Inferring population structure and genetic diversity of the invasive alien Nootka lupin in Iceland

  • Jakub Skorupski Institute of Marine and Environmental Sciences, University of Szczecin, Szczecin, Poland; Molecular Biology and Biotechnology Centre, University of Szczecin, Szczecin, Poland
  • Magdalena Szenejko Institute of Marine and Environmental Sciences, University of Szczecin, Szczecin, Poland; Molecular Biology and Biotechnology Centre, University of Szczecin, Szczecin, Poland
  • Martyna Gruba-Tabaka Institute of Marine and Environmental Sciences, University of Szczecin, Szczecin, Poland; Molecular Biology and Biotechnology Centre, University of Szczecin, Szczecin, Poland
  • Przemysław Śmietana Institute of Marine and Environmental Sciences, University of Szczecin, Szczecin, Poland; Molecular Biology and Biotechnology Centre, University of Szczecin, Szczecin, Poland
  • Remigiusz Panicz Faculty of Food Sciences and Fisheries, Department of Meat Technology, West Pomeranian University of Technology in Szczecin, Szczecin, Poland
Keywords: Biological invasions, genetic diversity, ITS2, Lupinus nootkatensis, population structure, nature conservation

Abstract

Polar and subpolar regions are known for their particular vulnerability and sensitivity to the detrimental effects of non-indigenous species, which is well exemplified by the Nootka lupin (Lupinus nootkatensis) spread in Iceland. Since understanding the population and ecological genetics of invasive alien species offers hope for counteracting harmful biological invasions, the objective of the present study was to investigate interspecific variation in L. nootkatensis in Iceland in relation to a native population in Alaska. Moreover, we aimed to assess whether internal transcribed spacer 2 (ITS2) has sufficient phylogenetic applicability for a large-scale screening of the genetic diversity of a non-indigenous population of this species. This study, which is the first attempt to investigate the genetic diversity of the Nootka lupin in Iceland, included plant samples from eight locations in Iceland and one in Alaska. The analyses included genotyping by sequencing of the 417-nucleotide fragment of the 5.8S ribosomal RNA, ITS2 and part of the large subunit ribosomal RNA (GenBank MT026578-MT026580, MT077004). The main findings showed the presence of five previously unexplained single-nucleotide polymorphisms (SNPs); however, their discriminatory power for Icelandic populations was relatively low, since polymorphism information content (PIC) values ranged from 0.0182 to 0.0526, with average heterozygosity 0.0296. Concomitantly, analysis of multilocus genotypes (MLG) revealed sufficient differences in MLGs variants and their frequency to form genotypic patterns unique for Alaskan and Icelandic populations, revealing an internal genetic structure of the studied group. The proposed SNP panel needs to be supplemented with other nuclear and organellar markers.

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References


Aggrey S.E. & Okimoto R. 2003. Genetic markers: prospects and applications in genetic analysis. In W.M. Muir & S.E. Aggrey (eds.): Poultry genetics, breeding and biotechnology. Pp. 419–438. Wallingford, UK: CABI Publishing.


Aïnouche A., Bayer R.J. & Misset M.-T. 2004. Molecular phylogeny, diversification and character evolution in Lupinus (Fabaceae) with special attention to Mediterranean and African lupins. Plant Systematics and Evolution 246, 211–222, doi: 10.1007/s00606-004-0149-8.


Aïnouche A.K. & Bayer R. 1999. Phylogenetic relationships in Lupinus (Fabaceae: Papilionoideae) based on internal transcribed spacer sequences (ITS) of nuclear ribosomal DNA. American Journal of Botany 86, 590–607, doi: 10.2307/2656820.


Alvarez I. & Wendel J. 2003. Ribosomal ITS sequences and plant phylogenetic inference. Molecular Phylogenetics and Evolution 29, 417–434, doi: 10.1016/S1055–7903(03)00208–2.


Atnaf M., Yao N., Martina K., Dagne K., Wegary D. & Tesfaye K. 2017. Molecular genetic diversity and population structure of Ethiopian white lupin landraces: implications for breeding and conservation. PLoS One 12, e0188696. doi: 10.1371/journal.pone.0188696.


