson’s curse (Echium plantagineum), a noxious invader. J Exp Bot. 2016;67(12):3777–88. doi: 10.1093/jxb/erw182 27194735
29. Burdon JJ, Brown AHD. Population genetics of Echium plantagineum L.-target weed for biological control. Australian Journal of Biological Sciences. 1986;39(4):369–78. WOS:A1986F547800006.
30. Piggin CM. The herbaceous species of Echium (Boraginaceae) naturalized in Australia. Muelleria. 1977;3:215–44.
31. Massy C. The Australian merino: the story of a nation. Rev. and updated. ed. North Sydney, N.S.W.: Random House Australia; 2007.
32. Rivas-Martínez S, Penas Á, Díaz González TE, Cantó P, del Río S, Costa JC, et al. Biogeographic Units of the Iberian Peninsula and Baelaric Islands to District Level. A Concise Synopsis. In: Loidi J, editor. The Vegetation of the Iberian Peninsula: Volume 1. Cham: Springer International Publishing; 2017. p. 131–88.
33. Gopurenko D, Fletcher M, Locker H, Mitchell A. Morphological and DNA barcode species identifications of leafhoppers, planthoppers and treehoppers (Hemiptera: Auchenorrhyncha) at Barrow Island. Records of Western Australian Museum. 2013;83:253–85.
34. Zhu X, Meyer L, Gopurenko D, Weston PA, Gurr GM, Callaway RM, et al., editors. Selection of DNA barcoding regions for identification and genetic analysis of two Echium invaders in Australia: E. plantagineum and E. vulgare. 19th Australasian Weeds Conference; 2014; Hobart, TAS, Australia: Tasmanian Weed Society.
35. Taberlet P, Gielly L, Pautou G, Bouvet J. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol. 1991;17(5):1105–9. doi: 10.1007/bf00037152 WOS:A1991GM46200017. 1932684
36. Hamilton MB. Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol. 1999;8(3):521–3. WOS:000079637800022. 10199016
37. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22(22):4673–80. PMC308517. doi: 10.1093/nar/22.22.4673 7984417
38. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series. 1999;41:95–8. citeulike-article-id:691774.
39. Bena G, Prosperi JM, Lejeune B, Olivieri I. Evolution of annual species of the genus Medicago: a molecular phylogenetic approach. Mol Phylogen Evol. 1998;9(3):552–9. Epub 1998/07/21. doi: 10.1006/mpev.1998.0493 9668004.
40. Gildenhuys E, Ellis AG, Carroll S, Le Roux JJ. From the Neotropics to the Namib: evidence for rapid ecological divergence following extreme long-distance dispersal. Bot J Linn Soc. 2015:n/a-n/a. doi: 10.1111/boj.12238
41. Villesen P. FaBox: an online toolbox for fasta sequences. Mol Ecol Notes. 2007;7(6):965–8. doi: 10.1111/j.1471-8286.2007.01821.x
42. Nei M. Molecular Evolutionary Genetics: Columbia University Press; 1987.
43. Slatkin M, Voelm L. FST in a hierarchical island model. Genetics. 1991;127(3):627. 2016058
44. Excoffier Laval LG, Schneider S. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 2005;1:47–50.
45. Petit RJ, El Mousadik A, Pons O. Identifying Populations for Conservation on the Basis of Genetic Markers. Conserv Biol. 1998;12(4):844–55. doi: 10.1111/j.1523-1739.1998.96489.x
46. Petit R. Contrib 2006 [cited 2019 July]. Available from: https://www6.bordeaux-aquitaine.inra.fr/biogeco_eng/Scientific-Production/Computer-software/Contrib-Permut/Contrib.
47. Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000;9(10):1657–9. Epub 2000/10/26. 11050560.
48. Museum NH. Echium plantagineum L.—Purple Viper's Bugloss [cited 2018 30th October]. Available from: http://www.nhm.ac.uk/our-science/data/uk-species/species/echium_plantagineum.html.
