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Evolutionary imbalance, climate and human history jointly shape the global biogeography of alien plants

Nature Ecology & Evolution volume 7, pages 1633–1644 (2023)Cite this article

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Abstract

Human activities are causing global biotic redistribution, translocating species and providing them with opportunities to establish populations beyond their native ranges. Species originating from certain global regions, however, are disproportionately represented among naturalized aliens. The evolutionary imbalance hypothesis posits that differences in absolute fitness among biogeographic divisions determine outcomes when biotas mix. Here, we compile data from native and alien distributions for nearly the entire global seed plant flora and find that biogeographic conditions predicted to drive evolutionary imbalance act alongside climate and anthropogenic factors to shape flows of successful aliens among regional biotas. Successful aliens tend to originate from large, biodiverse regions that support abundant populations and where species evolve against a diverse backdrop of competitors and enemies. We also reveal that these same native distribution characteristics are shared among the plants that humans select for cultivation and economic use. In addition to influencing species’ innate potentials as invaders, we therefore suggest that evolutionary imbalance shapes plants’ relationships with humans, impacting which species are translocated beyond their native distributions.

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Fig. 1: Variation and drivers of global naturalization success among plant origins.
Fig. 2: Geographic variation in naturalization success for species originating from each biogeographic syndrome.
Fig. 3: Drivers of economic use and naturalization across the global seed plant flora (n = 334,667).
Fig. 4: Drivers of naturalization extent among the naturalized alien seed plant flora (n = 13,280).

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Data availability

All results are based on publicly available data as described in Methods. Data used in analyses can be downloaded in Supplementary Data 1–5 and 7 through https://doi.org/10.6084/m9.figshare.21512145 (ref. 74).

Code availability

R code used to perform analyses can be found in Supplementary Code 1, available through https://doi.org/10.6084/m9.figshare.21512145 (ref. 74).

References

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

    Google Scholar 

  2. Darwin, C. On the Origin of Species (John Murray, 1859).

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

    PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  5. Dyer, E. E. et al. The global distribution and drivers of alien bird species richness. PLoS Biol. 15, e2000942 (2017).

    PubMed  PubMed Central  Google Scholar 

  6. Dyer, E. E., Redding, D. W. & Blackburn, T. M. The global avian invasions atlas, a database of alien bird distributions worldwide. Sci. Data 4, 170041 (2017).

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  8. Vermeij, G. J. When biotas meet: understanding biotic interchange. Science 253, 1099–1104 (1991).

    CAS  PubMed  Google Scholar 

  9. Vermeij, G. in Species Invasions: Insights into Ecology, Evolution, and Biogeography (eds Sax, D. F. et al.) 315–340 (Sinauer, 2005).

  10. Fridley, J. D. & Sax, D. F. The imbalance of nature: revisiting a Darwinian framework for invasion biology. Glob. Ecol. Biogeogr. 23, 1157–1166 (2014).

    Google Scholar 

  11. Leimu, R., Mutikainen, P., Koricheva, J. & Fischer, M. How general are positive relationships between plant population size, fitness and genetic variation? J. Ecol. 94, 942–952 (2006).

    Google Scholar 

  12. Tilman, D. Diversification, biotic interchange, and the universal trade-off hypothesis. Am. Nat. 178, 355–371 (2011).

    PubMed  Google Scholar 

  13. Dobzhansky, T. Evolution in the tropics. Am. Sci. 38, 209–221 (1950).

    Google Scholar 

  14. MacArthur, R. H. Geographical Ecology: Patterns in the Distribution of Species (Princeton Univ. Press, 1972).

  15. Cody, M. L. & Mooney, H. A. Convergence versus nonconvergence in Mediterranean-climate ecosystems. Annu. Rev. Ecol. Syst. 9, 265–321 (1978).

    Google Scholar 

  16. Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138, 1315–1341 (1991).

    Google Scholar 

  17. Leigh, E. G. Jr, Vermeij, G. J. & Wikelski, M. What do human economies, large islands and forest fragments reveal about the factors limiting ecosystem evolution? J. Evolut. Biol. 22, 1–12 (2009).

    Google Scholar 

  18. Fridley, J. D., Jo, I., Hulme, P. E. & Duncan, R. P. A habitat-based assessment of the role of competition in plant invasions. J. Ecol. 109, 1263–1274 (2021).

    Google Scholar 

  19. World Checklist of Vascular Plants, Version 2.0 (Royal Botanic Gardens Kew, 2022); http://wcvp.science.kew.org/

  20. Haeuser, E. et al. European ornamental garden flora as an invasion debt under climate change. J. Appl. Ecol. 55, 2386–2395 (2018).