Baldursson S. 1995. Frjóvgun og fræsenting alaskalúpínu. (Fertilization and seed set in Nootka lupin.) In B. Magnusson (ed.): Líffræði alaskalúpínu (Lupinus nootkatensis). Vöxtur, fræmyndun, efnainnihald og áhrif sláttar. (Biological studies of Nootka lupin [Lupinus nootkatensis] in Iceland. Growth, seed set, chemical content and effect of cutting.) Pp. 38–43. Reykjavik: Rannsóknastofnun Landbúnaðarins.


Balloux F., Lehmann L. & de Meeûs T. 2003. The population genetics of clonal and partially clonal diploids. Genetics 164, 1635–1644.


Benediktsson K. 2015. Floral hazards: Nootka lupin in Iceland and the complex politics of invasive life. Geografiska Annaler Series B, Human Geography 97, 139–154, doi: 10.1111/geob.12070


Bennett J.R., Shaw J.D., Terauds A., Smol J.P., Aerts R., Bergstrom D.M., Blais J.M., Cheung W.W.L., Chown S.L., Lea M.-A., Nielsen U.N., Pauly D., Reimer K.J., Riddle M.J., Snape I., Stark J.S., Tulloch V.J. & Possingham H.P. 2015. Polar lessons learned: long-term management based on shared threats in Arctic and Antarctic environments. Frontiers in Ecology and the Environment 13, 316–324, doi: 10.1890/140315.


Bińkowski J. & Miks S. 2018. Gene–Calc (computer software). Accessed on the internet at gene-calc.pl on 6 March 2020


Bjarnason H. 1981. Lúpínan frá Alaska. (Lupine from Alaska.) Lesbók Morgunblaðsins 33, 6–7.


Bohonak A.J., Davies N., Roderick G.K. & Villablanca F.X. 1998. Is population genetics mired in the past? Trends in Ecology & Evolution 13, 360, doi: 10.1016/S0169-5347(98)01422-0.


Botstein D., White R.L., Skolnick M. & Davies R.W. 1980. Construction of a genetic linkage map in man using restriction fragment length polymorphism. American Journal of Human Genetics 32, 314–331.


CAFF & PAME 2017. Arctic invasive alien species: strategy and action plan. Akureyri: The Conservation of Arctic Flora and Fauna / Protection of the Arctic Marine Environment.


Chase M.W., Cowan R.S., Hollingsworth P.M., Van den Berg C., Madrinan S., Petersen G., Seberg O., Jorgsensen T., Cameron K.M. & Carine M. 2007. A proposal for a standardised protocol to barcode all land plants. Taxonomy 56, 295–299, doi: 10.1002/tax.562004.


Chen S., Yao H., Han J., Liu C., Song J., Shi L., Zhu Y., Ma X., Gao T., Pang X., Luo K., Li Y., Li X., Jia X., Lin Y. & Leon C. 2010. Validation of the ITS2 region as a novel DNA barcode for identifying medicinal plant species. PLoS One 5, e8613, doi: 10.1371/journal.pone.0008613.


Ching A., Caldwell K.S., Jung M., Dolan M., Smith O.S., Tingey S., Morgante M. & Rafalski A.J. 2002. SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genetics 3, article no. 19, doi: 10.1186/1471–2156–3–19.


Desfeux C. & Lejeune B. 1996. Systematics of Euromediterranean silene (Caryophyllaceae): evidence from a phylogenetic analysis using ITS sequences. Comptes Rendus de l’Academie des Sciences, Paris, Sciences de le Vie/Life Sciences 319, 351–358.


Duan H., Wang W., Zeng Y., Guo M. & Zhou Y. 2019. The screening and identification of DNA barcode sequences for Rehmannia. Scientific Reports 9, article no. 17295, doi: 10.1038/s41598–019–53752–8.


Eastwood R.J., Drummond C.S., Schifino-Wittmann M.T. & Hughes C.E. 2008. Diversity and evolutionary history of Lupins—insights from new phylogenies. In J.A. Palta & J.B. Berger (eds.): Lupins for health and wealth. Proceedings of the 12th International Lupin Conference. International Lupin Association, Fremantle, Western Australia, 14–18 September 2008. Pp. 346–354. Canterbury: International Lupin Association.


El Mousadik A. & Petit R.J. 1996. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theoretical and Applied Genetics 92, 832–839, doi: 10.1007/BF00221895.


