Meta‐analysis of Trade‐offs among Plant Antiherbivore Defenses: Are Plants Jacks‐of‐All‐Trades, Masters of All?

Koricheva, Julia; Nykänen, Heli; Gianoli, Ernesto

doi:10.1086/382601

Cited by 268 publications

(272 citation statements)

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“…In this sense, many authors have reported the existence of evolutionary trade-offs among anti-herbivore resistance traits due to the costs of their production and/or redundant functions against herbivores (Rudgers et al, 2004;Wang et al, 2012). However, a convincing meta-analysis (Koricheva et al, 2004) proposed that plants may possess multiple defensive traits without excessive metabolic costs in particular situations, especially when the costs associated with the possession of multiple defensive traits are outweighed by their benefits. For example, the combined expression of multiple defensive traits may work to reduce herbivory and improve plant resistance to a large number of natural enemies more effectively than defensive traits that target individual herbivore species.…”

Section: Resultsmentioning

confidence: 99%

“…Assuming that the production of plant defences is costly in terms of growth and fitness, current theories on the evolution of plant resistance predict the existence of evolutionary trade-offs (negative genetic correlations) between resistance and fitness traits (Messina et al, 2002;Donaldson et al, 2006;Sampedro et al, 2011a), and between different resistance traits (reviewed by Koricheva et al (2004)). The existence of these trade-offs may severely constrain the invasion success of plant populations in non-indigenous habitats, as trade-offs limit the simultaneous change of negatively correlated traits (Orians and Ward, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Additive genetic variation in resistance traits of an exotic pine species: little evidence for constraints on evolution of resistance against native herbivores

2012

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The apparent failure of invasions by alien pines in Europe has been explained by the co-occurrence of native pine congeners supporting herbivores that might easily recognize the new plants as hosts. Previous studies have reported that exotic pines show reduced tolerance and capacity to induce resistance to those native herbivores. We hypothesize that limited genetic variation in resistance to native herbivores and the existence of evolutionary trade-offs between growth and resistance could represent additional potential constraints on the evolution of invasiveness of exotic pines outside their natural range. In this paper, we examined genetic variation for constitutive and induced chemical defences (measured as non-volatile resin in the stem and total phenolics in the needles) and resistance to two major native generalist herbivores of pines in cafeteria bioassays (the phloem-feeder Hylobius abietis and the defoliator Thaumetopoea pityocampa) using half-sib families drawn from a sample of the population of Pinus radiata introduced to Spain in the mid-19th century. We found (i) significant genetic variation, with moderate-to-high narrow-sense heritabilities for both the production of constitutive non-volatile resin and induced total phenolics, and for constitutive resistance against T. pityocampa in bioassays, (ii) no evolutionary trade-offs between plant resistance and growth traits or between the production of different quantitative chemical defences and (iii) a positive genetic correlation between constitutive resistance to the two studied herbivores. Overall, results of our study indicate that the exotic pine P. radiata has limited genetic constraints on the evolution of resistance against herbivores in its introduced range, suggesting that, at least in terms of interactions with these enemies, this pine species has potential to become invasive in the future. (2010)). For instance, the enemy release hypothesis predicts that exotic plants spread rapidly because they escape from their co-evolved natural enemies in the new range (Elton, 1958;Maron and Vilà, 2001). Accordingly, the evolution of increased competitive ability (EICA) hypothesis states that exotic plant species, with few specialized enemies in their new range, are more competitive than native species because they preferentially allocate resources to growth or reproduction instead of defences (Blossey and Nötzold, 1995). Although both hypotheses have been examined in a diverse array of terrestrial (Bossdorf et al.,

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Additive genetic variation in resistance traits of an exotic pine species: little evidence for constraints on evolution of resistance against native herbivores

2012

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“…Alternatively, a pattern of old defenses being replaced by new ones suggests that energetic cost or other tradeoffs constrain the macroevolution of defense (46). However, this explanation has been questioned because physiological tradeoffs between different kinds of defenses seem not to be general (29,47). Ecological costs, such as deterring pollinators, have also been described (48,49).…”

Section: Evolution Of Defensesmentioning

confidence: 99%

Macroevolution and the biological diversity of plants and herbivores

Futuyma

Agrawal

2009

Proc. Natl. Acad. Sci. U.S.A.

