Abstract—
According to one hypotheses, the success of invasive species is due to increased hybridization processes in the secondary distribution range. The purpose of the study was to predict the further rate of the introduction of goldenrod taxa (Solidago L.) in the natural phytocenoses that form in the secondary distribution range with verification of the hybrid nature of these taxa via experimental and molecular genetic methods and to test the hypothesis of higher competitiveness and invasive activity of hybrids with relation to parental species. For comparison, an analysis of the hybridogenic activity of some other representatives of the Asteraceae family of North American origin (Bidens spp., Erigeron sect., Conyza spp.) based on data previously obtained by the authors. It is shown that not all taxa with intermediate morphological characters are hybrids. Thus, neither experimental nor molecular genetic methods confirmed the hybrid origin of Bidens × garumnae and Solidago сanadensis × S. gigantea. Hybrids Solidago × niederederi, S. × snarskisii, and Conyza × rouyana, which have arisen in Europe. They are found only in the secondary distribution range of parental species and are solitary and less competitive than their ancestral forms. A tendency to naturalize is observed only in S. × niederederi. Thus, the hypothesis of the higher competitive ability and invasive activity of hybrids as compared to parental species is not comprehensive, and its supporting examples are the exception rather than the rule.
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REFERENCES
Abbott, R.J., James, J.K., Milne, R.I., et al., Plant introduction, hybridization and gene flow, Philos. Trans. R. Soc., B, 2003, vol. 358, pp. 1123–1132.
Ainouche, M., Chelaifa, H., Rousseau-Guetin, M., et al., Genome merger as evolutionary springboard: insights from recurrent hybridization and polyploidy in Spartina, Proc. Int. Conf. on Polyploidy, Hybridization and Biodiversity, Rovinj: Croat. Biol. Soc., 2016, p. 13.
Albuquerque, G.S., Tauber, C.A., and Tauber, M.J., Postmating reproductive isolation between Chrysopa quadripunctata and Chrysopa slossonae: mechanisms and geographic variation, Evolution, 1996, vol. 50, pp. 1598–1606.
Baumel, A., Ainouche, M.L., Misset, M.T., et al., Genetic evidence for hybridization between the native Spartina maritima and the introduced Spartina alterniflora (Poaceae) in South-West France: Spartina × neyrautii re-examined, Plant. Syst. Evol., 2003, vol. 237, pp. 87 –97.
Bleeker, W., Hybridization and Rorippa austriaca invasion in Germany, Mol. Ecol., 2003, vol. 12, no. 7, pp. 1831–1841.
Bleeker, W., Schmitz, U., and Ristow, M., Interspecific hybridization between alien and native plant species in Germany and its consequences for native biodiversity, Biol. Conserv., 2007, vol. 137, no. 2, pp. 248–253.
Brouillet, L., Semple, J.C., Allen, G.A., et al., Symphyotrichium Nees, in Flora of North America, Vol. 20: Magnoliophyta: Asteridae, Part 7: Asteraceae, Oxford: Oxford Univ. Press, 2006, part 2, pp. 465–539.
Buhk, C. and Thielsch, A., Hybridization boosts the invasion of an alien species complex: insights into future invasiveness, Persp. Plant Ecol., Evol., Syst., 2015, vol. 17, no. 4, pp. 274–283.
Buntjer, J.B., Cross Checker: computer assisted scoring of genetic AFLP data, Proc. VIII Conf. on Plant and Animal Genome, San Diego, CA, January, 9–12,2000, San Diego, 2000. http://wheat.pw.usda.gov/jag/papers99/ paper599/indexp599.html.
Galkina, M.A., Vinogradova, Yu.K., and Shanzer, I.A., Biomorphological features and microevolution of the invasive species Bidens L. in European Russia, Biol. Bull. (Moscow), 2015, vol. 42, no. 4, pp. 315–325.
Galkina, M.A. and Vinogradova, Yu.K., Hybridization of alien and aboriginal taxons of Bidens L. genus in Eastern Europe, Biol. Bull. (Moscow), 2017, vol. 44, no. 4, pp. 406–411.
Grant, V., Plant Speciation, Berkeley: Univ. of California Press, 1981.
Gudžinskas, Z. and Žalneravičius, E., Solidago × snarskisii nothosp. nov. (Asteraceae) from Lithuania and its position in the infrageneric classification of the genus, Phytotaxa, 2016, vol. 253, no. 2, pp. 147–155.
Guénégou, M.C. and Levasseur, J.E., La nouvelle espèce amphiloïde Spartina anglica C.E. Hubbard: son origine, argumentation et implications, Biogeographica, 1993, vol. 69, pp. 125–133.
