Insect Herbivores Drive Real-Time Ecological and Evolutionary Change in Plant Populations

Agrawal, Anurag A.; Hastings, Amy P.; Johnson, Marc T. J.; Maron, John L.; Salminen, Juha‐Pekka

doi:10.1126/science.1225977

Cited by 420 publications

(475 citation statements)

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“…Recent studies have shown that the heterogeneous distribution of herbivores can shape plant defensive chemistry above ground [7][8][9]. Moreover, it was found that heterogeneity in herbivore communities maintains intraspecific variation in defence genes [10].…”

Section: Discussionmentioning

confidence: 99%

“…Insect herbivores, the most abundant and diverse plant consumers, have long been suspected to play an important role in this context [6]. Recent studies demonstrate that herbivore abundance can covary with the expression of plant defence metabolites [7], that the exclusion of phytophagous insects can lead to a relaxation of defences within a few generations [8] and that defence genes are under differential selection across environments [9,10]. Together, these studies show that the temporal and spatial variation in above-ground herbivore communities can shape plant defensive chemistry.…”

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confidence: 99%

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A below-ground herbivore shapes root defensive chemistry in natural plant populations

et al. 2016

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Plants display extensive intraspecific variation in secondary metabolites. However, the selective forces shaping this diversity remain often unknown, especially below ground. Using Taraxacum officinale and its major native insect root herbivore Melolontha melolontha, we tested whether below-ground herbivores drive intraspecific variation in root secondary metabolites. We found that high M. melolontha infestation levels over recent decades are associated with high concentrations of major root latex secondary metabolites across 21 central European T. officinale field populations. By cultivating offspring of these populations, we show that both heritable variation and phenotypic plasticity contribute to the observed differences. Furthermore, we demonstrate that the production of the sesquiterpene lactone taraxinic acid b-D-glucopyranosyl ester (TA-G) is costly in the absence, but beneficial in the presence of M. melolontha, resulting in divergent selection of TA-G. Our results highlight the role of soil-dwelling insects for the evolution of plant defences in nature. BackgroundHeritable intraspecific variation is a common feature of many biological traits. Genetic variation results from heterogeneous selection pressures in relation to genetic architecture, population substructures and gene flow [1 -4]. In plants, local differences in both abiotic and biotic factors may drive trait evolution [5]. Insect herbivores, the most abundant and diverse plant consumers, have long been suspected to play an important role in this context [6]. Recent studies demonstrate that herbivore abundance can covary with the expression of plant defence metabolites [7], that the exclusion of phytophagous insects can lead to a relaxation of defences within a few generations [8] and that defence genes are under differential selection across environments [9,10]. Together, these studies show that the temporal and spatial variation in above-ground herbivore communities can shape plant defensive chemistry.In contrast with the ecological and evolutionary dynamics of above-ground plant-herbivore interactions, below-ground interactions have received little attention, despite the importance of roots for plant fitness and the high concentrations of secondary metabolites in below-ground organs [11][12][13][14]. The rhizosphere differs from the phyllosphere in both biotic and abiotic conditions [15], and the selective forces shaping variation in secondary metabolites may therefore differ between the two environments. The evolution of root secondary metabolites may for instance be driven by herbivores [11,12,16], pathogens [17] and symbionts [18], as well as nutrient availability [19], salt, drought and cold stress [20]. By comparing one mainland and two island populations, Watts et al. [21] showed that geographical isolation, including the escape from pocket gophers (Geomyidae), resulted in the evolutionary decline of root alkaloid concentrations of the host plant Eschscholzia californica (Papaveraceae). The specific potential of root herbivores to shap...

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Section: Discussionmentioning

confidence: 99%

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A below-ground herbivore shapes root defensive chemistry in natural plant populations

et al. 2016

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“…In the first example, Agrawal et al [75] used insecticides to manipulate densities of arthropods feeding on genetically diverse experimental field populations of evening primrose (Oenothera biennis). They then followed the evolutionary dynamics of these populations for four generations.…”

