Darwin's naturalization hypothesis predicts successful alien invaders to be distantly related to native species, whereas his pre-adaptation hypothesis predicts the opposite. It has been suggested that depending on the invasion stage (that is, introduction, naturalization and invasiveness), both hypotheses, now known as Darwin's naturalization conundrum, could hold true. We tested this by analysing whether the likelihood of introduction for cultivation, as well as the subsequent stages of naturalization and spread (that is, becoming invasive) of species alien to Southern Africa are correlated with their phylogenetic distance to the native flora of this region. Although species are more likely to be introduced for cultivation if they are distantly related to the native flora, the probability of subsequent naturalization was higher for species closely related to the native flora. Furthermore, the probability of becoming invasive was higher for naturalized species distantly related to the native flora. These results were consistent across three different metrics of phylogenetic distance. Our study reveals that the relationship between phylogenetic distance to the native flora and the success of an alien species changes from one invasion stage to the other.

Biodiversity Macroecology and Biogeography University of Goettingen Göttingen Germany

BioInvasions Global Change Macroecology Group Department of Botany and Biodiversity Research University of Vienna Vienna Austria

Campus Institut Data Science Göttingen Germany

Centre of Biodiversity and Sustainable Land Use University of Goettingen Göttingen Germany

Department of Biosciences Durham University Durham UK

Department of Ecology Charles University Prague Czech Republic

Department of Forest Management University of Khartoum North Khartoum Sudan

Department of Invasion Ecology Czech Academy of Sciences Institute of Botany Průhonice Czech Republic

Division of Biodiversity Dynamics and Conservation Department of Botany and Biodiversity Research University of Vienna Vienna Austria

Ecology Department of Biology University of Konstanz Konstanz Germany

Institute of Landscape and Plant Ecology University of Hohenheim Stuttgart Germany

Zhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation Taizhou University Taizhou China

Zobrazit více v PubMed

Richardson, D. M. et al. Naturalization and invasion of alien plants: concepts and definitions. Divers. Distrib. 6, 93–107 (2000). DOI

van Kleunen, M. et al. Global exchange and accumulation of non-native plants. Nature 525, 100–103 (2015). PubMed DOI

Capinha, C., Essl, F., Seebens, H., Moser, D. & Pereira, H. M. The dispersal of alien species redefines biogeography in the Anthropocene. Science 348, 1248–1251 (2015). PubMed DOI

Vilà, M. & Hulme, P. E. in Impact of Biological Invasions on Ecosystem Services Vol. 12 Invading Nature – Springer Series in Invasion Ecology (eds Vilà, M. & Hulme, P. E.) 1–14 (Springer, 2017).

Pyšek, P. et al. A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species’ traits and environment. Glob. Chang. Biol. 18, 1725–1737 (2012). DOI PMC

Pyšek, P. et al. Scientists’ warning on invasive alien species. Biol. Rev. 95, 1511–1534 (2020). PubMed DOI

Bacher, S. et al. Socio-economic impact classification of alien taxa (SEICAT). Methods Ecol. Evol. 9, 159–168 (2018). DOI

Seebens, H. et al. No saturation in the accumulation of alien species worldwide. Nat. Commun. 8, 14435 (2017). PubMed DOI PMC

Seebens, H. et al. Projecting the continental accumulation of alien species through to 2050. Glob. Chang. Biol. 27, 970–982 (2021). DOI

Kriticos, D. J., Sutherst, R. W., Brown, J. R., Adkins, S. W. & Maywald, G. F. Climate change and the potential distribution of an invasive alien plant: Acacia nilotica ssp. indica in Australia. J. Appl. Ecol. 40, 111–124 (2003). DOI

Thuiller, W., Richardson, D. M. & Midgley, G. F. in Biological Invasions (ed. Nentwig, W.) 197–211 (Springer, 2007).

Hobbs, R. J. in Invasive Species in a Changing World (eds Mooney, H. A. & Hobbs, R. J.) 55–64 (Island Press, 2000).

