The role of phylogenetic relatedness on alien plant success depends on the stage of invasion.
Journal
Nature plants
ISSN: 2055-0278
Titre abrégé: Nat Plants
Pays: England
ID NLM: 101651677
Informations de publication
Date de publication:
08 2022
08 2022
Historique:
received:
25
11
2021
accepted:
07
07
2022
pubmed:
12
8
2022
medline:
19
8
2022
entrez:
11
8
2022
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 35953709
doi: 10.1038/s41477-022-01216-9
pii: 10.1038/s41477-022-01216-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
906-914Subventions
Organisme : Austrian Science Fund FWF
ID : I 3757
Pays : Austria
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Richardson, D. M. et al. Naturalization and invasion of alien plants: concepts and definitions. Divers. Distrib. 6, 93–107 (2000).
doi: 10.1046/j.1472-4642.2000.00083.x
van Kleunen, M. et al. Global exchange and accumulation of non-native plants. Nature 525, 100–103 (2015).
pubmed: 26287466
doi: 10.1038/nature14910
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: 26068851
doi: 10.1126/science.aaa8913
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).
pmcid: 3597245
doi: 10.1111/j.1365-2486.2011.02636.x
Pyšek, P. et al. Scientists’ warning on invasive alien species. Biol. Rev. 95, 1511–1534 (2020).
pubmed: 32588508
doi: 10.1111/brv.12627
Bacher, S. et al. Socio-economic impact classification of alien taxa (SEICAT). Methods Ecol. Evol. 9, 159–168 (2018).
doi: 10.1111/2041-210X.12844
Seebens, H. et al. No saturation in the accumulation of alien species worldwide. Nat. Commun. 8, 14435 (2017).
pubmed: 28198420
pmcid: 5316856
doi: 10.1038/ncomms14435
Seebens, H. et al. Projecting the continental accumulation of alien species through to 2050. Glob. Chang. Biol. 27, 970–982 (2021).
doi: 10.1111/gcb.15333
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: 10.1046/j.1365-2664.2003.00777.x
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: 26152518
doi: 10.1111/gcb.13021
Razanajatovo, M. et al. Plants capable of selfing are more likely to become naturalized. Nat. Commun. 7, 13313 (2016).
pubmed: 27796365
pmcid: 5095580
doi: 10.1038/ncomms13313
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: 10.1111/j.1365-2745.2008.01469.x
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: 10.1111/j.1365-2435.2010.01739.x
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: 20002494
doi: 10.1111/j.1461-0248.2009.01418.x
van Kleunen, M., Dawson, W. & Maurel, N. Characteristics of successful alien plants. Mol. Ecol. 24, 1954–1968 (2015).
pubmed: 25421056
doi: 10.1111/mec.13013
Essl, F. et al. Drivers of the relative richness of naturalized and invasive plant species on Earth. AoB Plants 11, plz051 (2019).
pubmed: 31636882
pmcid: 6795282
doi: 10.1093/aobpla/plz051
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: 30011076
doi: 10.1002/ajb2.1126
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: 30401825
pmcid: 6219509
doi: 10.1038/s41467-018-06995-4
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: 10.1016/j.jenvman.2021.113054
Ni, M. et al. Invasion success and impacts depend on different characteristics in non-native plants. Divers. Distrib. 27, 1194–1207 (2021).
doi: 10.1111/ddi.13267
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: 34050023
pmcid: 8179145
doi: 10.1073/pnas.2021173118
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: 10.1111/ecog.05669
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: 26236872
doi: 10.1890/14-1005.1
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: 10.1007/s10530-021-02495-7
Duncan, R. P. & Williams, P. A. Darwin’s naturalization hypothesis challenged. Nature 417, 608–609 (2002).
pubmed: 12050652
doi: 10.1038/417608a
Daehler, C. C. Darwin’s naturalization hypothesis revisited. Am. Nat. 158, 324–330 (2001).
pubmed: 18707328
doi: 10.1086/321316
Pyšek, P. Is there a taxonomic pattern to plant invasions? Oikos 82, 282–294 (1998).
doi: 10.2307/3546968
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: 26098339
doi: 10.1086/681584
Thuiller, W. et al. Resolving Darwin’s naturalization conundrum: a quest for evidence. Divers. Distrib. 16, 461–475 (2010).