49. Lombaert E, Guillemaud T, Cornuet J-M, Malausa T, Facon B, Estoup A. Bridgehead Effect in the Worldwide Invasion of the Biocontrol Harlequin Ladybird. PLOS ONE. 2010;5(3):e9743. doi: 10.1371/journal.pone.0009743 20305822
50. Su N-Y. How to Become a Successful Invader. Fla Entomol. 2013;96(3):765–9. doi: 10.1653/024.096.0309
51. Gau RD, Merz U, Falloon RE, Brunner PC. Global genetics and invasion history of the potato powdery scab pathogen, Spongospora subterranea f.sp subterranea. Plos One. 2013;8(6):11. doi: 10.1371/journal.pone.0067944 WOS:000321148400146. 23840791
52. Gibbs PE. Taxonomic studies on the genus Echium: I. An outline revision. Lagascalia. 1971;1(1):27–82.
53. Barnard M. A history of Australia. 2nd ed. ed. Sydney: Angus and Robertson; 1963. 710 p.
54. Welsh F. A history of South Africa. London: HarperCollins; 1998. 606 p.
55. Zimmermann HG. South Africa. In: Macdonald IAW, Reaser JK, Bright C, Neville LE, Howard GW, Murphy SJ, et al., editors. Invasive alien species in southern Africa: national reports & directory of resources. Cape Town, South Africa: Global Invasive Species Programme; 2003. p. 45–69.
56. Kannan R, Shackleton CM, Uma Shaanker R. Reconstructing the history of introduction and spread of the invasive species, Lantana, at three spatial scales in India. Biol Invasions. 2013;15(6):1287–302. doi: 10.1007/s10530-012-0365-z
57. Evans KJ, Symon DE, Whalen MA, Hosking JR, Barker RM, Oliver JA. Systematics of the Rubus fruticosus aggregate (Rosaceae) and other exotic Rubus taxa in Australia. Aust Syst Bot. 2007;20(3):187–251. https://doi.org/10.1071/SB06044.
58. Clements DR, Peterson DJ, Prasad R. The biology of Canadian weeds. 112. Ulex europaeus L. Canadian Journal of Plant Science. 2001;81(2):325–37. doi: 10.4141/p99-128 CCC:000169474200017.
59. Ireson JE, Gourlay AH, Kwong RM, Holloway RJ, Chatterton WS. Host specificity, release, and establishment of the gorse spider mite, Tetranychus lintearius Dufour (Acarina: Tetranychidae), for the biological control of gorse, Ulex europaeus L. (Fabaceae), in Australia. Biol Control. 2003;26(2):117–27. doi: 10.1016/s1049-9644(02)00128-7 CCC:000181149000003.
60. Cronk QCB, Fuller JL. Plant invaders: the threat to natural ecosystems. Fuller JL, editor. London: Earthscan; 2001.
61. Correia M, Montesinos D, French K, Rodríguez-Echeverría S. Evidence for enemy release and increased seed production and size for two invasive Australian acacias. J Ecol. 2016;104(5):1391–9. doi: 10.1111/1365-2745.12612
62. Skoneczny D, Zhu X, Duran AG, Freijanes LC, Montesinos D, Serrano M, et al. A comparison of novel weapons in European and Australian Echium plantagineum populations using metabolic profiling. 8th World Congress of Allelopathy; Marseille, France: International Allelopathy Society; 2017.
63. Montesinos D, Callaway RM. Inter-regional hybrids of native and invasive Centaurea solstitialis display intermediate competitive ability. Ecography. 2017;40(7):801–2. doi: 10.1111/ecog.02653
64. Montesinos D, Callaway RM. Traits correlate with invasive success more than plasticity: A comparison of three Centaurea congeners. Ecology and Evolution. 2018;8(15):7378–85. doi: 10.1002/ece3.4080 30151157
65. Filipe JC, Montesinos D. Inter-regional hybrids of native and non-native Centaurea sulphurea inherit increased competitive ability from the non-natives. Plant Ecology & Diversity. 2016;9(4):381–6. doi: 10.1080/17550874.2016.1261950
66. Pyšek P, Jarošík V, Pergl J. Alien plants introduced by different pathways differ in invasion success: unintentional introductions as a threat to natural areas. PloS one. 2011;6(9):e24890–e. Epub 2011/09/15. doi: 10.1371/journal.pone.0024890 21949778.
67. Dehnen-Schmutz K, Touza J, Perrings C, Williamson M. A century of the ornamental plant trade and its impact on invasion success. Divers Distrib. 2007;13(5):527–34. doi: 10.1111/j.1472-4642.2007.00359.x
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