Ellstrand, N.C. and Shierenbeck, K.A., Hybridization as a stimulus for the evolution of invasiveness in plants? Proc. Natl. Acad. Sci. U.S.A., 2000, vol. 97, no. 13, pp. 7043–7050.
Elton, C.S., The Ecology of Invasions by Animals and Plants, London: Methuen, 1958.
Heywood, V.H., Patterns, extents and modes of invasions by terrestrial plants, in Biological Invasions: A Global Perspective, Drake J.A., Ed., Chichester: Wiley, 1989, pp. 31–60.
Huxel, G.R., Rapid displacement of native species by invasive species: effects of hybridization, Biol. Conserv., 1999, vol. 89, pp. 143–152.
Karpavičienė, B. and Radušienė, J., Morphological and anatomical characterization of Solidago × niederederi and other sympatric Solidago species, Weed Sci., 2016, vol. 64, no. 1, pp. 61–70.
Knope, M.L., Pender, R.J., Crawford, D.J., et al., Invasive congeners are unlikely to hybridize with native Hawaiian Bidens (Asteraceae), Am. J. Bot., 2013, vol. 100, no. 6, pp. 1221–1226.
Levin, D.A., Francisco-Ortega, J., and Jansen, R.K., Hybridization and the extinction of rate plant species, Conserv. Biol., 1996, vol. 10, pp. 10–16.
Macková, L., Vit, P., Ďurišová, L., Eliáš, P., et al., Hybridization success is largely limited to homoploid Prunus hybrids—multidisciplinary approach, Proc. Int. Conf. on Polyploidy, Hybridization and Biodiversity, Rovinj: Croat. Biol. Soc., 2016, p. 113.
Mardis, E.R., Next-generation DNA sequencing methods, Annu. Rev. Genomics Hum. Genet., 2008, vol. 9, pp. 397–402.
Melville, R.M. and Morton, J.K., A biosystematic study of the Solidago canadensis (Compositae) complex. I. The Ontario populations, Can. J. Bot., 2011, vol. 60, no. 6, pp. 976–997.
McGeoch, M.A., Butchart, C.H.M., Spear, D., et al., Global indicators of biological invasion: species numbers, biodiversity impact and policy responses, Diversity Distrib., 2010, vol. 16, pp. 95–108.
Pagitz, K., Solidago × niederederi (S. canadensis × S. virgaurea ssp. virgaurea) in the Eastern Alps, Proc. 9th Int. Conf. on Biological Invasions “Neobiota 2016,” Vianden: Fondation Faune-Flore, 2016, p. 194.
Pliszko, A. and Zając, M., Current and potential distribution of Solidago × niederederi (Asteraceae) in Poland, Proc. 9th Int. Conf. on Biological Invasions “Neobiota 2016,” Vianden: Fondation Faune-Flore, 2016, p. 163.
Radosavliević, I., Bogdanović, S., Filipović, M., et al., Contrasting patterns of phenotypic and genetic variation in hybrid offspring: causes and consequences, Proc. Int. Conf. on Polyploidy, Hybridization and Biodiversity, Rovinj: Croat. Biol. Soc., 2016, p. 97.
Rogers, S.O. and Bendich, A.J., Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues, Plant Mol. Biol., 1985, vol. 5, pp. 69–76.
Rhymer, J.M. and Simberloff, D., Extinction by hybridization and introgression, Ann. Rev. Ecol. Syst., 1996, vol. 27, pp. 83–109.
Rieseberg, L.H., Kim, S.-C., Randell, R.A., et al., Hybridization and the colonization of novel habitats by annual sunflowers, Genetica, 2007, vol. 129, pp. 149–165.
Rousseau, H., Dauvergne, X., Boutte, J., et al., Polyploidy and phenotypic novelty: phylogenetic context of DMSP (dimethylsulfoniopropionate) biosynthesis in Spartina (Poaceae, Chloridoideae), Proc. Int. Conf. on Polyploidy, Hybridization and Biodiversity, Rovinj: Croat. Biol. Soc., 2016, p. 59.
Salmon, A., Boutte, J., Rousseau, H., et al., How to detect duplicated sequences within highly polyploid species without any reference? An introduction to the use of the Pyro- and Illu-haplotyper pipelines for Spartina genomics, Proc. Int. Conf. on Polyploidy, Hybridization and Biodiversity, Rovinj: Croat. Biol. Soc., 2016, p. 29.