Section: Species Interactions and Evolutionmentioning

confidence: 99%

Evolution caused by extreme events

Grant

Huey

et al. 2017

Phil. Trans. R. Soc. B

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195

172

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One contribution of 14 to a theme issue 'Behavioural, ecological and evolutionary responses to extreme climatic events'. Extreme events can be a major driver of evolutionary change over geological and contemporary timescales. Outstanding examples are evolutionary diversification following mass extinctions caused by extreme volcanism or asteroid impact. The evolution of organisms in contemporary time is typically viewed as a gradual and incremental process that results from genetic change, environmental perturbation or both. However, contemporary environments occasionally experience strong perturbations such as heat waves, floods, hurricanes, droughts and pest outbreaks. These extreme events set up strong selection pressures on organisms, and are small-scale analogues of the dramatic changes documented in the fossil record. Because extreme events are rare, almost by definition, they are difficult to study. So far most attention has been given to their ecological rather than to their evolutionary consequences. We review several case studies of contemporary evolution in response to two types of extreme environmental perturbations, episodic ( pulse) or prolonged (press). Evolution is most likely to occur when extreme events alter community composition. We encourage investigators to be prepared for evolutionary change in response to rare events during long-term field studies.This article is part of the themed issue 'Behavioural, ecological and evolutionary responses to extreme climatic events'.

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“…This important diversification suggests that particular metabolic systems have been recruited through natural selection when the set of compounds that they produce address specific ecological needs. Interactions with insects are important selection pressures that have sculpted plant metabolism, and many plant metabolites protect against herbivore attack and physical damage (3)(4)(5). The timely production of particular secondary metabolites in response to insect attack benefits plants by decreasing the costs of constitutive metabolite production.…”

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confidence: 99%

Navigating natural variation in herbivory-induced secondary metabolism in coyote tobacco populations using MS/MS structural analysis

Baldwin

Gaquerel

2015

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

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Natural variation can be extremely useful in unraveling the determinants of phenotypic trait evolution but has rarely been analyzed with unbiased metabolic profiling to understand how its effects are organized at the level of biochemical pathways. Native populations of Nicotiana attenuata, a wild tobacco species, have been shown to be highly genetically diverse for traits important for their interactions with insects. To resolve the chemodiversity existing in these populations, we developed a metabolomics and computational pipeline to annotate leaf metabolic responses to Manduca sexta herbivory. We selected seeds from 43 accessions of different populations from the southwestern United Statesincluding the well-characterized Utah 30th generation inbred accession-and grew 183 plants in the glasshouse for standardized herbivory elicitation. Metabolic profiles were generated from elicited leaves of each plant using a high-throughput ultra HPLC (UHPLC)-quadrupole TOFMS (qTOFMS) method, processed to systematically infer covariation patterns among biochemically related metabolites, as well as unknown ones, and finally assembled to map natural variation. Navigating this map revealed metabolic branch-specific variations that surprisingly only partly overlapped with jasmonate accumulation polymorphisms and deviated from canonical jasmonate signaling. Fragmentation analysis via indiscriminant tandem mass spectrometry (idMS/MS) was conducted with 10 accessions that spanned a large proportion of the variance found in the complete accession dataset, and compound spectra were computationally assembled into spectral similarity networks. The biological information captured by this networking approach facilitates the mining of the mass spectral data of unknowns with high natural variation, as demonstrated by the annotation of a strongly herbivory-inducible phenolic derivative, and can guide pathway analysis.plant-insect interactions | metabolomics | mass spectrometry | natural variation E lucidating the structure of metabolites underlying complex traits and the factors that maintain their variation in natural populations are important challenges in plant ecological studies (1). Many studies have notably shown that stress-responsive pathways that produce secondary metabolites are sporadically found across different plant taxa with extensive diversification (2). This important diversification suggests that particular metabolic systems have been recruited through natural selection when the set of compounds that they produce address specific ecological needs. Interactions with insects are important selection pressures that have sculpted plant metabolism, and many plant metabolites protect against herbivore attack and physical damage (3-5). The timely production of particular secondary metabolites in response to insect attack benefits plants by decreasing the costs of constitutive metabolite production. Trade-offs between defense metabolite productions and the intrinsic growth-related functions of central metabolic pathways likely prov...

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Insect Herbivores Drive Real-Time Ecological and Evolutionary Change in Plant Populations

Cited by 420 publications

References 35 publications

A below-ground herbivore shapes root defensive chemistry in natural plant populations

A below-ground herbivore shapes root defensive chemistry in natural plant populations

Evolution caused by extreme events

Navigating natural variation in herbivory-induced secondary metabolism in coyote tobacco populations using MS/MS structural analysis

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