Skip to main content
Springer Nature Link
Log in

A meta-analysis of the evolution of increased competitive ability hypothesis: genetic-based trait variation and herbivory resistance trade-offs

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Non-native organisms are an abundant component of almost all global ecosystems. A prominent framework to explain the success of non-native plants is the evolution of increased competitive ability (EICA) hypothesis. EICA predicts that plants escape from co-evolved herbivores after introduction into a non-native habitat. Assuming limited resources, a relaxation in selection pressures for resistance traits against the co-evolved specialist herbivores allows plants to allocate increased resources to traits related to fitness and/or competitive ability. Despite the prominence of the EICA hypothesis in the literature, empirical evidence has been mixed. We conducted a meta-analysis on 30 studies that focused on genetic-based trait variation and the trade-off between resistance traits and fitness to assess support for the EICA hypothesis. We found general support for EICA across studies. Performance of herbivores was higher on non-native plant populations than on native populations of the same species. Fitness trait values were higher in non-native populations, relative to native, and we found evidence for trade-offs between herbivore performance and plant fitness traits. Support for EICA was strongest when we focused on direct measurements of herbivore performance, and weakest when we assessed resistance traits, highlighting the complex and often unknown relationship between resistance traits and particular herbivores in many plant–herbivore systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aarssen LW (2005) On size, fecundity, and fitness in competing plants. In: Reekie E, Bazzaz FA (eds) Reproductive allocation in plants. Elsevier Academic Press, Oxford, pp 211–240

    Google Scholar 

  • Abhilasha D, Joshi J (2009) Enhanced fitness due to higher fecundity, increased defence against a specialist and tolerance towards a generalist herbivore in an invasive annual plant. J Plant Ecol 2(2):77–86

    Article  Google Scholar 

  • Adams DC (2008) Phylogenetic meta-analysis. Evolution 62(3):567–572

    Article  PubMed  Google Scholar 

  • Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87(7):132–143

    Article  Google Scholar 

  • Agrawal AA, Hastings AP, Johnson MT, Maron JL, Salminen JP (2012) Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338(6103):113–116

    Article  PubMed  CAS  Google Scholar 

  • Agrawal AA, Hastings AP, Bradburd GS, Woods EC, Züst T, Harvey JA, Bukovinszky T (2015) Evolution of plant growth and defense in a continental introduction. Am Nat 186(1):1–15

    Article  Google Scholar 

  • Alba C, Bowers MD, Blumenthal D, Hufbauer R (2011) Evolution of growth but not structural or chemical defense in Verbascum thapsus (common mullein) following introduction to North America. Biol Invasions 13(10):2379–2389

    Article  Google Scholar 

  • Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17(5):293–302

    Article  PubMed  CAS  Google Scholar 

  • Barton KE (2016) Tougher and thornier: general patterns in the induction of physical defence traits. Funct Ecol 30(2):181–187

    Article  Google Scholar 

  • Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37(1):58–67

    Article  Google Scholar 

  • Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50(4):1088–1101

    Article  PubMed  CAS  Google Scholar 

  • Blair AC, Wolfe LM (2004) The evolution of an invasive plant: an experimental study with Silene latifolia. Ecology 85(11):3035–3042

    Article  Google Scholar 

  • Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83(5):887–889

    Article  Google Scholar 

  • Bossdorf O, Schroder S, Prati D, Auge H (2004) Palatability and tolerance to simulated herbivory in native and introduced populations of Alliaria petiolata (Brassicaceae). Am J Bot 91(3):856–862

    Article  PubMed  Google Scholar 

  • Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144(1):1–11

    Article  PubMed  Google Scholar 

  • Brooks ML (2000) Competition between alien annual grasses and native annual plants in the Mojave Desert. Am Midl Nat 144(1):92–108

    Article  Google Scholar 

  • Buschmann H, Edwards PJ, Dietz H (2005) Variation in growth pattern and response to slug damage among native and invasive provenances of four perennial Brassicaceae species. J Ecol 93(2):322–334

    Article  Google Scholar 

  • Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290(5491):521–523

    Article  PubMed  CAS  Google Scholar 

  • Cappuccino N, Arnason JT (2006) Novel chemistry of invasive exotic plants. Biol Let 2(2):189–193

    Article  CAS  Google Scholar 

  • Cappuccino N, Carpenter D (2005) Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol Let 1(4):435–438

    Article  Google Scholar 

  • Carmona D, Lajeunesse MJ, Johnson MT (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25(2):358–367