Estoup A., Ravigné V., Hufbauer R., Vitalis R., Gautier M., Facon B. 2016. Is there a genetic paradox of biological invasion? Annual Review of Ecology, Evolution, and Systematics 47, 51–72, doi: 10.1146/annurev-ecolsys-121415-032116.


Feng S., Jiang M., Shi Y., Jiao K., Shen Ch., Lu J., Ying Q. & Wang H. 2016. Application of the ribosomal DNA ITS2 region of Physalis (Solanaceae): DNA barcoding and phylogenetic study. Frontiers in Plant Science 7, article no. 1047, doi: 10.3389/fpls.2016.01047.


Finkeldey R. 1994. A simple derivation of the partitioning of genetic differentiation within subdivided populations. Theoretical and Applied Genetics 89, 198–200, doi: 10.1007/BF00225141.


Finkeldey R. & Murillo O. 1999. Contributions of subpopulations to total gene diversity. Theoretical and Applied Genetics 98, 664–668, doi: 10.1007/s001220051118.


Gallardo B., Bacher S., Bradley B., Comín F.A., Gallien L., Jeschke J.M., Sorte C.J.B. & Vilà M. 2019. InvasiBES: understanding and managing the impacts of invasive alien species on biodiversity and ecosystem services. NeoBiota 50, 109–122, doi: 10.3897/neobiota.50.35466.


Gamache I., Jaramillo-Correa J.P., Payette S. & Bousquet J. 2003. Diverging patterns of mitochondrial and nuclear DNA diversity in Subarctic black spruce: imprint of a founder effect associated with postglacial colonization. Molecular Ecology 12, 891–901, doi: 10.1046/j.1365-294X.2003.01800.x.


Goodall–Copestake W., Tarling G. & Murphy E. 2012. On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals. Heredity 109, 50–56. doi: 10.1038/hdy.2012.12.


Guðjohnsen S.K. & Magnússon B. 2019. Útbreiðsla og flatarmál lúpínubreiða á Íslandi 2017. (Distribution and area occupied by lupin in Iceland 2017.) Garðabæ: Náttúrufræðistofnun Íslands.


Hamblin M.T., Warburton M.L. & Buckler E.S. 2007. Empirical comparison of simple sequence repeats and single nucleotide polymosphism in assessment of maize diversity and relatedness. PLoS One 2, e1367, doi: 10.1371/journal.pone.0001367.


Han J., Zhu Y., Chen X., Liao B., Yao H., Song J., Chen S. & Meng F. 2013. The short ITS2 sequence serves as an efficient taxonomic sequence tag in comparison with the full-length, ITS. BioMed Research International 2013, article no. 741476, doi: 10.1155/2013/741476.


Hartl D.L. & Clark A.G. 1989. Principles of population genetics. 2nd edn. Sunderland, MA: Sinauer Associates.


Harvey-Samuel T. & Ant T. & Alphey L. 2017. Towards the genetic control of invasive species. Biological Invasions 19, 1683–1703, doi: 10.1007/s10530–017–1384–6.


Hedrick P. 2011. Genetics of populations. Sudbury, MA: Jones & Bartlett Learning.


Heuertz M., Fineschi S., Anzidei M., Pastorelli R., Salvini D., Paule L., Frascaria-Lacoste L., Hardy N., Vekemans O. & Vendramin X.G.G. 2004. Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior) in Europe. Molecular Ecology 13, 3437–3452, doi: 10.1111/j.1365-294X.2004.02333.x.


Hildebrand C.E., Torney D.C. & Wagner R.P. 1992. Informativeness of polymorphic DNA markers. Los Alamos Science 20, 100–102.


Hufnagel B., Marques A., Soriano A., Marquès L., Divol F., Doumas P., Sallet E., Mancinotti D., Carrere S., Marande W., Arribat S., Keller J., Huneau C., Blein T., Aimé D., Laguerre M., Taylor J., Schubert V., Nelson M., Geu-Flores F., Crespi M., Gallardo K., Delaux P.M., Salse J., Bergès H., Guyot R., Gouzy J. & Péret B. 2020. High-quality genome sequence of white lupin provides insight into soil exploration and seed quality. Nature Communications 11, article no. 492, doi: 10.1038/s41467–019–14197–9.


Hughes C.E., Eastwood R.J. & Bailey C.D. 2006. From famine to feast? Selecting nuclear DNA sequence loci for plant species-level phylogeny reconstruction. Philosophical Transactions of the Royal Society B 361, 211–225, doi: 10.1098/rstb.2005.1735.


