THE EVOLUTION OF CARBON ALLOCATION TO PLANT SECONDARY METABOLITES: A GENETIC ANALYSIS OF COST IN<i>DIPLACUS AURANTIACUS</i>

Han, Kaiping; Lincoln, David E.

doi:10.1111/j.1558-5646.1994.tb02195.x

Cited by 54 publications

(38 citation statements)

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“…For example, potential seed production is negatively correlated with furanocoumarin concentrations in Pastinaca sativa (Berenbaum et al 1986;Zangerl and Berenbaum 1997). Plant growth rate is negatively correlated with the production of leaf phenolic resin in Diplacus aurantiacus (Han and Lincoln 1994) and with plant chemicals that confer resistance to Fusarium oxysporium in Raphanus sativus L. cultivars (Hoffland et al 1996). The second type are ecological costs (Simms 1992), which are due to negative genetic correlations between the levels of defense against different organisms, the levels of defense against a single organism expressed in different environments, or different components of defense such as resistance and tolerance.…”

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Fitness Costs of Chemical Defense in Plantago Lanceolata L.: Effects of Nutrient and Competition Stress

2003

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Abstract. Fitness costs of defense are often invoked to explain the maintenance of genetic variation in levels of chemical defense compounds in natural plant populations. We investigated fitness costs of iridoid glycosides (IGs), terpenoid compounds that strongly deter generalist insect herbivores, in ribwort plantain (Plantago lanceolata L.) using lines that had been artificially selected for high and low leaf IG concentrations for four generations. Twelve maternal half-sib families from each selection line were grown in four environments, consisting of two nutrient and two competition treatments. We tested whether: (1) in the absence of herbivores and pathogens, plants from lines selected for high IG levels have a lower fitness than plants selected for low IG levels; and (2) costs of chemical defense increase with environmental stress. Vegetative biomass did not differ between selection lines, but plants selected for high IG levels produced fewer inflorescences and had a significantly lower reproductive dry weight than plants selected for low IG levels, indicating a fitness cost of IG production. Line-by-nutrient and line-by-competition interactions were not significant for any of the fitness-related traits. Hence, there was no evidence that fitness costs increased with environmental stress. Two factors may have contributed to the absence of higher costs under environmental stress. First, IGs are carbon-based chemicals. Under nutrient limitation, the relative carbon excess may result in the production of IGs without imposing a further constraint on growth and reproduction. Second, correlated responses to selection on IG levels indicate the existence of a positive genetic association between IG level and cotyledon size. At low nutrient level, a path analysis based on family means revealed that in the presence of competitors, the negative direct effect of a high IG level on aboveground plant dry weight was partly offset by a positive direct effect of the associated larger cotyledon size. This indicates that fitness costs of defense may be modulated by environment-specific fitness effects of genetically associated traits.

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Fitness Costs of Chemical Defense in Plantago Lanceolata L.: Effects of Nutrient and Competition Stress

2003

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“…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.…”

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Tradeoffs associated with constitutive and induced plant resistance against herbivory

Kempel

Schädler

Chrobock

et al. 2011

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

217

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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“…Berenbaum et al (1986) found negative genetic correlations between levels of defensive compounds and estimators of individual fecundity. Han and Lincoln (1994) found a significant negative genetic correlation between growth rate and levels of secondary metabolites in Diplacus aurantiacus. Many studies, including our own, have measured fitness components in controlled environments, where environmental variation may be reduced, or gene expression may be altered by novel environments.…”

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confidence: 88%

“…Berenbaum et al (1986) showed a negative genetic correlation between insect resistance and fecundity in Pastinaca sativa. Han and Lincoln (1994) found a significant negative genetic correlation between growth rate and levels of secondary metabolites in Diplacus aurantiacus. In Escherichia coli, mutations causing resistance to virus T4 carry pleiotropic costs of resistance, which can be ameliorated by epistatic modifiers (Lenski 1988a,b).…”

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GENETICS OF BRASSICA RAPA. 3. COSTS OF DISEASE RESISTANCE TO THREE FUNGAL PATHOGENS

Mitchell‐Olds

Bradley

1996

Evolution

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Abstract.-Genetic costs of resistance to pathogens may be an important factor maintaining heritable variation for resistance in natural populations. Pleiotropic fitness trade-offs occur when genetic resistance causes reduction in other components of fitness. Although costs of resistance have an important influence on plant-pathogen interactions, few previous studies have detected pleiotropic costs of resistance in the absence of confounding effects of linkage disequilibrium. To avoid this potential problem, we performed artificial selection experiments on resistance to two fungal pathogens, Leptosphaeria maculans, and Peronospora parasitica, and compared growth rates of resistant and susceptible genotypes of Brassica rapa in the absence of pathogens. Leptosphaeria resistance had no effect on growth rate, indicating cost-free defense. In contrast, Peronospora-resistant genotypes grow 6% slower than Peronospora-susceptible genotypes in pathogen-free environments, indicating a significant genetic fitness cost to Peronospora resistance. Such genetic trade-offs could maintain genetic variation in the wild. Another factor that might explain heritable variation for resistance is ecological trade-offs, in which genetic resistance to one species causes susceptibility to another. Such ecological trade-offs do not exist for the pathogens studied in this system.

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THE EVOLUTION OF CARBON ALLOCATION TO PLANT SECONDARY METABOLITES: A GENETIC ANALYSIS OF COST INDIPLACUS AURANTIACUS

Cited by 54 publications

References 58 publications

Fitness Costs of Chemical Defense in Plantago Lanceolata L.: Effects of Nutrient and Competition Stress

Fitness Costs of Chemical Defense in Plantago Lanceolata L.: Effects of Nutrient and Competition Stress

Tradeoffs associated with constitutive and induced plant resistance against herbivory

GENETICS OF BRASSICA RAPA. 3. COSTS OF DISEASE RESISTANCE TO THREE FUNGAL PATHOGENS

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