    Article  Google Scholar 

  • Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15(1):22–40

    Article  Google Scholar 

  • Cipollini D, Mbagwu J, Barto K, Hillstrom C, Enright S (2005) Expression of constitutive and inducible chemical defenses in native and invasive populations of Alliaria petiolata. J Chem Ecol 31(6):1255–1267

    Article  PubMed  CAS  Google Scholar 

  • Cooper HM, Lindsay JLL (1998) Research synthesis and meta-analysis. Sage Publications, Thousand Oaks

    Google Scholar 

  • Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Pausas JG (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51(4):335–380

    Article  Google Scholar 

  • Cornell HV, Hawkins BA (2003) Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. Am Nat 161(4):507–522

    Article  PubMed  Google Scholar 

  • Cripps MG, Hinz HL, McKenney JL, Price WJ, Schwarzländer M (2009) No evidence for an ‘evolution of increased competitive ability’ for the invasive Lepidium draba. Basic Appl Ecol 10(2):103–112

    Article  Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88(3):528–534

    Article  Google Scholar 

  • Doorduin LJ, Vrieling K (2011) A review of the phytochemical support for the shifting defence hypothesis. Phytochem Rev 10(1):99–106

    Article  PubMed  CAS  Google Scholar 

  • Duncan RP, Williams PA (2002) Ecology: Darwin’s naturalization hypothesis challenged. Nature 417(6889):608–609

    Article  PubMed  CAS  Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci 97(13):7043–7050

    Article  PubMed  CAS  Google Scholar 

  • Felker-Quinn E, Schweitzer JA, Bailey JK (2013) Meta-analysis reveals evolution in invasive plant species but little support for evolution of increased competitive ability (EICA). Ecol Evol 3(3):739–751

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukano Y, Yahara T (2012) Changes in defense of an alien plant Ambrosia artemisiifolia before and after the invasion of a native specialist enemy Ophraella communa. PLoS ONE 7(11):e49114

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Genton BJ, Kotanen PM, Cheptou PO, Adolphe C, Shykoff JA (2005) Enemy release but no evolutionary loss of defence in a plant invasion: an inter-continental reciprocal transplant experiment. Oecologia 146(3):404–414

    Article  PubMed  Google Scholar 

  • Graves SD, Shapiro AM (2003) Exotics as host plants of the California butterfly fauna. Biol Cons 110(3):413–433

    Article  Google Scholar 

  • Guo WF, Zhang J, Li XQ, Ding JQ (2011) Increased reproductive capacity and physical defense but decreased tannin content in an invasive plant. Insect Sci 18(5):521–532

    Article  Google Scholar 

  • Harris GA (1977) Root phenology as a factor of competition among grass seedlings. J Range Manag 14(2):172–177

    Article  Google Scholar 

  • Hedges L, Olkin I (1985) Statistical models for meta-analysis. Academic Press, New York

    Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Hill SB, Kotanen PM (2009) Evidence that phylogenetically novel non-indigenous plants experience less herbivory. Oecologia 161:581–590

    Article  PubMed  Google Scholar 

  • Hornoy B, Tarayre M, Hervé M, Gigord L, Atlan A (2011) Invasive plants and enemy release: evolution of trait means and trait correlations in Ulex europaeus. PLoS ONE 6(10):e26275

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang W, Ding J (2015) Effects of generalist herbivory on resistance and resource allocation by the invasive plant, Phytolacca americana. Insect Sci 23:191–199

    Article  PubMed  Google Scholar 

  • Huang W, Siemann E, Wheeler GS, Zou J, Carrillo J, Ding J (2010) Resource allocation to defence and growth are driven by different responses to generalist and specialist herbivory in an invasive plant. J Ecol 98(5):1157–1167

    Article  Google Scholar 

  • Joshi S, Tielbörger K (2012) Response to enemies in the invasive plant Lythrum salicaria is genetically determined. Ann Bot 110(7):1403–1410

    Article  PubMed  PubMed Central  Google Scholar 

  • Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8(7):704–714

    Article  Google Scholar 

  • Koricheva J (2002) Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83(1):176–190

    Article  Google Scholar 

  • Koricheva J, Gurevitch J, Mengersen K (2013) Handbook of meta-analysis in ecology and evolution. Princeton University Press, Princeton

    Book  Google Scholar 

  • Kumschick S, Hufbauer RA, Alba C, Blumenthal DM (2013) Evolution of fast-growing and more resistant phenotypes in introduced common mullein (Verbascum thapsus). J Ecol 101(2):378–387