    Google Scholar 

  21. Liu, C., Wolter, C., Xian, W. & Jeschke, J. M. Most invasive species largely conserve their climatic niche. Proc. Natl Acad. Sci. USA 117, 23643–23651 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  23. Bertelsmeier, C., Ollier, S., Liebhold, A. & Keller, L. Recent human history governs global ant invasion dynamics. Nat. Ecol. Evol. 1, 0184 (2017).

    PubMed  PubMed Central  Google Scholar 

  24. di Castri, F. in Biological Invasions: A Global Perspective (eds Drake, J.A. et al.) 1–30 (Wiley, 1989).

    Google Scholar 

  25. MacDougall, A. S. & Turkington, R. Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86, 42–55 (2005).

    Google Scholar 

  26. Brummitt, R. World Geographical Scheme for Recording Plant Distributions, Edition 2 (Hunt Institute for Botanical Documentation, Carnegie Mellon University, 2001); http://www.tdwg.org/standards/109

  27. Global Compositae Database (Compositae Working Group, 2022); https://www.compositae.org/

  28. The IUCN Red List of Threatened Species (IUCN, 2022); https://www.iucnredlist.org

  29. USDA-ARS Germplasm Resources Information Network (GRIN) (United States Department of Agriculture, 2022); https://www.ars-grin.gov

  30. Plants of the World Online (Royal Botanic Gardens Kew, 2022); http://www.plantsoftheworldonline.org/

  31. Brown, S. C., Wigley, T. M. L., Otto-Bliesner, B. L. & Fordham, D. A. StableClim, continuous projections of climate stability from 21000 bp to 2100 ce at multiple spatial scales. Sci. Data 7, 335 (2020).

    PubMed  PubMed Central  Google Scholar 

  32. Ehlers, J., Gibbard, P. L. & Hughes, P. D. Quaternary Glaciations - Extent and Chronology: A Closer Look (Elsevier, 2011).

  33. Yang, Q. et al. The global loss of floristic uniqueness. Nat. Commun. 12, 7290 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Lenzner, B. et al. Naturalized alien floras still carry the legacy of European colonialism. Nat. Ecol. Evol. 6, 1723–1732 (2022).

  35. Klein Goldewijk, K., Beusen, A., Doelman, J. & Stehfest, E. Anthropogenic land use estimates for the Holocene – HYDE 3.2. Earth Syst. Sci. Data 9, 927–953 (2017).

    Google Scholar 

  36. Diamond, J. M. Guns, Germs, and Steel: The Fates of Human Societies (W.W. Norton, 1997).

  37. Diamond, J. & Bellwood, P. Farmers and their languages: the first expansions. Science 300, 597–603 (2003).

    CAS  PubMed  Google Scholar 

  38. Vilela, B. et al. Cultural transmission and ecological opportunity jointly shaped the spread of human agriculture. Evol. Hum. Sci. 2, E53 (2020).

  39. Balick, M. J. & Cox, P. A. Plants, People, and Culture: The Science of Ethnobotany (Garland Science, 2020).

    Google Scholar 

  40. Vavilov, N. I., Vavylov, M. I. & Dorofeev, V. F. Origin and Geography of Cultivated Plants (Cambridge Univ. Press, 1992).

  41. Phillips, O. & Gentry, A. H. The useful plants of Tambopata, Peru: II. Additional hypothesis testing in quantitative ethnobotany. Econ. Bot. 47, 33–43 (1993).

    Google Scholar 

  42. Gaoue, O. G. et al. Theories and major hypotheses in ethnobotany. Econ. Bot. 71, 269–287 (2017).

    Google Scholar 

  43. Milla, R. et al. Phylogenetic patterns and phenotypic profiles of the species of plants and mammals farmed for food. Nat. Ecol. Evol. 2, 1808–1817 (2018).

    PubMed  Google Scholar 

  44. Enquist, B. J. et al. The commonness of rarity: global and future distribution of rarity across land plants. Sci. Adv. 5, eaaz0414 (2019).

    PubMed  PubMed Central  Google Scholar 

  45. Pyšek, P. et al. The global invasion success of central European plants is related to distribution characteristics in their native range and species traits. Divers. Distrib. 15, 891–903 (2009).

    Google Scholar 

  46. 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).

  47. Sheth, S. N. & Angert, A. L. The evolution of environmental tolerance and range size: a comparison of geographically restricted and widespread Mimulus. Evolution 68, 2917–2931 (2014).

    PubMed  Google Scholar 

  48. 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  Google Scholar 

  49. Hulme, P. E. Trade, transport and trouble: managing invasive species pathways in an era of globalization. J. Appl. Ecol. 46, 10–18 (2009).

    Google Scholar 

  50. Fristoe, T. S., Iwaniuk, A. N. & Botero, C. A. Big brains stabilize populations and facilitate colonization of variable habitats in birds. Nat. Ecol. Evol. 1, 1706–1715 (2017).