Jeffries D.L., Copp G.H., Handley L.L., Olsén H.K., Sayer C.D. & Hänfling B. 2016. Comparing RADseq and microsatellites to infer complex phylogeographic patterns, an empirical perspective in the Crucian carp, Carassius carassius, L. Biological Invasions 25, 2997–3018, doi: 10.1111/mec.13613.


Jogesh T., Peery R., Downie S.R. & Berenbaum M.R. 2015. Patterns of genetic diversity in the globally invasive species wild parsnip (Pastinaca sativa). Invasive Plant Science and Management 8, 415–429, doi: 10.1614/IPSM–D–15–00024.1.


Käss E. & Wink M. 1997. Molecular phylogeny and phylogeography of Lupinus (Leguminosae) inferred from nucleotide sequences of the rbcL gene and ITS 1 + 2 regions of rDNA. Plant Systematics and Evolution 208, 139–167, doi: 10.1007/BF00985439.


Kawuki R.S., Ferguson M., Labuschagne M., Herselman L. & Kim D.-J. 2009. Identification, characterisation and application of single nucleotide polymorphisms for diversity assessment in cassava (Manihot esculenta Crantz). Molecular Breeding 23, 669–684, doi: 10.1007/s11032–009–9264–0.


Kimura M. & Crow J. 1964. The number of alleles that can be maintained in a finite population. Genetics 49, 725–738, doi: 10.1093/genetics/49.4.725.


Kollipara K.P., Singh R.J. & Hymowitz T. 1997. Phylogenetic and genomic relationships in the genus Glycine Willd. based on sequences from the ITS region of nuclear rDNA. Genome 40, 57–68, doi: 10.1139/g97-008.


Kruglyak L. 1997. The use of a genetic map of biallelic markers in linkage studies. Nature Genetics 17, 21–24, doi: 10.1038/ng0997–21.


Książkiewicz M., Nazzicari N., Yang H., Nelson M.N., Renshaw D., Rychel S., Ferrari B., Carelli M., Tomaszewska M., Stawiński S., Naganowska B., Wolko B. & Annicchiarico P. 2017. A high-density consensus linkage map of white lupin highlights synteny with narrow-leafed lupin and provides markers tagging key agronomic traits. Scientific Reports 7, article no. 15335, doi: 10.1038/s41598–017–15625–w.


Kumar S., Stecher G., Li M., Knyaz C. & Tamura K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549, doi: 10.1093/molbev/msy096.


Lawson Handley L.-J., Estoup A., Evans D.M., Thomas C.E., Lombaert E., Facon B., Aebi A. & Roy H.E. 2011. Ecological genetics of invasive alien species. Biological Control 56, 409–428, doi: 10.1007/s10526-011-9386-2.


Lewontin R.C. 1972. The apportionment of human diversity. Evolutionary Biology 6, 381–398, doi: 10.1007/978-1-4684-9063-3_14.


Li X., Yang Y., Henry R.J., Rosseto M., Wang Y. & Chen S. 2015. Plant DNA barcoding: from gene to genome. Biological Reviews 90, 157–166, doi: 10.1111/brv.12104.


Mäder G., Zamberlan P.M., Fagundes N.J.R., Magnus T., Salzano F.M., Bonatto S.L. & Freitas L.B. 2009. The use and limits of ITS data in the analysis of intraspecific variation in Passiflora L. (Passifloraceae). Genetics and Molecular Biology 33, 99–108, doi: 10.1590/S1415-47572009005000101.


Mishra P., Kumar A., Rodrigues V., Shukla A.K. & Sundaresan V. 2016. Feasibility of nuclear ribosomal region ITS1 over ITS2 in barcoding taxonomically challenging genera of subtribe Cassiinae (Fabaceae). PeerJ 4, e2638, doi: 10.7717/peerj.2638.


Nei M. 1972. Genetic distance between populations. American Naturalist 106, 283–292, doi: 10.1086/282771.


Nei M. 1973. Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences of the United States of America 70, 3321–3323, doi: 10.1073/pnas.70.12.3321.


Nei M. 1987. Molecular evolutionary genetics. New York, NY: Columbia University Press.


