Evolution Of Plant Defense Research Articles

Plant size, latitude, and phylogeny explain within-population variability in herbivory.

Interactions between plants and herbivores are central in most ecosystems, but their strength is highly variable. The amount of variability within a system is thought to influence most aspects of plant-herbivore biology, from ecological stability to plant defense evolution. Our understanding of what influences variability, however, is limited by sparse data. We collected standardized surveys of herbivory for 503 plant species at 790 sites across 116° of latitude. With these data, we show that within-population variability in herbivory increases with latitude, decreases with plant size, and is phylogenetically structured. Differences in the magnitude of variability are thus central to how plant-herbivore biology varies across macroscale gradients. We argue that increased focus on interaction variability will advance understanding of patterns of life on Earth.

The Evolutionary Ecology of Plant Chemical Defenses: From Molecules to Communities

Classic theory relates herbivore pressure to the ecology and evolution of plant defenses. Here, we summarize current trends in the study of plant–herbivore interactions and how they shape the evolution of plant chemical defenses, host choice, and community composition and diversity. Inter- and intraspecific variation in defense investment is driven by resource availability. The evolution of defenses at deeper nodes of plant phylogeny is conserved, yet defenses are highly labile at the tips. On an ecological timescale, while greater specialization of tropical herbivores enhances local diversity by reducing the performance of plants with similar defenses, in temperate ecosystems with more generalist herbivores, rare defense profiles are at a disadvantage. On an evolutionary timescale, host choice by herbivores is largely determined by plant defenses rather than host phylogeny, leading to evolutionary tracking by herbivores rather than cocladogenesis. The interplay between plants and herbivores shapes both the origin and maintenance of diversity.

Using biological invasions to improve plant defense theory

AbstractTheory to explain how plants defend themselves against herbivorous insects is rich, but can be difficult to test. Biological invasions provide unique opportunities to test and improve upon plant defense theory, as plants experience predictable shifts in insect herbivory after introduction to a new range. Here, we use an invasion to evaluate the power of three cornerstone hypotheses to predict the evolution of defense against herbivorous insects. These three hypotheses represent increasing refinements of classic plant‐insect theory regarding optimal defense, and each rests on the same three assumptions: that introduced plant populations escape natural enemies, that insect herbivory reduces plant fitness, and that putative defenses decrease herbivory. These assumptions remain untested in most invasions, which likely contributes to conflicting support for many plant defense hypotheses. We provide evidence that these assumptions are met in common mullein, Verbascum thapsus L. (Scrophulariaceae), which we propose can thus be used as a model system to test plant defense theory. We find that the hypothesis that integrates predictions of within‐plant optimal defense theory and the evolutionary dilemma model (i.e., the ‘shifting defense allocation’ hypothesis) provides strong insights into both invasion and evolution of plant defense. Specifically, we show that introduced populations that escape important specialist herbivores increase the concentration of secondary compounds in high‐quality tissue in particular, in this case protecting valuable young leaves from generalist herbivores that dominate in the introduced range. We would not have detected this shift without exploring within‐plant defense allocation across native and introduced populations, a task rarely undertaken when assessing evolutionary change in plant defenses. This finding provides broad insight into how native and introduced plant populations alike may respond to shifts in herbivore pressure. We close by highlighting future directions of inquiry using introduced plant populations to develop and test plant defense theory more generally.

Hybridization and complex evolution of Barbarea vulgaris and related species (Brassicaceae)