Tokhtar, V.K., Vinogradova, Yu.K., and Groshenko, A.S., Microevolution and invasiveness of Oenothera L. species (subsect. Oenothera, Onagraceae) in Europe, Russ. J. Biol. Invasions, 2011, vol. 2, no. 4, pp. 273–280.
Vasil’eva, N.V. and Papchenkov, V.G., Distribution of Bidens frondosa L. in the Volga River basin and its biological features, in Estestvennye i invaziinye protsessy formirovaniya vodnykh i nazemnykh ekosistem (Natural and Invasive Formation Processes of Aquatic and Terrestrial Ecosystems), Rostov-on-Don: Yuzhn. Nauchn. Tsentr, Ross. Akad. Nauk, 2007, pp. 64–65.
Vasilyeva, N.V. and Papchenkov, V.G., Mechanisms of influence of invasive Bidens frondosa L. on indigenous Bidens species, Russ. J. Biol. Invasions, 2011, vol. 2, nos. 2–3, pp. 81–85.
Vinogradova, Yu.K., Biodiversity of taxons of genus Solidago L. by micromorphological features, in Bioraznoobrazie: problemy izucheniya i sokhraneniya (Biological Diversity: Study and Conservation), Tver: Tversk. Gos. Univ., 2012, pp. 346–350.
Vinogradova, Yu.K. and Galkina, M.A., Possible hybrid origin of Bidens connata, Materialy XIII Moskovskogo soveshchaniya po filogenii rastenii (Proc. XIII Moscow Conf. on the Plant Phylogeny), Moscow: Maks Press, 2015, pp. 64–69.
Vinogradova, Yu.K. and Kvitka, A.Yu., Invasive species of genus Solidago in flora of Central Russia, in Floristicheskie issledovaniya v Srednei Rossii (Floristic Studies in Central Russia), Moscow: KMK, 2006, pp. 74–78.
Vinogradova, Yu.K. and Maiorov, S.R., History of introduction, microevolution and speciation in the genus Conyza Less. in secondary range, in Sovremennaya botanika v Rossii (Modern Botany in Russia), Tolyatti: Kassandra, 2014, vol. 4, pp. 61–63.
Vinogradova, Yu.K. and Maiorov, S.R., Duration of lag-phase as a reflection of microevolution of the plants in secondary range, Materialy XIII Moskovskogo soveshchaniya po filogenii rastenii (Proc. XIII Moscow Conf. on the Plant Phylogeny), Moscow: Maks Press, 2015, pp. 70–74.
Vinogradova, Yu.K., Maiorov, S.R., and Khorun, L.V., Chernaya kniga flory Srednei Rossii (The Black Book of Flora of Central Russia), Moscow: GEOS, 2010.
Vinogradova, Yu.K., Abramova, L.M., Akatova, T.V., et al., The “Black hundred” of invasive plants of Russia, Inf. Byull. Sov. Bot. Sadov Stran SNG, 2015, no. 4 (27), pp. 85–89.
Vinogradova, Yu.K. and Galkina, M.A., Taxons of genus Bidens L. in Central Russia: variability and inheritance of biomorphological features, Vestn. Udmurt. Gos. Univ.,Ser. Biol., 2016, vol. 26, no. 1, pp. 53–62.
Vinogradova, Yu.K., Ryabchenko, A.S., and Galkina, M.A., The taxonomic relevance of achenial trichomes in invasive European Asteraceae, Ann. Mo. Bot. Gard., 2017, vol. 102, no. 4, pp. 730–741.
Williamson, M., Biological Invasions, London: Chapman and Hall, 1996, p. 33.
Zalapa, J.E., Brunet, J., and Guries, R.P., Patterns of hybridization and introgression between invasive Ulmus pumila (Ulmaceae) and native U. rubra,Am. J. Bot., 2009, vol. 96, pp. 1116–1128.
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The authors are grateful to the anonymous reviewer of this article, whose comments helped us to improve the text significantly.
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The studies were carried out within the framework of the State Budget Service of Main Botanical Garden, Russian Academy of Sciences, “Biological Diversity of Natural and Cultural Flora: Fundamental and Applied Issues of Study and Preservation” (no. 118021490111-5) with the partial financial support of the Russian Foundation for Basic Research (project no. 18-04-00411).
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Vinogradova, Y.K., Galkina, M.A. Hybridization as a Factor of Invasive Activity of Alien Goldenrod Species (Solidago). Biol Bull Rev 10, 57–70 (2020). https://doi.org/10.1134/S2079086420010090
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DOI: https://doi.org/10.1134/S2079086420010090