Nei M. & Kumar S. 2000. Molecular evolution and phylogenetics. New York, NY: Oxford University Press.


Nieto-Feliner G. & Rosselló J.A. 2007. Better the devil you know? Guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants. Molecular Phylogenetics and Evolution 44, 911–919, doi: 10.1016/j.ympev.2007.01.013.


Ohta T. 1982. Linkage disequilibrium due to random drift in finite subdivided populations. Proceedings of the National Academy of Sciences of the United States of America USA 79, 1940–1944, doi: 10.1073/pnas.79.6.1940.


Olgeirsson F.G. 2007. Sáðmenn sandanna. Saga landgræðslu á Íslandi 1907-2007. (Sowers of the sands. History of land reclamation in Iceland 1907-2007.) Gunnarsholti: Landgræðsla Ríkisins.


Ott J. 1992. Strategies for characterizing highly polymorphic markers in human gene mapping. American Journal of Human Genetics 51, 283–290.


Qin Y., Li M., Cao Y., Gao Y. & Zhang W. 2017. Molecular thresholds of ITS2 and their implications for molecular evolution and species identification in seed plants. Scientific Reports 7, article no. 17316, doi: 10.1038/s41598-017-17695-2.


Richardson D.M., Pyšek P., Rejmanek M., Barbour M.G., Panetta F.D. & West C.J. 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 6, 93–107, doi: 10.1046/j.1472-4642.2000.00083.x.


Rozas J., Ferrer-Mata A., Sánchez-DelBarrio J.C., Guirao-Rico S., Librado P., Ramos-Onsins S.E. & Sánchez-Gracia A. 2017. DnaSP 6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution 34, 3299–3302, doi: 10.1093/molbev/msx248.


Salmaso M., Faes G., Segala C., Stefanini M., Salakhutdinov I., Zyprian E., Toepfer R., Grando M.S. & Velasco R. 2004. Genome diversity and gene haplotypes in the grapevine (Vitis vinifera L) as revealed by single nucleotide polymorphisms. Molecular Breeding 14, 385–395, doi: 10.1007/s11032-004-0261-z.


Schierbeck G. 1886. Skýrsla um nokkrar tilraunir til jurtaræktunar á Íslandi. (Report on some experiments in vegetable-growing in Iceland.) Tímarit Hins Íslenska Bókmenntafélag 7, 1–66.


Shannon C.E. & Weaver W. 1949. The mathematical theory of communication. Urbana: University of Illinois Press.


Skorupski J., Szenejko M., Śmietana P., Panicz R., Keszka S., Czerniejewski P., Soroka M., Orłowska L., Albrycht M., Zatoń-Dobrowolska M., Moska M., Kirczuk L. & Rymaszewska A. 2017. Invasive alien species—identification of threats to protect biodiversity. Szczecin: Green Federation Gaia / Polish Society for Conservation Genetics Lutreola.


Smith A.L., Trevor R., Hodkinson T.R., Villellas J., Catford J.A., Csergö A.M., Blomberg S.P., Crone E.E., Ehrlén J., Garciak M.B., Lainel A-L., Roach D.A., Salguero-Gómezo R., Wardlep G.M., Childs D.Z., Elderd B.D., Finn A., Munné-Bosch S., Baudraza M.E.A, Bódis J., Brearley F.Q., Bucharova A., Caruso C.M., Duncan R.P., Dwyer J.M., Gooden B., Groenteman R., Hamre L.N., Helm A., Kelly R., Laanisto L., Lonati M., Moore J.L., Morales M., Olsen S.L., Pärtel M., Petry W.K., Ramula S., Rasmussen P.U., Enri S.R., Roeder A., Roscher Ch., Saastamoinen M., Tack A.J.M., Töpper J.P., Vose G.E., Wandrag E.M., Wingler A., Yvonne M. & Buckleya Y.M. 2020. Global gene flow releases invasive plants from environmental constraints on genetic diversity. Proceedings of the National Academy of Sciences of the United States of America 117, 4218–4227, doi: 10.1073/pnas.1915848117.


Sonnante G., Galasso I. & Pignone D. 2003. ITS sequence analysis and phylogenetic inference in the genus Lens Mill. Annales of Botany 91, 49–54, doi: 10.1093/aob/mcg007.