Barbarea, winter-cress, is a genus of 29 species in Brassicaceae, the mustard family, which has emerged as a model for evolution of plant defence and specialised metabolites. Notably, some Barbarea species have evolved the ability to produce triterpenoid saponins as the only ones in Brassicaceae, some of which make plants resistant to important herbivores. Resistance has, however, been lost in a distinct group of plants within B. vulgaris ssp. arcuata, which is genetically strongly diverged from other B. vulgaris plants. This divergence is not reflected present in taxonomy. Thus, a phylogeny is needed to understand evolution and defence in Barbarea. Here, we analysed the nuclear ITS and the plastid matK, ndhF, rps16, and psbA-trnH DNA regions from seven out of 29 Barbarea species, 57 accessions of B. vulgaris, 10 accessions of other Barbarea species, and eight outgroup species, in addition to sequences available from GenBank. All Barbarea species formed a highly supported monophyletic group, separated from sister genera. Several clades seem to have radiated within the genus with no simple branching pattern, and discordant nuclear and plastid DNA phylogenies indicate reticulate evolution and chloroplast capture. One of the complex patterns may have resulted from chloroplast capture of a non-Nordic Barbarea species not included in the study. Two pairs of species were almost identical, B. australis and B. grayi, and B. orthoceras and B. stricta. Despite hybridization, chloroplast capture, and incongruence among the plastid and nuclear DNA data, the high level of intraspecific diversity, coupled with lineage specificity, lead us to recognize three groups of Barbarea vulgaris: G-type (glabrous) and P-type (pubescent) individuals of the current B. vulgaris ssp. arcuata as two distinct groups and the current B. vulgaris ssp. vulgaris as the third. Despite the high molecular diversity below species level, the evolutionary history of the saponin-based resistance remains unsettled due to unresolved basal branching.

Geographic variation and temporal changes in plant–herbivore interaction: Case studies with Solidago altissima in native and introduced ranges

AbstractPlants are subjected to environmental gradients and may encounter various herbivores, leading to geographic variation in defensive traits. The present review highlights that biological invasions are remarkable natural experiments for studying geographic variation in plant–herbivore interaction and tracking temporal dynamics in plant defense in response to environmental changes. Studies from this viewpoint can challenge various general topics in plant ecology, including the evolution of plant defense and indirect interactions among plants. First, I provide a brief overview on how the introduction of exotic herbivores drives rapid evolution after the establishment of exotic plants and its impacts on native plants. Second, I present a series of case studies investigating the patterns and mechanisms of geographic variation in the interaction between Solidago altissima and Corythucha marmorata (lace bug) in the native range in the United States and the introduced range in Japan. By combining biogeographical and experimental approaches, my collaborators and I unraveled the temporal dynamics of S. altissima's resistance to lace bugs and explored the drivers of differentiation in resistance between native and introduced ranges. These studies provide new insight into the geographic variation in exotic plant–herbivore interaction by unraveling the mechanisms and the temporal scale that cause the variation. These findings are vital not only for predicting invasiveness of exotic plants but also for understanding the evolution of plant–herbivore interaction in community contexts and under climate change.

Herbivore-induced defenses are not under phylogenetic constraints in the genus Quercus (oak): Phylogenetic patterns of growth, defense, and storage.

The evolution of plant defenses is often constrained by phylogeny. Many of the differences between competing plant defense theories hinge upon the differences in the location of meristem damage (apical versus auxiliary) and the amount of tissue removed. We analyzed the growth and defense responses of 12 Quercus (oak) species from a well‐resolved molecular phylogeny using phylogenetically independent contrasts. Access to light is paramount for forest‐dwelling tree species, such as many members of the genus Quercus. We therefore predicted a greater investment in defense when apical meristem tissue was removed. We also predicted a greater investment in defense when large amounts of tissue were removed and a greater investment in growth when less tissues were removed. We conducted five simulated herbivory treatments including a control with no damage and alterations of the location of meristem damage (apical versus auxiliary shoots) and intensity (25% versus 75% tissue removal). We measured growth, defense, and nutrient re‐allocation traits in response to simulated herbivory. Phylomorphospace models were used to demonstrate the phylogenetic nature of trade‐offs between characteristics of growth, chemical defenses, and nutrient re‐allocation. We found that growth–defense trade‐offs in control treatments were under phylogenetic constraints, but phylogenetic constraints and growth–defense trade‐offs were not common in the simulated herbivory treatments. Growth–defense constraints exist within the Quercus genus, although there are adaptations to herbivory that vary among species.