Seebens, H. et al. Global trade will accelerate plant invasions in emerging economies under climate change. Glob. Chang. Biol. 21, 4128–4140 (2015). PubMed DOI

Razanajatovo, M. et al. Plants capable of selfing are more likely to become naturalized. Nat. Commun. 7, 13313 (2016). PubMed DOI PMC

Bucharova, A. & van Kleunen, M. Introduction history and species characteristics partly explain naturalization success of North American woody species in Europe. J. Ecol. 97, 230–238 (2009). DOI

Ordonez, A., Wright, I. J. & Olff, H. Functional differences between native and alien species: a global-scale comparison. Funct. Ecol. 24, 1353–1361 (2010). DOI

van Kleunen, M., Weber, E. & Fischer, M. A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol. Lett. 13, 235–245 (2010). PubMed DOI

van Kleunen, M., Dawson, W. & Maurel, N. Characteristics of successful alien plants. Mol. Ecol. 24, 1954–1968 (2015). PubMed DOI

Essl, F. et al. Drivers of the relative richness of naturalized and invasive plant species on Earth. AoB Plants 11, plz051 (2019). PubMed DOI PMC

Winkler, D. E., Gremer, J. R., Chapin, K. J., Kao, M. & Huxman, T. E. Rapid alignment of functional trait variation with locality across the invaded range of Sahara mustard (Brassica tournefortii). Am. J. Bot. 105, 1188–1197 (2018). PubMed DOI

Divíšek, J. et al. Similarity of introduced plant species to native ones facilitates naturalization, but differences enhance invasion success. Nat. Commun. 9, 4631 (2018). PubMed DOI PMC

Banerjee, A. K., Prajapati, J., Bhowmick, A. R., Huang, Y. & Mukherjee, A. Different factors influence naturalization and invasion processes – a case study of Indian alien flora provides management insights. J. Environ. Manag. 294, 113054 (2021). DOI

Ni, M. et al. Invasion success and impacts depend on different characteristics in non-native plants. Divers. Distrib. 27, 1194–1207 (2021). DOI

Fristoe, T. S. et al. Dimensions of invasiveness: links between local abundance, geographic range size, and habitat breadth in Europe’s alien and native floras. Proc. Natl Acad. Sci. USA 118, e2021173118 (2021). PubMed DOI PMC

Omer, A. et al. Characteristics of the naturalized flora of Southern Africa largely reflect the non-random introduction of alien species for cultivation. Ecography 44, 1812–1825 (2021). DOI

Pyšek, P. et al. Naturalization of central European plants in North America: species traits, habitats, propagule pressure, residence time. Ecology 96, 762–774 (2015). PubMed DOI

Omer, A., Kordofani, M., Gibreel, H. H., Pyšek, P. & van Kleunen, M. The alien flora of Sudan and South Sudan: taxonomic and biogeographical composition. Biol. Invasions 23, 2033–2045 (2021). DOI

Duncan, R. P. & Williams, P. A. Darwin’s naturalization hypothesis challenged. Nature 417, 608–609 (2002). PubMed DOI

Daehler, C. C. Darwin’s naturalization hypothesis revisited. Am. Nat. 158, 324–330 (2001). PubMed DOI

Pyšek, P. Is there a taxonomic pattern to plant invasions? Oikos 82, 282–294 (1998). DOI

Tan, J., Pu, Z., Ryberg, W. A. & Jiang, L. Resident–invader phylogenetic relatedness, not resident phylogenetic diversity, controls community invasibility. Am. Nat. 186, 59–71 (2015). PubMed DOI

Thuiller, W. et al. Resolving Darwin’s naturalization conundrum: a quest for evidence. Divers. Distrib. 16, 461–475 (2010). DOI

Loiola, P. P. et al. Invaders among locals: alien species decrease phylogenetic and functional diversity while increasing dissimilarity among native community members. J. Ecol. 106, 2230–2241 (2018). DOI

Lososová, Z. et al. Alien plants invade more phylogenetically clustered community types and cause even stronger clustering. Glob. Ecol. Biogeogr. 24, 786–794 (2015). DOI

Marx, H. E., Giblin, D. E., Dunwiddie, P. W. & Tank, D. C. Deconstructing Darwin’s naturalization conundrum in the San Juan Islands using community phylogenetics and functional traits. Divers. Distrib. 22, 318–331 (2016). DOI

Darwin, C. On the Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life (John Murray, 1859).

Procheş, Ş., Wilson, J. R. U., Richardson, D. M. & Rejmánek, M. Searching for phylogenetic pattern in biological invasions. Glob. Ecol. Biogeogr. 17, 5–10 (2008).

