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Commentary

Enemy release and evolution ofincreased competitive ability: atlast, a smoking gun!

Evolution by natural selection can sometimes be very rapid andtherefore relevant for many ecological questions (Schoener, 2011).One area of ecology where this appears to be particularly true isbiological invasions, probably because species introductions ofteninvolve major changes in biotic interactions and thus novelenvironments with different selective forces than in the species

native ranges. The study of evolutionary changes in invasive specieshas recently become an extremely active area of research (Bossdorfet al., 2005; Prentis et al., 2008), and one of the keyhypotheses thatstimulated this research was the evolution of increased competitiveability (EICA) hypothesis (Blossey & Notzold, 1995). It proposesthat release from natural enemies, and subsequent evolution ofmore competitive genotypes, may explain the increased perfor-mance of dominant plant invaders in their introduced ranges.

Although the original EICA paper has now been cited over 500times, and numerous studies examined the (putative) consequencesof EICA by comparing growth, competitive ability and/orherbivore defence of native and introduced populations in

common environments, with mixed results (Bossdorfet al., 2005;Colautti et al., 2009), there has been surprisingly little proof ofEICA in action. In this issue ofNew Phytologist, Uesugi & Kessler(pp.916924) now present experimental evidence thatrelease fromabove-ground herbivory can indeed cause rapid evolution ofincreased plant competitive ability, and they therefore provide animportant smoking gun for the proposed evolutionary mecha-nism underlying the EICA hypothesis.

the study elegantly links, and in fact, unifies two of the

most popular hypotheses attempting to explaining plantinvasiveness, the EICA hypothesis and the novel weapons

hypothesis

Uesugi & Kessler studied tall goldenrod (Solidago altissima), aperennial plant native to North America but highly invasive inEurope and other parts of the world. They studied goldenrod in itsnative range, in a 12-yr herbivore-exclosure experiment in an oldfield in eastern North America (Fig. 1). Since all study plots were

initially established from the same goldenrod genotypes, any

genetic differentiation observed between herbivore-exclusion andcontrol plots can be causally linked to the experimental treatments,and it is thus evidence of rapid evolution in response to changes inherbivory. Uesugi & Kessler sampled offspring from each of thestudy plots and showed that in a common environment, goldenrodplants from herbivore-exclusion plots performed significantlybetter in the presence of interspecific competitors, and hadsubstantially higher root concentrations of polyacetylenes, putativeallelopathic agents of goldenrod, than plants from control plots.They also showed that the most abundant of the polyacetylenesstrongly reduced germination and growth of an interspecificcompetitor in a bioassay.Takentogether, this demonstrates that the

release from natural enemies (created by insecticides) caused rapidevolution of increased competitive ability in goldenrod, and itstrongly suggests thatthe underlying mechanismmightbe selectionfor increased production of polyacetylene, an allelochemicalsuppressing interspecific competitors.

One intriguing aspect of the study of Uesugi & Kessler is that itelegantly links, and in fact, unifies two of the most popularhypotheses attempting to explaining plant invasiveness, the EICAhypothesis and the novel weapons hypothesis (Callaway &Ridenour, 2004), which proposes that some highly invasive plantsmay be dominant because they possess novel allelochemicals towhich their new neighbours have not previously been exposed, andwhich therefore have particularly strong negative effects on these

natives.

Fig.1 Solidago altissima is common in old fields in eastern North Americawhere it experiences strong intraspecific and interspecific competition.(Image courtesy of Andre Kessler.)

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Callaway & Ridenour (2004) already pointed out the possiblelink between novel weapons and EICA. They hypothesized that ifallelopathy indeed confers a substantial fitness advantage, it mightevolve rapidly after enemy release and could therefore, in somecases, be the key mechanism underlying EICA. However, at thetime no empirical evidence existed for such an evolutionarychange, and the EICA and Novel weapons hypothesis have largelybeen studied independently since then. Still, a link betweenenemy release, EICA and novel weapons is very likely, because

both enemy release and novel weapons are expected to be stronglyinfluenced by the phylogenetic distinctness of plant invaders(Fig. 2).

Introduced plants that are phylogenetically distinct from theirrecipient communities are not only more likely to possess novelallelochemicals but also a chemical defence novel to the herbivoresin the introduced range. As a consequence, phylogeneticallydistinct invaders experience greater enemy release (Cappuccino &Carpenter, 2005; Hill & Kotanen, 2009; Ness et al., 2011), andthey should thus not only possess novel weapons but also the meansfor their rapid evolutionary increase. Because of this doubleadvantage we should expect evolutionof increased allelopathy to be

common in phylogenetically distinct invaders, and it may wellcontribute to the frequently observed associations between phylo-genetic novelty, chemical novelty and plant invasion success(Cappuccino & Arnason, 2006; Strauss et al., 2006).