Features of conspecific and heterospecific interactions of greenhouse whitefly Trialeurodes vaporariorum and spider mite Tetranychus urticae on cucumber

Рlant-mediated interactions between greenhouse whitefly Trialeurodes vaporariorum and spider mite Tetranychus urticae have been studied under laboratory experiments on cucumber. The seedlings have been infested using different herbivores densities, when the first true leaf was fully unfolded The response of pests to previously damaged plants has been studied. Whitefly and spider mite plant selection in free-choice bioassay, as well as the larvae number of the whitefly daughter generation and the daily spider mite fecundity have been evaluated in the experiment. We have found, that the antixenotic and antibiotic cucumber properties in regard to the herbivorous arthropods, as a result of herbivore-induced plant defense development, depend on herbivore species and intensity of arthropod damage to plants. Damage to plants by whitefly has affected the behavior and development of a conspecific individuals only. Damage to plants by spider mites has affected both whitefly and spider mite individuals. Analysis of literature on this issue and the results of our research show a specificity of plant responses to arthropod damage, that can be determined by the specific features of herbivorous species and depend on the nature and intensity of the plant damage.

The evolution of pyrrolizidine alkaloid diversity among and withinJacobaeaspecies

Plants produce many secondary metabolites showing considerable inter- and intraspecific diversity of concentration and composition as a strategy to cope with environmental stresses. The evolution of plant defenses against herbivores and pathogens can be unraveled by understanding the mechanisms underlying chemical diversity. Pyrrolizidine alkaloids are a class of secondary metabolites with high diversity. We performed a qualitative and quantitative analysis of 80 pyrrolizidine alkaloids with liquid chromatography-tandem mass spectrometry of leaves from 17 Jacobaea species including one to three populations per species with 4–10 individuals per population grown under controlled conditions in a climate chamber. We observed large inter- and intraspecific variation in pyrrolizidine alkaloid concentration and composition, which were both species-specific. Furthermore, we sequenced 11 plastid and three nuclear regions to reconstruct the phylogeny of the 17 Jacobaea species. Ancestral state reconstruction at the species level showed mainly random distributions of individual pyrrolizidine alkaloids. We found little evidence for phylogenetic signals, as nine out of 80 pyrrolizidine alkaloids showed a significant phylogenetic signal for Pagel's λ statistics only, whereas no significance was detected for Blomberg's K measure. We speculate that this high pyrrolizidine alkaloid diversity is the result of the upregulation and downregulation of specific pyrrolizidine alkaloids depending on ecological needs rather than gains and losses of particular pyrrolizidine alkaloid biosynthesis genes during evolution.

Ontogenetic changes in the targets of natural selection in three plant defenses.

The evolution of plant defenses has traditionally been studied at single plant ontogenetic stages, overlooking the fact that natural selection acts continuously on organisms along their development, and that the adaptive value of phenotypes can change along ontogeny. We exposed 20 replicated genotypes of Turnera velutina to field conditions to evaluate whether the targets of natural selection on different defenses and their adaptative value change across plant development. We found that low chemical defense was favored in seedlings, which seems to be explained by the assimilation efficiency and the ability of the specialist herbivore to sequester cyanogenic glycosides. Whereas trichome density was unfavored in juvenile plants, it increased relative plant fitness in reproductive plants. At this stage we also found a positive correlative gradient between cyanogenic potential and sugar content in extrafloral nectar. We visualize this complex multi-trait combination as an ontogenetic defensive strategy. The inclusion of whole-plant ontogeny as a key source of variation in plant defense revealed that the targets and intensity of selection change along the development of plants, indicating that the influence of natural selection cannot be inferred without the assessment of ontogenetic strategies in the expression of multiple defenses.

The cytochrome P450 CYP72A552 is key to production of hederagenin-based saponins that mediate plant defense against herbivores.

Plants continuously evolve new defense compounds. One class of such compounds is triterpenoid saponins. A few species in the Barbarea genus produce saponins as the only ones in the large crucifer family. However, the molecular mechanism behind saponin biosynthesis and their role in plant defense remains unclear. We used pathway reconstitution in planta, enzymatic production of saponins invitro, insect feeding assays, and bioinformatics to identify a missing gene involved in saponin biosynthesis and saponin-based herbivore defense. A tandem repeat of eight CYP72A cytochromes P450 colocalise with a quantitative trait locus (QTL) for saponin accumulation and flea beetle resistance in Barbarea vulgaris. We found that CYP72A552 oxidises oleanolic acid at position C-23 to hederagenin. In vitro-produced hederagenin monoglucosides reduced larval feeding by up to 90% and caused 75% larval mortality of the major crucifer pest diamondback moth and the tobacco hornworm. Sequence analysis indicated that CYP72A552 evolved through gene duplication and has been under strong selection pressure. In conclusion, CYP72A552 has evolved to catalyse the formation of hederagenin-based saponins that mediate plant defense against herbivores. Our study highlights the evolution of chemical novelties by gene duplication and selection for enzyme innovations, and the importance of chemical modification in plant defense evolution.