Diez, J. M., Sullivan, J. J., Hulme, P. E., Edwards, G. & Duncan, R. P. Darwin’s naturalization conundrum: dissecting taxonomic patterns of species invasions. Ecol. Lett. 11, 674–681 (2008). PubMed DOI

Cadotte, M. W., Campbell, S. E., Li, S. P., Sodhi, D. S. & Mandrak, N. E. Preadaptation and naturalization of nonnative species: Darwin’s two fundamental insights into species invasion. Annu Rev. Plant Biol. 69, 661–684 (2018). PubMed DOI

van Kleunen, M., Bossdorf, O. & Dawson, W. The ecology and evolution of alien plants. Annu. Rev. Ecol. Evol. Syst. 49, 25–47 (2018). DOI

Park, D. S., Feng, X., Maitner, B. S., Ernst, K. C. & Enquist, B. J. Darwin’s naturalization conundrum can be explained by spatial scale. Proc. Natl Acad. Sci. USA 117, 10904–10910 (2020). PubMed DOI PMC

Diez, J. M. et al. Learning from failures: testing broad taxonomic hypotheses about plant naturalization. Ecol. Lett. 12, 1174–1183 (2009). PubMed DOI

Malecore, E. M., Dawson, W., Kempel, A., Müller, G. & van Kleunen, M. Nonlinear effects of phylogenetic distance on early-stage establishment of experimentally introduced plants in grassland communities. J. Ecol. 107, 781–793 (2019). DOI

Schaefer, H., Hardy, O. J., Silva, L., Barraclough, T. G. & Savolainen, V. Testing Darwin’s naturalization hypothesis in the Azores. Ecol. Lett. 14, 389–396 (2011). PubMed DOI

Strauss, S. Y., Webb, C. O. & Salamin, N. Exotic taxa less related to native species are more invasive. Proc. Natl Acad. Sci. USA 103, 5841–5845 (2006). PubMed DOI PMC

Li, S.-p. et al. The effects of phylogenetic relatedness on invasion success and impact: deconstructing Darwin’s naturalisation conundrum. Ecol. Lett. 18, 1285–1292 (2015). PubMed DOI

Pellock, S., Thompson, A., He, K., Mecklin, C. & Yang, J. Validity of Darwin’s naturalization hypothesis relates to the stages of invasion. Community Ecol. 14, 172–179 (2013). DOI

Blackburn, T. M. et al. A proposed unified framework for biological invasions. Trends Ecol. Evol. 26, 333–339 (2011). PubMed DOI

van Kleunen, M. et al. Economic use of plants is key to their naturalization success. Nat. Commun. 11, 3201 (2020). PubMed DOI PMC

Broennimann, O. et al. Distance to native climatic niche margins explains establishment success of alien mammals. Nat. Commun. 12, 2353 (2021). PubMed DOI PMC

Carboni, M. et al. What it takes to invade grassland ecosystems: traits, introduction history and filtering processes. Ecol. Lett. 19, 219–229 (2016). PubMed DOI

Milbau, A. & Stout, J. C. Factors associated with alien plants transitioning from casual, to naturalized, to invasive. Conserv. Biol. 22, 308–317 (2008). PubMed DOI

Dawson, W., Burslem, D. F. R. P. & Hulme, P. E. Factors explaining alien plant invasion success in a tropical ecosystem differ at each stage of invasion. J. Ecol. 97, 657–665 (2009). DOI

Rejmánek, M. in Invasive Species and Biodiversity Management (eds Schei, P. J. & Vilken, A.) 79–102 (Kluwer Academic, 1998).

Rejmánek, M. A theory of seed plant invasiveness: the first sketch. Biol. Conserv. 78, 171–181 (1996). DOI

Maurel, N., Hanspach, J., Kuhn, I., Pysek, P. & van Kleunen, M. Introduction bias affects relationships between the characteristics of ornamental alien plants and their naturalization success. Glob. Ecol. Biogeogr. 25, 1500–1509 (2016). DOI

Glen, H. F. Cultivated Plants of Southern Africa: Botanical Names, Common Names, Origins, Literature (National Botanical Institute, 2002).

Reichard, S. H. & White, P. Horticulture as a pathway of invasive plant introductions in the United States. Bioscience 51, 103–113 (2001). DOI

Faulkner, K. T., Robertson, M. P., Rouget, M. & Wilson, J. R. U. Understanding and managing the introduction pathways of alien taxa: South Africa as a case study. Biol. Invasions 18, 73–87 (2016). DOI

Dodd, A. J., Burgman, M. A., McCarthy, M. A. & Ainsworth, N. The changing patterns of plant naturalization in Australia. Divers. Distrib. 21, 1038–1050 (2015). DOI

Lambdon, P.-W. et al. Alien flora of Europe: species diversity, temporal trends, geographical patterns and research needs. Preslia 80, 101–149 (2008).

Bennett, B. M. Naturalising Australian trees in South Africa: climate, exotics and experimentation. J. South. Afr. Stud. 37, 265–280 (2011). DOI

Richardson, D. M. et al. in Biological Invasions in South Africa (eds van Wilgen, B. W. et al.) 67–96 (Springer, 2020).