  51. Sunday, J. M., Bates, A. E. & Dulvy, N. K. Global analysis of thermal tolerance and latitude in ectotherms. Proc. R. Soc. B 278, 1823–1830 (2011).

    PubMed  Google Scholar 

  52. Khaliq, I., Hof, C., Prinzinger, R., Böhning-Gaese, K. & Pfenninger, M. Global variation in thermal tolerances and vulnerability of endotherms to climate change. Proc. R. Soc. B 281, 20141097 (2014).

    PubMed  PubMed Central  Google Scholar 

  53. Svenning, J.-C., Eiserhardt, W. L., Normand, S., Ordonez, A. & Sandel, B. The influence of paleoclimate on present-day patterns in biodiversity and ecosystems. Annu. Rev. Ecol. Evol. Syst. 46, 551–572 (2015).

    Google Scholar 

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

    CAS  Google Scholar 

  55. Preston, C. D., Pearman, D. A. & Hall, A. R. Archaeophytes in Britain. Bot. J. Linn. Soc. 145, 257–294 (2004).

    Google Scholar 

  56. Ecseri, K. & Honfi, P. Comparison of European archaeophyte lists in the light of distribution data. Not. Bot. Horti Agrobot. Cluj Napoca 48, 480–491 (2020).

    Google Scholar 

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

    Google Scholar 

  58. Lenzner, B. et al. Role of diversification rates and evolutionary history as a driver of plant naturalization success. N. Phytol. 229, 2998–3008 (2021).

    Google Scholar 

  59. Pyšek, P. et al. Naturalized alien flora of the world. Preslia 89, 203–274 (2017).

    Google Scholar 

  60. Lonsdale, W. M. Global patterns of plant invasions and the concept of invasibility. Ecology 80, 1522–1536 (1999).

    Google Scholar 

  61. Faith, D. P. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10 (1992).

    Google Scholar 

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

    PubMed  Google Scholar 

  63. Dengler, J. Which function describes the species–area relationship best? A review and empirical evaluation. J. Biogeogr. 36, 728–744 (2009).

    Google Scholar 

  64. Diazgranados, M. et al. World Checklist of Useful Plant Species (Knowledge Network for Biocomplexity, 2020); https://doi.org/10.5063/F1CV4G34

  65. Fouquin, M. & Hugot, J. Two Centuries of Bilateral Trade and Gravity Data: 1827–2014 (CEPII, 2016).

  66. Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  68. R: A Language and Environment for Statistical Computing (R Development Core Team, 2022).

  69. Dormann, C. F. et al. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27–46 (2013).

    Google Scholar 

  70. Pinheiro, J., Bates, D. & R Core Team nlme: Linear and Nonlinear Mixed Effects Models http://CRAN.R-project.org/package=nlme (2023).

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

    Google Scholar 

  72. Hilbe, J. M. Logistic Regression Models (CRC Press, 2009).

    Google Scholar 

  73. Hartig, F. DHARMa: Residual Diagnostics for HierARchical Models http://florianhartig.github.io/DHARMa/ (2022).

  74. Fristoe, T. S. et al. Evolutionary imbalance, human history, and the global biogeography of alien plants. Figshare https://doi.org/10.6084/m9.figshare.21512145 (2023).

Download references

Acknowledgements

M.v.K. and N.L.K. thank the German Research Foundation DFG for funding (grants 264740629 and 432253815 to M.v.K.). F.E. appreciates funding by the Austrian Science Foundation FWF (grant no. I 5825-B). P.P. and J.P. were supported by EXPRO grant no. 19-28807X (Czech Science Foundation) and long-term research development project RVO 67985939 (Czech Academy of Sciences). J.-M.D.-D. is an independent ecologist.

Author information

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  1. Unaffiliated

Authors and Affiliations

  1. Ecology, Department of Biology, University of Konstanz, Konstanz, Germany

    Trevor S. Fristoe, Jonas Bleilevens, Nicole L. Kinlock, Qiang Yang, Zhijie Zhang & Mark van Kleunen

  2. Centre for Organismal Studies (COS) Heidelberg, Biodiversity and Plant Systematics, Heidelberg University, Heidelberg, Germany