Stefansson R., von Schmalensee M. & Skorupski J. 2016. A tale of conquest and crisis: invasion history and status of the American mink (Neovison vison) in Iceland. Acta Biologica 23, 87–100, doi: 10.18276/ab.2016.23-08.


Stout J.C., Duffy K.J., Egan P.A., Harbourne M. & Hodkinson T.R. 2015. Genetic diversity and floral width variation in introduced and native populations of a long-lived woody perennial. AoB Plants 7, plu087, doi: 10.1093/aobpla/plu087.


Stronen A.V., Iacolina L. & Ruiz-Gonzalez A. 2019. Rewilding and conservation genomics: how developments in (re)colonization ecology and genomics can offer mutual benefits for understanding contemporary evolution. Global Ecology and Conservation 17, e00502, doi: 10.1016/j.gecco.2018.e00502.


Tajima F. 1983. Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460, doi: 10.1093/genetics/105.2.437.


Tajima F. 1989. Statistical methods to test for nucleotide mutation hypothesis by DNA polymorphism. Genetics 123, 585–595, doi: 10.1093/genetics/123.3.585.


Thorsson J. & Hlidberg K. 1997. Potential speciality products in Lupinus nootkatensis and some native Icelandic plant species. A. Quinolizidine alkaloids and the Nootka lupin. In L. Andreasen (ed.): Plant based speciality products and biopolymers. Pp. 147–155. Copenhagen: Nordic Council of Ministers.


Thuiller W., Albert C., Araújo M.B., Berry P.M., Guisan A., Hickler T., Midgley G.F., Paterson J., Schurr F.M., Sykes M.T. & Zimmermann N.E. 2008. Predicting global change impacts on plant species distributions: future challenges. Perspectives in Plant Ecology, Evolution and Systematics 9, 137–152, doi: 10.1016/j.ppees.2007.09.004.


Tollefsrud M.M., Sønstebø J.H., Brochmann C., Johnsen Ø., Skrøppa T. & Vendramin G.G. 2009. Combined analysis of nuclear and mitochondrial markers provide new insight into the genetic structure of North European Picea abies. Heredity 102, 549–562, doi: 10.1038/hdy.2009.16.


Varshney R.K., Beier U., Khlestkina E.K., Kota R., Korzun V., Graner A. & Börner A. 2007. Single nucleotide polymorphisms in rye (Secale cereale L.): discovery, frequency and application for genome mapping and diversity studies. Theoretical and Applied Genetics 114, 1105–1116, doi: 10.1007/s00122-007-0504-6.


Vetter V.M.S., Tjaden N.B., Jaeschke A., Buhk C., Wahl V., Wasowicz P. & Jentsch A. 2018. Invasion of a legume ecosystem engineer in a cold biome alters plant biodiversity. Frontiers in Plant Science 9, article no. 715, doi: 10.3389/fpls.2018.00715.


Vyšniauskienė R., Rančelienė V., Žvingila D. & Patamsytė J. 2011. Genetic diversity of invasive alien species Lupinus polyphyllus populations in Lithuania. Žemdirbystė 98, 383–390.


Wahlund S. 1928. Zusammensetzung von Population und Korrelation-serscheinung vom Standpunkt der Vererbungslehre aus betrachtet. (Composition of population and correlation phenomenon from the point of view of heredity.) Hereditas 11, 65–106, doi: 10.1111/j.1601-5223.1928.tb02483.x.


Wallace I.M., O’Sullivan O., Higgins D.G. & Notredame C. 2006. M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Research 34, 1692–1699, doi: 10.1093/nar/gkl091.


Wang X., Xu Z., Yan C., Luo W., Wang R., Han X., Jiang Y. & Li M.-H. 2017. Responses and sensitivity of N, P and mobile carbohydrates of dominant species to increased water, N and P availability in semi-arid grasslands in northern China. Journal of Plant Ecology 10, 486–496, doi: org/10.1093/jpe/rtw053.


Wang X., Zheng S. Liu Y. & Han J. 2016. ITS2, a better DNA barcode than ITS in identification of species in Artemisia L. Chinese Herbal Medicines 8, 352–358, doi: 10.1016/S1674-6384(16)60062-X.


Ward S.M., Gaskin J.F. & Wilson L.M. 2008. Ecological genetics of plant invasion: what do we know? Invasive Plant Science and Management 1, 98–109, doi: 10.1614/IPSM-07-022.1.