Testing for latitudinal gradients in defense at the macroevolutionary scale.

Plant defenses against herbivores are predicted to evolve to be greater in warmer climates, such as lower latitudes where herbivore pressure is also thought to be higher. Instead, recent findings are often inconsistent with this expectation, suggesting alternative hypotheses are needed. We tested for latitudinal gradients in plant defense evolution at the macroevolutionary scale by characterizing plant chemical defenses across 80 species of the evening primroses, spanning both North and South America. We quantified phenolics in leaves, flowers, and fruits, using advanced analytical chemistry techniques. Dominant individual ellagitannin compounds, total concentrations of ellagitannins, flavonoids, total phenolics, and compound diversity were quantified. Variation in these compounds was predicted with latitude, temperature, precipitation, and continent using phylogenetic generalized least squares (PGLS) multiple regression models. Latitude did not strongly explain variation in chemical defenses. Instead, fruit total ellagitannins, oenothein A, and total phenolics were greater in species inhabiting regions with colder climates. Using analytical chemistry and 80 species in two continents, we show that contrary to classic predictions, concentrations of secondary metabolites are not greater at lower latitudes or in warmer regions. We propose higher herbivore pressure in colder climates and gradients in resource availability as potential drivers of the observed patterns in Oenothera.

Invasive Spartina alterniflora exhibits increased resistance but decreased tolerance to a generalist insect in China

Several theories explaining the post-introduction evolution of invasive plants predict that specialist-enemy release often leads to decreased defense in introduced plants, but how novel generalist consumers in the introduced ranges affect plant-defense evolution remains largely unexplored. According to the shifting defense hypothesis, the decreased defense against specialist enemies may result in the increased defense against generalists. We compared resistance and tolerance of native (from the USA) and invasive populations (from China) of Spartina alterniflora to the dominant generalist insect Laelia coenosa in China. We also compared leaf traits between Spartina population origins. We found that Laelia had lower performance on invasive than on native Spartina populations. Native Spartina populations, however, had a greater capacity to compensate for leaf damage by Laelia than invasive ones. Although specific leaf area and leaf carbon content did not significantly vary between Spartina origins, invasive Spartina populations had lower leaf-nitrogen content than native populations. These results suggest that, following its introduction to China, Spartina has developed increased resistance but decreased tolerance to the generalist herbivore, which may be related to evolutionary increases in leaf carbon-to-nitrogen ratio. These findings enhance our understanding of invasive plant defense against generalist herbivores in the introduced ranges and highlight the trade-off between resistance and tolerance.

Order of herbivore arrival on wild cabbage populations influences subsequent arthropod community development

In plant–arthropod associations, the first herbivores to colonise a plant may directly or indirectly affect community assembly on that particular plant. Whether the order of arrival of different arthropod species further modulates community assembly and affects plant fitness remains unclear.Using wild Brassica oleracea plants in the field, we manipulated the order of arrival of early‐season herbivores that belong to different feeding guilds, namely the aphid Brevicoryne brassicae and caterpillars of Plutella xylostella. We investigated the effect of herbivore identity and order of arrival on community assembly on two B. oleracea plant populations during two growth seasons. For this perennial plant, we evaluated whether foliar herbivory also affected herbivore communities on the flowers and if these interactions affected plant seed production.Aphid infestation caused an increase in parasitoid abundance, but caterpillars modulated these effects, depending on the order of herbivore infestation and plant population. In the second growth season, when plants flowered, the order of infestation of leaves with aphids and caterpillars more strongly affected abundance of herbivores feeding on the flowers than those feeding on leaves. Infestation with caterpillars followed by aphids caused an increase in flower‐feeding herbivores compared to the reversed order of infestation in one plant population, whereas the opposite effects were observed for the other plant population. The impact on plant seed set in the first reproductive year was limited.Our work shows that the identity and arrival order of early season herbivores may have long‐term consequences for community composition on individual plants and that these patterns may vary among plant populations. We discuss how these community processes may affect plant fitness and speculate on the implications for evolution of plant defences.