doi: 10.1111/j.1472-4642.2010.00645.x
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: 10.1111/1365-2745.12986
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: 10.1111/geb.12317
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: 10.1111/ddi.12401
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: 18400019
doi: 10.1111/j.1461-0248.2008.01178.x
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: 29489400
doi: 10.1146/annurev-arplant-042817-040339
van Kleunen, M., Bossdorf, O. & Dawson, W. The ecology and evolution of alien plants. Annu. Rev. Ecol. Evol. Syst. 49, 25–47 (2018).
doi: 10.1146/annurev-ecolsys-110617-062654
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: 32366659
pmcid: 7245080
doi: 10.1073/pnas.1918100117
Diez, J. M. et al. Learning from failures: testing broad taxonomic hypotheses about plant naturalization. Ecol. Lett. 12, 1174–1183 (2009).
pubmed: 19723283
doi: 10.1111/j.1461-0248.2009.01376.x
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: 10.1111/1365-2745.13059
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: 21320262
doi: 10.1111/j.1461-0248.2011.01600.x
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: 16581902
pmcid: 1421337
doi: 10.1073/pnas.0508073103
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: 26437879
doi: 10.1111/ele.12522
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: 10.1556/ComEc.14.2013.2.7
Blackburn, T. M. et al. A proposed unified framework for biological invasions. Trends Ecol. Evol. 26, 333–339 (2011).
pubmed: 21601306
doi: 10.1016/j.tree.2011.03.023
van Kleunen, M. et al. Economic use of plants is key to their naturalization success. Nat. Commun. 11, 3201 (2020).
pubmed: 32581263
pmcid: 7314777
doi: 10.1038/s41467-020-16982-3
Broennimann, O. et al. Distance to native climatic niche margins explains establishment success of alien mammals. Nat. Commun. 12, 2353 (2021).
pubmed: 33883555
pmcid: 8060396
doi: 10.1038/s41467-021-22693-0
Carboni, M. et al. What it takes to invade grassland ecosystems: traits, introduction history and filtering processes. Ecol. Lett. 19, 219–229 (2016).
pubmed: 26689431
doi: 10.1111/ele.12556
Milbau, A. & Stout, J. C. Factors associated with alien plants transitioning from casual, to naturalized, to invasive. Conserv. Biol. 22, 308–317 (2008).
pubmed: 18261149
doi: 10.1111/j.1523-1739.2007.00877.x
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: 10.1111/j.1365-2745.2009.01519.x
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: 10.1016/0006-3207(96)00026-2
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: 10.1111/geb.12520
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: 10.1641/0006-3568(2001)051[0103:HAAPOI]2.0.CO;2
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: 10.1007/s10530-015-0990-4
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: 10.1111/ddi.12351
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: 10.1080/03057070.2011.579434
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: 10.1111/1365-2664.12365
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: 10.1111/oik.07680
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: 10.1111/j.1365-2745.2009.01565.x
Valiente-Banuet, A. & Verdu, M. Plant facilitation and phylogenetics. Annu. Rev. Ecol. Evol. Syst. 44, 347–366 (2013).
doi: 10.1146/annurev-ecolsys-110512-135855
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: 27859164
doi: 10.1890/15-1285.1
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: 21508611
doi: 10.1086/659060
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: 32605513
pmcid: 7423470
doi: 10.1098/rspb.2020.1070
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: 34476548
doi: 10.1007/s00442-021-05024-4
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: 10.1111/1365-2745.12410
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: 10.1111/ddi.13220
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: 35199921
doi: 10.1111/ele.13899
Smith, S. A. & Brown, J. W. Constructing a broadly inclusive seed plant phylogeny. Am. J. Bot. 105, 302–314 (2018).
pubmed: 29746720
doi: 10.1002/ajb2.1019
Henderson, L. Comparisons of invasive plants in Southern Africa originating from southern temperate, northern temperate and tropical regions. Bothalia 36, 201–222 (2006).
doi: 10.4102/abc.v36i2.362
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: 10.1111/jbi.13623
van Kleunen, M. et al. The Global Naturalized Alien Flora (GloNAF) database. Ecology 100, e02542 (2019).
pubmed: 30341991
doi: 10.1002/ecy.2542
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: 10.1111/j.2041-210X.2011.00169.x
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: 10.1111/j.2041-210X.2010.00012.x
Nagelkerke, N. J. D. A note on a general definition of the coefficient of determination. Biometrika 78, 691–692 (1991).
doi: 10.1093/biomet/78.3.691
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: 10.1093/sysbio/syu005