Li, S.-p. et al. Contrasting effects of phylogenetic relatedness on plant invader success in experimental grassland communities. J. Appl. Ecol. 52, 89–99 (2015). DOI

Duarte, M., Verdú, M., Cavieres, L. A. & Bustamante, R. O. Plant–plant facilitation increases with reduced phylogenetic relatedness along an elevation gradient. Oikos 130, 248–259 (2021). DOI

Verdú, M., Rey, P. J., Alcántara, J. M., Siles, G. & Valiente-Banuet, A. Phylogenetic signatures of facilitation and competition in successional communities. J. Ecol. 97, 1171–1180 (2009). DOI

Valiente-Banuet, A. & Verdu, M. Plant facilitation and phylogenetics. Annu. Rev. Ecol. Evol. Syst. 44, 347–366 (2013). DOI

Anacker, B. L. & Strauss, S. Y. Ecological similarity is related to phylogenetic distance between species in a cross-niche field transplant experiment. Ecology 97, 1807–1818 (2016). PubMed DOI

Dostál, P. Plant competitive interactions and invasiveness: searching for the effects of phylogenetic relatedness and origin on competition intensity. Am. Nat. 177, 655–667 (2011). PubMed DOI

Levin, S. C., Crandall, R. M., Pokoski, T., Stein, C. & Knight, T. M. Phylogenetic and functional distinctiveness explain alien plant population responses to competition. Proc. R. Soc. B 287, 20201070 (2020). PubMed DOI PMC

Williams, E. W., Zeldin, J., Semski, W. R., Hipp, A. L. & Larkin, D. J. Phylogenetic distance and resource availability mediate direction and strength of plant interactions in a competition experiment. Oecologia 197, 459–469 (2021). PubMed DOI

Bezeng, S. B., Davies, J. T., Yessoufou, K., Maurin, O. & Van der Bank, M. Revisiting Darwin’s naturalization conundrum: explaining invasion success of non-native trees and shrubs in Southern Africa. J. Ecol. 103, 871–879 (2015). DOI

Trotta, L. B., Siders, Z. A., Sessa, E. B. & Baiser, B. The role of phylogenetic scale in Darwin’s naturalization conundrum in the critically imperilled pine rockland ecosystem. Divers. Distrib. 27, 618–631 (2021). DOI

Sol, D. et al. A test of Darwin’s naturalization conundrum in birds reveals enhanced invasion success in the presence of close relatives. Ecol. Lett. 25, 661–672 (2022). PubMed DOI

Smith, S. A. & Brown, J. W. Constructing a broadly inclusive seed plant phylogeny. Am. J. Bot. 105, 302–314 (2018). PubMed DOI

Henderson, L. Comparisons of invasive plants in Southern Africa originating from southern temperate, northern temperate and tropical regions. Bothalia 36, 201–222 (2006). DOI

Cayuela, L., Stein, A. & Oksanen, J. Taxonstand: Taxonomic Standardization of Plant Species Names. R package version 2.2. https://CRAN.R-project.org/package=Taxonstand (R Foundation for Statistical Computing, Vienna, 2019).

Weigelt, P., König, C. & Kreft, H. GIFT – A Global Inventory of Floras and Traits for macroecology and biogeography. J. Biogeogr. 47, 16–43 (2020). DOI

van Kleunen, M. et al. The Global Naturalized Alien Flora (GloNAF) database. Ecology 100, e02542 (2019). PubMed DOI

Zengeya, T. A. & Wilson, J. R. (eds) The Status of Biological Invasions and Their Management in South Africa in 2019 (South African National Biodiversity Institute and DSI-NRF Centre of Excellence for Invasion Biology, 2021).

Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012). DOI

R: A Language and Environment for Statistical Computing v.3.6.1 (R Foundation for Statistical Computing, 2019).

Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R Vol. 574 (Springer, 2009).

Schielzeth, H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1, 103–113 (2010). DOI

Nagelkerke, N. J. D. A note on a general definition of the coefficient of determination. Biometrika 78, 691–692 (1991). DOI

rcompanion: Functions to support extension education program evaluation v. 2.4.1 (R Foundation for Statistical Computing, 2021).

Tung Ho, L. S. & Ané, C. A linear-time algorithm for Gaussian and non-Gaussian trait evolution models. Syst. Biol. 63, 397–408 (2014). DOI

Stage dependence of Elton's biotic resistance hypothesis of biological invasions

Plant invasion and naturalization are influenced by genome size, ecology and economic use globally

A latitudinal gradient in Darwin's naturalization conundrum at the global scale for flowering plants

Contrasting patterns in phylogenetic and biogeographic factories of invasive grasses (Poaceae) across the globe