Wąsowicz P., Przedpelska-Wąsowicz E.M. & Kristinsson H. 2013. Alien vascular plants in Iceland: diversity, spatial patterns, temporal trends, and the impact of climate change. Flora—Morphology Distribution Functional Ecology of Plants 208, 648–673, doi: 10.1016/j.flora.2013.09.009.


Watterson G.A. 1977. Heterosis or neutrality? Genetics 85, 789–814.


Weir B.S. 1990. Genetic data analysis. Sunderland, MA: Sinauer Associates.


White T.L., Adams W.T. & Neale D.B. 2007. Forest genetics. Wallingford: CABI Publishing.


Whitlock M. & McCauley D. 1999. Indirect measures of gene flow and migration: FST≠1/(4Nm+1). Heredity 82, 117–125, doi: 10.1038/sj.hdy.6884960.


Willow J., Tamayo M. & Jóhannsson M.H. 2017. Potential impact of Nootka lupin (Lupinus nootkatensis) invasion on pollinator communities in Iceland. Icelandic Agricultural Sciences 30, 51–54, doi: 10.16886/IAS.2017.06.


Wilson J.R.U., Dormontt E.E., Prentis P.J., Lowe A.J. & Richardson D.M. 2009. Something in the way you move: dispersal pathways affect invasion success. Trends in Ecology & Evolution 24, 136–144, doi: 10.1016/j.tree.2008.10.007.


Wright S. 1931. Evolution in Mendelian populations. Genetics 16, 97–159, doi: 10.1093/genetics/16.2.97.


Wright S. 1943. Isolation by distance. Genetics 28, 114–138, doi: 10.1093/nq/184.4.114g.


Wright S. 1978. Evolution and the genetics of populations. Vol. 4. Variability within and among natural populations. Chicago, IL: University of Chicago Press.


Xu L., Myneni R.B., Chapin F.S. III, Callaghan T.V., Pinzon J.E., Tucker C.J., Zhu Z., Bi J., Ciais P., Tømmervik H., Euskirchen E.S., Forbes B.C., Piao S.L., Anderson B.T., Ganguly S., Nemani R.R., Goetz S.J., Beck P.S.A., Bunn A.G., Cao C. & Stroeve J.C. 2013. Temperature and vegetation seasonality diminishment over northern lands. Nature Climate Change 3, 581–586, doi: 10.1038/NCLIMATE1836.


Yao H., Song J., Liu C., Luo K., Han J., Li Y., Pang X., Xu H., Zhu Y., Xiao P. & Chen S. 2010. Use of ITS2 region as the universal DNA barcode for plants and animals. PLoS One 5, e13102, doi: 10.1371/journal.pone.0013102.


Yeh F.C. & Boyle T.J.B. 1997. Population genetic analysis of co-dominant and dominant markers and quantitative traits. Belgian Journal of Botany 129, 157.


Yuan Y.M. & Küpfer P. 1995. Molecular phylogenetics of the subtribe Gentianinae (Gentianaceae) inferred from the sequences of the internal transcribed spacers (ITS) of nuclear ribosomal DNA. Plant Systematics and Evolution 196, 207–226, doi: 10.1007/BF00982961.


Zar J.H. 2009. Biostatistical analysis. 5th edn. Upper Saddle River, NJ: Prentice Hall.


Zhao L.-L., Feng S.-J., Tian J.-Y., Wei A.-Z. & Yang T.-X. 2018. Internal transcribed spacer 2 (ITS2) barcodes: a useful tool for identifying Chinese Zanthoxylum. Applications in Plant Sciences 6, e01157, doi: 10.1002/aps3.1157.


Zhou G., Jian J., Wang P., Li C., Tao Y., Li X., Renshaw D., Clements J., Sweetingham M. & Yang H. 2018. Construction of an ultra-high density consensus genetic map, and enhancement of the physical map from genome sequencing in Lupinus angustifolius. Theoretical and Applied Genetics 131, 209–223, doi: 10.1007/s00122-017-2997-y.
Published
2021-02-17
How to Cite
Skorupski J., Szenejko M., Gruba-Tabaka M., Śmietana P., & Panicz R. (2021). Inferring population structure and genetic diversity of the invasive alien Nootka lupin in Iceland. Polar Research, 40. https://doi.org/10.33265/polar.v40.4536
Section
Research Articles