Exotic plant invaders pose a serious threat to native plants. However, despite showing inferior competitive ability and decreased performance, native species often subsist in invaded communities. The decline of native populations is hypothesized to be halted and eventually reversed if adaptive evolutionary changes can keep up with the environmental stress induced by invaders, that is, when population extinction is prevented by evolutionary rescue (ER). Nevertheless, evidence for the role of ER in postinvasion persistence of native flora remains scarce. Here, I explored the population density of a native forb, Veronica chamaedrys, and evaluated the changes in the shade-responsive traits of its populations distributed along the invasion chronosequence of an exotic transformer, Heracleum mantegazzianum, which was replicated in five areas. I found a U-shaped population trajectory that paralleled the evolution of plasticity to shade. Whereas V. chamaedrys genotypes from intact, more open sites exhibited a shade-tolerance strategy (pronounced leaf area/mass ratio), reduced light availability at the invaded sites selected for a shade-avoidance strategy (greater internode elongation). Field experiments subsequently confirmed that the shifts in shade-response strategies were adaptive and secured postinvasion population persistence, as indicated by further modeling. Alternative ecological mechanisms (habitat improvement or arrival of immigrants) were less likely explanations than ER for the observed population rebound, although the contribution of maternal effects cannot be dismissed. These results suggest that V. chamaedrys survived because of adaptive evolutionary changes operating on the same timescale as the invasion-induced stress, but the generality of ER for postinvasion persistence of native plants remains unknown.

Institute of Botany The Czech Academy of Sciences CZ 252 43 Průhonice Czech Republic

Zobrazit více v PubMed

Callaway R. M., Aschehoug E. T., Invasive plants versus their new and old neighbors: A mechanism for exotic invasion. Science 290, 521–523 (2000). PubMed

Phillips B. L., Shine R., Adapting to an invasive species: Toxic cane toads induce morphological change in Australian snakes. Proc. Natl. Acad. Sci. U.S.A. 101, 17 150–17 155 (2004). PubMed PMC

Engelkes T., et al. , Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature 456, 946–948 (2008). PubMed

Alexander J. M., Diez J. M., Levine J. M., Novel competitors shape species’ responses to climate change. Nature 525, 515–518 (2015). PubMed

Rosenberger D. W., Venette R. C., Aukema B. H., Development of an aggressive bark beetle on novel hosts: Implications for outbreaks in an invaded range. J. Appl. Ecol. 55, 1526–1537 (2018).

Vilà M., et al. , Ecological impacts of invasive alien plants: A meta-analysis of their effects on species, communities and ecosystems. Ecol. Lett. 14, 702–708 (2011). PubMed

Gurevitch J., Padilla D. K., Are invasive species a major cause of extinctions? Trends Ecol. Evol. 19, 470–474 (2004). PubMed

Sax D. F., Gaines S. D., Colloquium paper: Species invasions and extinction: The future of native biodiversity on islands. Proc. Natl. Acad. Sci. U.S.A. 105 (suppl. 1), 11490–11497 (2008). PubMed PMC

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

Powell K. I., Chase J. M., Knight T. M., Invasive plants have scale-dependent effects on diversity by altering species-area relationships. Science 339, 316–318 (2013). PubMed

Gilbert B., Levine J. M., Plant invasions and extinction debts. Proc. Natl. Acad. Sci. U.S.A. 110, 1744–1749 (2013). PubMed PMC

Strauss S. Y., Lau J. A., Carroll S. P., Evolutionary responses of natives to introduced species: What do introductions tell us about natural communities? Ecol. Lett. 9, 357–374 (2006). PubMed

Strayer D. L., Eviner V. T., Jeschke J. M., Pace M. L., Understanding the long-term effects of species invasions. Trends Ecol. Evol. 21, 645–651 (2006). PubMed

Lankau R. A., Nuzzo V., Spyreas G., Davis A. S., Evolutionary limits ameliorate the negative impact of an invasive plant. Proc. Natl. Acad. Sci. U.S.A. 106, 15362–15367 (2009). PubMed PMC

Dostál P., Müllerová J., Pyšek P., Pergl J., Klinerová T., The impact of an invasive plant changes over time. Ecol. Lett. 16, 1277–1284 (2013). PubMed

Bell G., Evolutionary rescue. Annu. Rev. Ecol. Evol. Syst. 48, 605–627 (2017).