However, the study of Uesugi & Kessler has not been done ininvasive populations, but in a native population of goldenrod, andit is now important to test whether evolution of increasedallelopathy indeed also occurred in response to natural enemyrelease. Of course the interpretation of Uesugi & Kesslers resultsrests on the assumption of a trade-off between allocation to defencevs allelopathy,and their study didnot provide anyformal proof thatsuch a trade-off exists. Providing these missing pieces of evidence

will be crucial next steps towards understanding goldenrodinvasion. Another important direction for future research shouldbe to test for increased allelopathy of invasive populations acrossmultiple invasive species, connect these data to phylogeneticdistance, enemy release and invasion success, and thereby test thegenerality of Uesugi & Kesslers findings.

Even though evolution experiments are the gold standard fortesting eco-evolutionary hypotheses, and their usefulness forecologists has long been recognized (Conner, 2003), evolution

experiments in the field are still quite rare (Kawecki et al., 2012).The study of Uesugi & Kessler, together with other recent studies(Agrawal et al., 2012), clearly demonstrate the power of theexperimental evolution approach. It also shows the strength ofcombining multiple approaches, in their case a long-term selectionexperiment in the field with common garden studies, bioassays andchemical analyses. Ultimately, it is such combinations of well-designed ecological and evolutionary experiments with thoroughanalyses of the underlying functional mechanisms combiningrealism with precision, why? and how? questions that mostadvance our understanding of ecological systems.

Oliver Bossdorf

Institute of Plant Sciences, University of Bern, Altenbergrain 21,CH-3013, Bern, Switzerland

(tel +41 31 631 4926; email bossdorf@ips.unibe.ch)

References

Agrawal AA, Hastings AP, Johnson MTJ, Maron JL, Salminen JP. 2012. Insect

herbivores drive real-time ecological and evolutionary change in plant

populations. Science338: 113116.Blossey B, Notzold R. 1995. Evolution of increased competitive ability in invasive

nonindigenous plants: a hypothesis. Journal of Ecology83: 887889.

Enemy release

Possession of

novel weapons

In

creaseddominance

andinvasiveness

Phylogenetic

distance

Evolution of resourcecompetitive abbility

Evolution of

allelopathic potential

EICA hypothesis

Fig.2 Relationships between different hypotheses attempting to explain the increased dominance and invasiveness of plants in their introduced range.

2013 The Author

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Bossdorf O, Auge H, LafumaL, RogersW, Siemann E, Prati D. 2005. Phenotypic

and genetic differentiation between native and introduced plant populations.

Oecologia144: 111.Callaway RM, Ridenour WM. 2004. Novel weapons: invasive success and the

evolution of increased competitive ability. Frontiers in Ecology and theEnvironment2: 436443.

Cappuccino N, Arnason JT.2006. Novel chemistryof invasiveexotic plants. BiologyLetters2: 189193.

Cappuccino N, CarpenterD. 2005.Invasive exotic plants suffer less herbivory thannon-invasive exotic plants. Biology Letters1: 435438.

ColauttiRI, MaronJL, BarrettSCH. 2009.Common garden comparisons of native

and introduced plant populations: latitudinal clines can obscure evolutionary

inferences. Evolutionary Applications2: 187199.Conner JK. 2003. Artificial selection: a powerful tool for ecologists. Ecology84:

16501660.

Hill SB, Kotanen PM.2009. Evidence that phylogenetically novel non-indigenous

plants experience less herbivory. Oecologia161: 581590.

Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC. 2012.

Experimental evolution. Trends in Ecology & Evolution27: 547560.Ness JH, Rollinson EJ, Whitney KD. 2011. Phylogenetic distance can predict

susceptibility to attack by natural enemies. Oikos120: 13271334.Prentis PJ, Wilson JRU,Dormontt EE,Richardson DM,Lowe AJ. 2008.Adaptive

evolution in invasive species. Trends in Plant Science13: 288294.Schoener TW. 2011. The newest synthesis: understanding the interplay of

evolutionary and ecological dynamics. Science331: 426429.

Strauss SY, Webb CO, Salamin N. 2006. Exotic taxa less related to native speciesare more invasive. Proceedings of the National Academy of Sciences, USA103:58415845.

Uesugi A, Kessler A. 2013. Herbivore-exclusion drives the evolution of plant

competitiveness via increased allelopathy. New Phytologist198: 916924.

Key words: biological invasions, competitive ability, herbivory, natural selection,

rapid evolution.

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