    Jonas Bleilevens

  3. The German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany

    Qiang Yang

  4. Department of Biosciences, Durham University, Durham, UK

    Wayne Dawson

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

    Franz Essl

  6. Biodiversity, Macroecology & Biogeography, University of Goettingen, Göttingen, Germany

    Holger Kreft & Patrick Weigelt

  7. Centre of Biodiversity and Sustainable Land Use (CBL), University of Goettingen, Göttingen, Germany

    Holger Kreft & Patrick Weigelt

  8. Department of Invasion Ecology, Institute of Botany, Czech Academy of Sciences, Průhonice, Czech Republic

    Jan Pergl & Petr Pyšek

  9. Department of Ecology, Faculty of Science, Charles University, Prague, Czech Republic

    Petr Pyšek

  10. Botanical Museum, Finnish Museum of Natural History, University of Helsinki, Helsinki, Finland

    Alexander N. Sennikov

  11. Icelandic Institute of Natural History, Borgir vid Nordurslod, Akureyri, Iceland

    Pawel Wasowicz

  12. Department of Natural History, NTNU University Museum, Norwegian University of Science and Technology, Trondheim, Norway

    Kristine B. Westergaard

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

    Mark van Kleunen

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Contributions

T.S.F. and J.B. conceived and designed the study with input from N.L.K., Q.Y., Z.Z. and M.v.K. T.S.F. and J.B. analysed the data. T.S.F. and J.B. wrote the initial draft with input from M.v.K. T.S.F., J.B., N.L.K., Q.Y., Z.Z., W.D., F.E., H.K., J.P., P.P., P. Weigelt, J.-M.D.-D., A.N.S., P. Wasowicz, K.B.W. and M.v.K. contributed data and to subsequent manuscript revisions.

Corresponding author

Correspondence to Trevor S. Fristoe.

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Nature Ecology & Evolution thanks Jason Fridley and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Table 1 Loadings for varimax rotated principal components of predictors of global naturalization success measured for biogeographic syndromes (‘BG’)
Full size table
Extended Data Table 2 Coefficients from linear regression predicting global naturalization success across biogeographic syndromes (n = 19)
Full size table
Extended Data Table 3 Loadings for rotated principal components of predictors of regional naturalization success measured for biogeographic syndromes (‘BGReg’ for biogeographic syndrome by region analysis)
Full size table
Extended Data Table 4 Coefficients from linear mixed model predicting regional naturalization success across biogeographic syndromes (n = 6061 biogeographic syndrome x recipient region comparisons)
Full size table
Extended Data Table 5 Loadings for varimax rotated principal components of predictors of probability of economic use and probability of naturalization among species (‘Spp’)
Full size table
Extended Data Table 6 Coefficients from phylogenetic binomial regression predicting probability of economic use among species (n = 334,667)
Full size table
Extended Data Table 7 Coefficients from phylogenetic binomial regression predicting probability of naturalization among species (n = 334,667)
Full size table
Extended Data Table 8 Loadings for rotated principal components of predictors of number of naturalized regions among species that have naturalized beyond their native distributions (‘Nat’)
Full size table
Extended Data Table 9 Coefficients from phylogenetic linear regression predicting number naturalized regions among species that have naturalized beyond their native distributions (n = 13,280)
Full size table

Extended Data Fig. 1 Drivers of regional naturalization success among biogeographic syndromes (n = 6061 biogeographic syndrome x recipient region comparisons).

Partial residual plots from linear mixed model predicting regional naturalization success among biogeographic syndromes (full results Extended Data Table 4). In the bottom panels, main contributors to a given principal component (loading > 0.50) are listed along the x-axes with the length and direction of arrows indicating the value and sign of the variable loading (see Extended Data Table 3; ‘BGReg’ indicates that PCs for the regional analysis were derived using data for biogeographic syndromes, but not including climate suitability or territorial links). Variables associated with the evolutionary imbalance hypothesis are colored green (Precip. Var. = precipitation variability), anthropogenic variables purple, and climatic suitability in pink. Shaded bands indicate 95% confidence bands.

Supplementary information

Supplementary Information

Supplementary Figs. 1–4, and descriptions for Supplementary Data 1–7 and Supplementary Code 1.

Reporting Summary

Peer Review File

Supplementary Data 1

Table describing matching between GloNAF and TDWG3 regions in .csv format.

Supplementary Data 2

Data for TDWG3 regions, including information for matching to country level data (columns ‘Country1’ to ‘Country6’) in .csv format.

Supplementary Data 3

Data for biogeographic syndromes in .csv format.

Supplementary Data 4

Data for analysis of regional naturalization success in .csv format.

Supplementary Data 5

Species-level data in .csv format.

Supplementary Data 6

Results from single predictor models in .xlsx format.

Supplementary Data 7

Phylogeny used for phylogenetic analyses in Newick (.txt) format.

Supplementary Code 1

R code for reproducing analyses.

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Fristoe, T.S., Bleilevens, J., Kinlock, N.L. et al. Evolutionary imbalance, climate and human history jointly shape the global biogeography of alien plants. Nat Ecol Evol 7, 1633–1644 (2023). https://doi.org/10.1038/s41559-023-02172-z

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