Carlson S. M., Cunningham C. J., Westley P. A. H., Evolutionary rescue in a changing world. Trends Ecol. Evol. 29, 521–530 (2014). PubMed

Gomulkiewicz R., Holt R. D., When does evolution by natural selection prevent extinction? Evolution 49, 201–207 (1995). PubMed

Hufbauer R. A., et al. , Three types of rescue can avert extinction in a changing environment. Proc. Natl. Acad. Sci. U.S.A. 112, 10557–10562 (2015). PubMed PMC

Gomulkiewicz R., Shaw R. G., Evolutionary rescue beyond the models. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20120093 (2013). PubMed PMC

Charmantier A., et al. , Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800–803 (2008). PubMed

Pyšek P., Heracleum mantegazzianum in the Czech Republic: Dynamics of spreading from the historical perspective. Folia Geobot. Phytotaxon. 26, 439–454 (1991).

Hejda M., Pyšek P., Jarošík V., Impact of invasive plants on the species richness, diversity and composition of invaded communities. J. Ecol. 97, 393–403 (2009).

Jandová K., et al. , Long-term impact of Heracleum mantegazzianum invasion on soil chemical and biological characteristics. Soil Biol. Biochem. 68, 270–278 (2014).

Franklin K. A., Shade avoidance. New Phytol. 179, 930–944 (2008). PubMed

Novoplansky A., Picking battles wisely: Plant behaviour under competition. Plant Cell Environ. 32, 726–741 (2009). PubMed

Gruntman M., Groß D., Májeková M., Tielbörger K., Decision-making in plants under competition. Nat. Commun. 8, 2235 (2017). PubMed PMC

Gommers C. M. M., Visser E. J. W., St Onge K. R., Voesenek L. A. C. J., Pierik R., Shade tolerance: When growing tall is not an option. Trends Plant Sci. 18, 65–71 (2013). PubMed

Galloway L. F., Etterson J. R., Transgenerational plasticity is adaptive in the wild. Science 318, 1134–1136 (2007). PubMed

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

Germain R. M., Srivastava D., Angert A. L., Evolution of an inferior competitor increases resistance to biological invasion. Nat. Ecol. Evol. 4, 419–425 (2020). PubMed

Golivets M., Wallin K. F., Neighbour tolerance, not suppression, provides competitive advantage to non-native plants. Ecol. Lett. 21, 745–759 (2018). PubMed

Nomoto H. A., Alexander J. M., Drivers of local extinction risk in alpine plants under warming climate. Ecol. Lett. 24, 1157–1166 (2021). PubMed PMC

Singer M. C., Parmesan C., Lethal trap created by adaptive evolutionary response to an exotic resource. Nature 557, 238–241 (2018). PubMed

Latzel V., Pitfalls in ecological research—Transgenerational effects. Folia Geobot. 50, 75–85 (2015).

van Moorsel S. J., et al. , Evidence for rapid evolution in a grassland biodiversity experiment. Mol. Ecol. 28, 4097–4117 (2019). PubMed

Bates D., Maechler M., Bolker B., Walker S., Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

R Development Core Team, R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2017).

Hothorn T., Bretz F., Westfall P., Simultaneous inference in general parametric models. Biom. J. 50, 346–363 (2008). PubMed

Hanski I., A practical model of metapopulation dynamics. J. Anim. Ecol. 63, 151–162 (1994).

van Kleunen M., Schlaepfer D. R., Glaettli M., Fischer M., Preadapted for invasiveness: Do species traits or their plastic response to shading differ between invasive and non-invasive plant species in their native range? J. Biogeogr. 38, 1294–1304 (2011).

Zhang Y. Y., Fischer M., Colot V., Bossdorf O., Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol. 197, 314–322 (2013). PubMed

Robinson G. K., That BLUP is a good thing: The estimation of random effects. Stat. Sci. 6, 15–32 (1991).

Berlin S., et al. , Genetics of phenotypic plasticity and biomass traits in hybrid willows across contrasting environments and years. Ann. Bot. 120, 87–100 (2017). PubMed PMC

Lankau R. A., Coevolution between invasive and native plants driven by chemical competition and soil biota. Proc. Natl. Acad. Sci. U.S.A. 109, 11240–11245 (2012). PubMed PMC

Dahlgren J. P., Ehrlén J., Incorporating environmental change over succession in an integral projection model of population dynamics of a forest herb. Oikos 120, 1183–1190 (2011).

Hairston N. G. Jr., Ellner S. P., Geber M. A., Yoshida T., Fox J. A., Rapid evolution and the convergence of ecological and evolutionary time. Ecol. Lett. 8, 1114–1127 (2005).