Biological Invasions

, Volume 20, Issue 9, pp 2647–2660 | Cite as

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

  • Michael C. RotterEmail author
  • Liza M. Holeski
Original Paper


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.


Evolution of increased competitive ability EICA Herbivory Non-native plants Meta-analysis 



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).

Supplementary material

10530_2018_1724_MOESM1_ESM.docx (41 kb)
Supplementary material 1 (DOCX 41 kb)
10530_2018_1724_MOESM2_ESM.jpg (5.4 mb)
Supplementary material 2 (JPEG 5499 kb)


  1. 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 211–240Google Scholar
  2. 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):77–86CrossRefGoogle Scholar
  3. Adams DC (2008) Phylogenetic meta-analysis. Evolution 62(3):567–572CrossRefPubMedGoogle Scholar
  4. Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87(7):132–143CrossRefGoogle Scholar
  5. 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):113–116CrossRefPubMedGoogle Scholar
  6. 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):1–15CrossRefGoogle Scholar
  7. 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):2379–2389CrossRefGoogle Scholar
  8. Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17(5):293–302CrossRefPubMedGoogle Scholar
  9. Barton KE (2016) Tougher and thornier: general patterns in the induction of physical defence traits. Funct Ecol 30(2):181–187CrossRefGoogle Scholar
  10. Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37(1):58–67CrossRefGoogle Scholar
  11. Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50(4):1088–1101CrossRefPubMedGoogle Scholar
  12. Blair AC, Wolfe LM (2004) The evolution of an invasive plant: an experimental study with Silene latifolia. Ecology 85(11):3035–3042CrossRefGoogle Scholar
  13. Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83(5):887–889CrossRefGoogle Scholar
  14. 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):856–862CrossRefPubMedGoogle Scholar
  15. 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):1–11CrossRefPubMedGoogle Scholar
  16. Brooks ML (2000) Competition between alien annual grasses and native annual plants in the Mojave Desert. Am Midl Nat 144(1):92–108CrossRefGoogle Scholar
  17. 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):322–334CrossRefGoogle Scholar
  18. Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290(5491):521–523CrossRefPubMedGoogle Scholar
  19. Cappuccino N, Arnason JT (2006) Novel chemistry of invasive exotic plants. Biol Let 2(2):189–193CrossRefGoogle Scholar
  20. Cappuccino N, Carpenter D (2005) Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol Let 1(4):435–438CrossRefGoogle Scholar
  21. Carmona D, Lajeunesse MJ, Johnson MT (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25(2):358–367CrossRefGoogle Scholar
  22. Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15(1):22–40CrossRefGoogle Scholar
  23. 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):1255–1267CrossRefPubMedGoogle Scholar
  24. Cooper HM, Lindsay JLL (1998) Research synthesis and meta-analysis. Sage Publications, Thousand OaksGoogle Scholar
  25. 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):335–380CrossRefGoogle Scholar
  26. Cornell HV, Hawkins BA (2003) Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. Am Nat 161(4):507–522CrossRefPubMedGoogle Scholar
  27. 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):103–112CrossRefGoogle Scholar
  28. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88(3):528–534CrossRefGoogle Scholar
  29. Doorduin LJ, Vrieling K (2011) A review of the phytochemical support for the shifting defence hypothesis. Phytochem Rev 10(1):99–106CrossRefPubMedGoogle Scholar
  30. Duncan RP, Williams PA (2002) Ecology: Darwin’s naturalization hypothesis challenged. Nature 417(6889):608–609CrossRefPubMedGoogle Scholar
  31. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci 97(13):7043–7050CrossRefPubMedGoogle Scholar
  32. 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):739–751CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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):e49114CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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):404–414CrossRefPubMedGoogle Scholar
  35. Graves SD, Shapiro AM (2003) Exotics as host plants of the California butterfly fauna. Biol Cons 110(3):413–433CrossRefGoogle Scholar
  36. 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):521–532CrossRefGoogle Scholar
  37. Harris GA (1977) Root phenology as a factor of competition among grass seedlings. J Range Manag 14(2):172–177CrossRefGoogle Scholar
  38. Hedges L, Olkin I (1985) Statistical models for meta-analysis. Academic Press, New YorkGoogle Scholar
  39. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  40. Hill SB, Kotanen PM (2009) Evidence that phylogenetically novel non-indigenous plants experience less herbivory. Oecologia 161:581–590CrossRefPubMedGoogle Scholar
  41. 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):e26275CrossRefPubMedPubMedCentralGoogle Scholar
  42. Huang W, Ding J (2015) Effects of generalist herbivory on resistance and resource allocation by the invasive plant, Phytolacca americana. Insect Sci 23:191–199CrossRefPubMedGoogle Scholar
  43. 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):1157–1167CrossRefGoogle Scholar
  44. Joshi S, Tielbörger K (2012) Response to enemies in the invasive plant Lythrum salicaria is genetically determined. Ann Bot 110(7):1403–1410CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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):704–714CrossRefGoogle Scholar
  46. Koricheva J (2002) Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83(1):176–190CrossRefGoogle Scholar