    Article  Google Scholar 

  • Lajeunesse MJ (2009) Meta-analysis and the comparative phylogenetic method. Am Nat 174(3):369–381

    PubMed  Google Scholar 

  • Lajeunesse MJ (2011) phyloMeta: a program for phylogenetic comparative analyses with meta-analysis. Bioinformatics 27(18):2603–2604

    PubMed  CAS  Google Scholar 

  • Lajeunesse MJ, Forbes MR (2003) Variable reporting and quantitative reviews: a comparison of three meta-analytical techniques. Ecol Lett 6(5):448–454

    Article  Google Scholar 

  • Lankau RA (2007) Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytol 175(1):176–184

    Article  PubMed  Google Scholar 

  • Liao ZY, Zheng YL, Lei YB, Feng YL (2014) Evolutionary increases in defense during a biological invasion. Oecologia 174(4):1205–1214

    Article  PubMed  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20(5):223–228

    Article  PubMed  Google Scholar 

  • Maron JL, Vilà M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypothesis. Oikos 95:361–373

    Article  Google Scholar 

  • Memmott J, Fowler SV, Paynter Q, Sheppard AW, Syrett P (2000) The invertebrate fauna on broom, Cytisus scoparius, in two native and two exotic habitats. Acta Oecol 21:213–222

    Article  Google Scholar 

  • Meyer G, Clare R, Weber E (2005) An experimental test of the evolution of increased competitive ability hypothesis in goldenrod, Solidago gigantea. Oecologia 144(2):299–307

    Article  PubMed  Google Scholar 

  • Mithöfer A, Boland W (2008) Recognition of herbivory-associated molecular patterns. Plant Physiol 146(3):825–831

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moloney KA, Holzapfel C, Tielbörger K, Jeltsch F, Schurr FM (2009) Rethinking the common garden in invasion research. Perspect Plant Ecol Evol Syst 11:311–320

    Article  Google Scholar 

  • Morrison WE, Hay ME (2011) Herbivore preference for native vs. exotic plants: generalist herbivores from multiple continents prefer exotic plants that are evolutionarily naïve. PLoS ONE 6(3):e17227

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Müller C, Martens N (2005) Testing predictions of the ‘evolution of increased competitive ability’hypothesis for an invasive crucifer. Evol Ecol 19(6):533–550

    Article  Google Scholar 

  • Nötzold R, Blossey B, Newton E (1997) The influence of below ground herbivory and plant competition on growth and biomass allocation of purple loosestrife. Oecologia 113(1):82–93

    Article  PubMed  Google Scholar 

  • Oduor AM, Lankau RA, Strauss SY, Gómez JM (2011) Introduced Brassica nigra populations exhibit greater growth and herbivore resistance but less tolerance than native populations in the native range. New Phytol 191(2):536–544

    Article  PubMed  Google Scholar 

  • Orians CM, Ward D (2010) Evolution of plant defenses in nonindigenous environments. Annu Rev Entomol 55:439–459

    Article  PubMed  CAS  Google Scholar 

  • Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8(9):959–967

    Article  Google Scholar 

  • Parker IM, Rodriguez J, Loik ME (2003) An evolutionary approach to understanding the biology of invasions: local adaptation and general-purpose genotypes in the weed Verbascum thapsus. Conserv Biol 17(1):59–72

    Article  Google Scholar 

  • Pyšek P, Richardson DM (2008) Traits associated with invasiveness in alien plants: Where do we stand? In: Nentwig W (ed) Biological invasions. Springer, New York, pp 97–125

    Google Scholar 

  • Rapo C, Müller-Schärer H, Vrieling K, Schaffner U (2010) Is there rapid evolutionary response in introduced populations of tansy ragwort, Jacobaea vulgaris, when exposed to biological control? Evol Ecol 24(5):1081–1099

    Article  Google Scholar 

  • Reddy AM, Carruthers RI, Mills NJ (2015) No evolution of reduced resistance and compensation for psyllid herbivory by the invasive Genista monspessulana. Plant Ecol 216(10):1–12

    Article  Google Scholar 

  • Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77(6):1655–1661

    Article  Google Scholar 

  • Ridenour WM, Vivanco JM, Feng Y, Horiuchi JI, Callaway RM (2008) No evidence for trade-offs: Centaurea plants from America are better competitors and defenders. Ecol Monogr 78(3):369–386

    Article  Google Scholar 

  • Rosenberg MS (2005) The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59(2):464–468