534

467

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Terrestrial biodiversity is dominated by plants and the herbivores that consume them, and they are one of the major conduits of energy flow up to higher trophic levels. Here, we address the processes that have generated the spectacular diversity of flowering plants (>300,000 species) and insect herbivores (likely >1 million species). Long-standing macroevolutionary hypotheses have postulated that reciprocal evolution of adaptations and subsequent bursts of speciation have given rise to much of this biodiversity. We critically evaluate various predictions based on this coevolutionary theory. Phylogenetic reconstruction of ancestral states has revealed evidence for escalation in the potency or variety of plant lineages' chemical defenses; however, escalation of defense has been moderated by tradeoffs and alternative strategies (e.g., tolerance or defense by biotic agents). There is still surprisingly scant evidence that novel defense traits reduce herbivory and that such evolutionary novelty spurs diversification. Consistent with the coevolutionary hypothesis, there is some evidence that diversification of herbivores has lagged behind, but has nevertheless been temporally correlated with that of their host-plant clades, indicating colonization and radiation of insects on diversifying plants. However, there is still limited support for the role of host-plant shifts in insect diversification. Finally, a frontier area of research, and a general conclusion of our review, is that community ecology and the long-term evolutionary history of plant and insect diversification are inexorably intertwined.coevolution ͉ herbivory ͉ insect host range ͉ phylogenetic analyses ͉ plant defense theory

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“…This indicates that being well defended may not always be the best strategy-most likely because allocation to resistance may physiologically constrain other investments (reviewed in refs. 4 and 5) and because constraints on resource allocation may produce negative genetic correlations between resistance mechanisms and other life-history traits (6)(7)(8). The current assumption in evolutionary ecology is that such tradeoffs contribute to the generation and maintenance of species diversity (8).…”

mentioning

confidence: 99%

Tradeoffs associated with constitutive and induced plant resistance against herbivory

Kempel

Schädler

Chrobock

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

218

193

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Several prominent hypotheses have been posed to explain the immense variability among plant species in defense against herbivores. A major concept in the evolutionary ecology of plant defenses is that tradeoffs of defense strategies are likely to generate and maintain species diversity. In particular, tradeoffs between constitutive and induced resistance and tradeoffs relating these strategies to growth and competitive ability have been predicted. We performed three independent experiments on 58 plant species from 15 different plant families to address these hypotheses in a phylogenetic framework. Because evolutionary tradeoffs may be altered by human-imposed artificial selection, we used 18 wild plant species and 40 cultivated garden-plant species. Across all 58 plant species, we demonstrate a tradeoff between constitutive and induced resistance, which was robust to accounting for phylogenetic history of the species. Moreover, the tradeoff was driven by wild species and was not evident for cultivated species. In addition, we demonstrate that more competitive species-but not fast growing ones-had lower constitutive but higher induced resistance. Thus, our multispecies experiments indicate that the competition-defense tradeoff holds for constitutive resistance and is complemented by a positive relationship of competitive ability with induced resistance. We conclude that the studied genetically determined tradeoffs are indeed likely to play an important role in shaping the high diversity observed among plant species in resistance against herbivores and in life history traits.comparative experimental study | phylogenetic corrections | plant defense theory | plant-insect interaction | Spodoptera littoralis G iven that green plants are the ultimate source of energy for most other organisms, it is not surprising that plants evolved a variety of resistance strategies, which can be constitutively expressed or induced after damage (1). Although herbivory selects for enhanced plant resistance, plants vary greatly in their resistance, both among species (2) and among genotypes within species (3). This indicates that being well defended may not always be the best strategy-most likely because allocation to resistance may physiologically constrain other investments (reviewed in refs. 4 and 5) and because constraints on resource allocation may produce negative genetic correlations between resistance mechanisms and other life-history traits (6-8). The current assumption in evolutionary ecology is that such tradeoffs contribute to the generation and maintenance of species diversity (8).Several hypotheses on tradeoffs associated with constitutive and induced resistance have been formulated. Among the most fundamental ones is the long-predicted tradeoff between constitutive and induced resistance itself (6, 9). This hypothesis is derived from the idea that resistance is costly and that a species already well defended by high constitutive resistance will benefit only negligibly by further induced resistance (1, 10). However, genera...

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Meta‐analysis of Trade‐offs among Plant Antiherbivore Defenses: Are Plants Jacks‐of‐All‐Trades, Masters of All?

Cited by 268 publications

References 73 publications

Additive genetic variation in resistance traits of an exotic pine species: little evidence for constraints on evolution of resistance against native herbivores

Additive genetic variation in resistance traits of an exotic pine species: little evidence for constraints on evolution of resistance against native herbivores

Macroevolution and the biological diversity of plants and herbivores

Tradeoffs associated with constitutive and induced plant resistance against herbivory

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