  47. Koricheva J, Gurevitch J, Mengersen K (2013) Handbook of meta-analysis in ecology and evolution. Princeton University Press, PrincetonCrossRefGoogle Scholar
  48. 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):378–387CrossRefGoogle Scholar
  49. Lajeunesse MJ (2009) Meta-analysis and the comparative phylogenetic method. Am Nat 174(3):369–381PubMedGoogle Scholar
  50. Lajeunesse MJ (2011) phyloMeta: a program for phylogenetic comparative analyses with meta-analysis. Bioinformatics 27(18):2603–2604PubMedGoogle Scholar
  51. Lajeunesse MJ, Forbes MR (2003) Variable reporting and quantitative reviews: a comparison of three meta-analytical techniques. Ecol Lett 6(5):448–454CrossRefGoogle Scholar
  52. Lankau RA (2007) Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytol 175(1):176–184CrossRefPubMedGoogle Scholar
  53. Liao ZY, Zheng YL, Lei YB, Feng YL (2014) Evolutionary increases in defense during a biological invasion. Oecologia 174(4):1205–1214CrossRefPubMedGoogle Scholar
  54. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20(5):223–228CrossRefPubMedGoogle Scholar
  55. Maron JL, Vilà M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypothesis. Oikos 95:361–373CrossRefGoogle Scholar
  56. 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 21:213–222CrossRefGoogle Scholar
  57. 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):299–307CrossRefPubMedGoogle Scholar
  58. Mithöfer A, Boland W (2008) Recognition of herbivory-associated molecular patterns. Plant Physiol 146(3):825–831CrossRefPubMedPubMedCentralGoogle Scholar
  59. Moloney KA, Holzapfel C, Tielbörger K, Jeltsch F, Schurr FM (2009) Rethinking the common garden in invasion research. Perspect Plant Ecol Evol Syst 11:311–320CrossRefGoogle Scholar
  60. 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):e17227CrossRefPubMedPubMedCentralGoogle Scholar
  61. Müller C, Martens N (2005) Testing predictions of the ‘evolution of increased competitive ability’hypothesis for an invasive crucifer. Evol Ecol 19(6):533–550CrossRefGoogle Scholar
  62. 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):82–93CrossRefPubMedGoogle Scholar
  63. 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):536–544CrossRefPubMedGoogle Scholar
  64. Orians CM, Ward D (2010) Evolution of plant defenses in nonindigenous environments. Annu Rev Entomol 55:439–459CrossRefPubMedGoogle Scholar
  65. Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8(9):959–967CrossRefGoogle Scholar
  66. 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):59–72CrossRefGoogle Scholar
  67. 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 97–125Google Scholar
  68. 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):1081–1099CrossRefGoogle Scholar
  69. 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):1–12CrossRefGoogle Scholar
  70. Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77(6):1655–1661CrossRefGoogle Scholar
  71. 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):369–386CrossRefGoogle Scholar
  72. Rosenberg MS (2005) The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59(2):464–468CrossRefPubMedGoogle Scholar
  73. Rosenberg MS, Adams DC, Gurevitch J (2000) MetaWin: statistical software for meta-analysis. Sinauer Associates, SunderlandGoogle Scholar
  74. Sax DF, Stachowicz JJ, Gaines SD (2005) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates, SunderlandGoogle Scholar
  75. Scott JA (1992) The butterflies of North America: a natural history and field guide. Stanford University Press, StanfordGoogle Scholar
  76. 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):13384–13389CrossRefPubMedGoogle Scholar
  77. Siemann E, Rogers WE (2001) Genetic differences in growth of an invasive tree species. Ecol Lett 4(6):514–518CrossRefGoogle Scholar
  78. Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102CrossRefGoogle Scholar
  79. Stastny M, Schaffner URS, Elle E (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J Ecol 93(1):27–37CrossRefGoogle Scholar
  80. 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):333–345CrossRefGoogle Scholar
  81. Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21(4):208–216CrossRefPubMedGoogle Scholar
  82. Uesugi A, Kessler A (2013) Herbivore exclusion drives the evolution of plant competitiveness via increased allelopathy. New Phytol 198(3):916–924CrossRefPubMedGoogle Scholar
  83. van der Meijden E (1996) Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomological Experimentalis et Applicata 80:307–310CrossRefGoogle Scholar
  84. 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):235–245CrossRefPubMedGoogle Scholar
  85. 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):941–947CrossRefGoogle Scholar
  86. Webb CO, Donoghue MJ (2004) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol News 5:181–183CrossRefGoogle Scholar
  87. Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers Distrib 14(4):569–580CrossRefGoogle Scholar
  88. 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):632–640CrossRefPubMedGoogle Scholar
  89. Wolfe LM (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am Nat 160:705–711PubMedGoogle Scholar
  90. Wolfe LM, Elzinga JA, Biere A (2004) Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia. Ecol Lett 7(9):813–820CrossRefGoogle Scholar
  91. 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):339–346CrossRefGoogle Scholar
  92. Younginger BS, Sirova D, Cruzan MB, Balhorn DJ (2017) Is biomass a reliable estimate of plant fitness? Appl Plant Sci 5(2):1600094CrossRefGoogle Scholar
  93. 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):1350–1359CrossRefPubMedGoogle Scholar
  94. Zou J, Rogers WE, Siemann E (2008) Increased competitive ability and herbivory tolerance in the invasive plant Sapium sebiferum. Biol Invasions 10(3):291–302CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesNorthern Arizona UniversityFlagstaffUSA

Personalised recommendations