    Article  PubMed  Google Scholar 

  • Rosenberg MS, Adams DC, Gurevitch J (2000) MetaWin: statistical software for meta-analysis. Sinauer Associates, Sunderland

    Google Scholar 

  • Sax DF, Stachowicz JJ, Gaines SD (2005) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates, Sunderland

    Google Scholar 

  • Scott JA (1992) The butterflies of North America: a natural history and field guide. Stanford University Press, Stanford

    Google Scholar 

  • Seabloom EW, Harpole WS, Reichman OJ, Tilman D (2003) Invasion, competitive dominance, and resource use by exotic and native California grassland species. Proc Natl Acad Sci 100(23):13384–13389

    Article  PubMed  CAS  Google Scholar 

  • Siemann E, Rogers WE (2001) Genetic differences in growth of an invasive tree species. Ecol Lett 4(6):514–518

    Article  Google Scholar 

  • Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102

    Article  Google Scholar 

  • Stastny M, Schaffner URS, Elle E (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J Ecol 93(1):27–37

    Article  Google Scholar 

  • Torchin ME, Lafferty KD, Kuris AM (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invasions 3(4):333–345

    Article  Google Scholar 

  • Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21(4):208–216

    Article  PubMed  Google Scholar 

  • Uesugi A, Kessler A (2013) Herbivore exclusion drives the evolution of plant competitiveness via increased allelopathy. New Phytol 198(3):916–924

    Article  PubMed  Google Scholar 

  • van der Meijden E (1996) Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomological Experimentalis et Applicata 80:307–310

    Article  Google Scholar 

  • Van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13(2):235–245

    Article  PubMed  Google Scholar 

  • Wallace BC, Lajeunesse MJ, Dietz G, Dahabreh IJ, Trikalinos TA, Schmid CH, Gurevitch J (2017) OpenMEE: intuitive, open-source software for meta-analysis in ecology and evolutionary biology. Met Eco Evo 8(8):941–947

    Article  Google Scholar 

  • Webb CO, Donoghue MJ (2004) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol News 5:181–183

    Article  Google Scholar 

  • Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers Distrib 14(4):569–580

    Article  Google Scholar 

  • Willis AJ, Thomas MB, Lawton JH (1999) Is the increased vigour of invasive weeds explained by a trade-off between growth and herbivore resistance? Oecologia 120(4):632–640

    Article  PubMed  Google Scholar 

  • Wolfe LM (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am Nat 160:705–711

    PubMed  Google Scholar 

  • Wolfe LM, Elzinga JA, Biere A (2004) Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia. Ecol Lett 7(9):813–820

    Article  Google Scholar 

  • Yang X, Huang W, Tian B, Ding J (2014) Differences in growth and herbivory damage of native and invasive kudzu (Peuraria montana var. lobata) populations grown in the native range. Plant Ecol 215(3):339–346

    Article  Google Scholar 

  • Younginger BS, Sirova D, Cruzan MB, Balhorn DJ (2017) Is biomass a reliable estimate of plant fitness? Appl Plant Sci 5(2):1600094

    Article  Google Scholar 

  • Zheng YL, Feng YL, Zhang LK, Callaway RM, Valiente-Banuet A, Luo DQ, Silva-Pereyra C (2015) Integrating novel chemical weapons and evolutionarily increased competitive ability in success of a tropical invader. New Phytol 205(3):1350–1359

    Article  PubMed  Google Scholar 

  • Zou J, Rogers WE, Siemann E (2008) Increased competitive ability and herbivory tolerance in the invasive plant Sapium sebiferum. Biol Invasions 10(3):291–302

    Article  Google Scholar 

Download references

Acknowledgements

Rotter was supported by the Genes to Environment Program at Northern Arizona University. Thanks to the Holeski lab group, S. M. Mahoney, and several anonymous reviewers for providing comments on a draft of this manuscript as well as to the meta-analysis seminar group and N. C. Nieto at Northern Arizona University. Additional financial support was provided by Northern Arizona University (Holeski start-up funds).

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, USA

    Michael C. Rotter & Liza M. Holeski

Authors
  1. Michael C. Rotter
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Liza M. Holeski
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Michael C. Rotter.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 41 kb)

Supplementary material 2 (JPEG 5499 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rotter, M.C., Holeski, L.M. A meta-analysis of the evolution of increased competitive ability hypothesis: genetic-based trait variation and herbivory resistance trade-offs. Biol Invasions 20, 2647–2660 (2018). https://doi.org/10.1007/s10530-018-1724-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-018-1724-1

Keywords