Plant Defenses against Herbivory: Closing the Fitness Gap.

Many morphological and chemical features of plants are classified as plant defenses against herbivores. By definition, plant defenses should increase a plant's fitness (i.e., its contribution to the gene pool of the next generation) as a function of herbivory. Over the past years, substantial progress has been made in understanding and manipulating the mechanistic basis of many putative plant defense traits. However, most plant defenses are still characterized by proximate variables such as herbivore performance or plant damage rather than actual fitness. Determining fitness benefits as a function of herbivory therefore remains a major knowledge gap that must be filled to understand the ecology and evolution of plant defenses.

A whole-plant perspective reveals unexpected impacts of above- and belowground herbivores on plant growth and defense.

Trade-offs between plant growth and defense are central to theoretical frameworks used to study the ecology and evolution of plant defense against herbivores. However, these frameworks, as well as the experiments designed to test them, rarely include belowground herbivores. We experimentally challenged seedlings of the tropical shrub Solanum lycocarpum (Solanaceae) with either aboveground foliar herbivores (Spodoptera caterpillars) or belowground root herbivores (the nematode Meloidogyne incognita) and measured the resulting changes in plant growth rates, biomass allocation, and the concentration of defensive terpenoids in roots and leaves. We found that plants that suffered aboveground herbivory responded with aboveground growth but belowground defense. Similarly, belowground herbivory resulted in root growth but elevated defenses of leaves. These results underscore the importance of belowground plant-herbivore interactions, and suggest that, in contrast to theoretical predictions, plants can simultaneously invest in both growth and defense. Finally, they emphasize the need for a "whole-plant" perspective in theoretical and empirical evaluations of plant-herbivore interactions.

Evolution of plant defences along an invasion chronosequence: defence is lost due to enemy release – but not forever

Summary The success of invasive plants has often been attributed to their rapid evolution at the introduced range. In particular, release from native enemies has been suggested to select for an evolutionary shift in resource allocation patterns from herbivore defence to increased size. Such evolutionary processes can take place not only between the native and invasive ranges but also within the invasive range over time, but this premise has been very seldom studied. In this study, we examined the potential for post‐invasion evolution in two traits hypothesized to facilitate plant invasion success, that is herbivore resistance and allelopathic ability. We studied these traits in the invasive plant Impatiens glandulifera by comparing plants from its native populations and from populations across its invasion chronosequence. Results of common‐garden experiment and chemical analyses revealed that plants from native populations or older populations within the invasive range show greater resistance to the generalist herbivore, Deilephila elpenor, coupled with greater production of the secondary defence compound 2‐methoxy‐1,4‐naphthoquinone glycoside. In contrast, no differences were found between populations in their allelopathic effect on the germination of the co‐occurring neighbour, Urtica doica. Finally, results from a field survey suggested that older populations within the invasive range incur greater attack rates from local herbivores compared to more recently established populations. Synthesis. Our findings support the idea that the selection pressure of enemy release at the introduced range might attenuate over time, leading to the evolutionary recovery of enemy resistance. This study emphasizes the importance of incorporating the effect of time since introduction when examining evolutionary or ecological processes of plant invasions.

Giant tortoises spread to western Indian Ocean islands by sea drift in pre-Holocene times, not by later human agency - response to Wilmé et al . (2016a)

Evidence from DNA phylogeny, Plio-Pleistocene ocean currents, giant tortoise dispersal, evolution of plant defences, radiocarbon dates and archaeology indicates that the endemic giant tortoises on the Mascarenes and Seychelles colonized naturally and were not translocated there by humans. Giant tortoises have fascinated Indian Ocean travellers since their first discovery on Mauritius by the Dutch in 1598 (Cheke & Bour, 2014), and a Reunion tortoise was among the earliest biological specimens to reach Europe from the Malagasy region (in 1671: Bour, 2004), but Wilme et al. (2016a) are the first to suggest that humans introduced them, their main arguments being that: Sea drift is too rare, uncertain and contrary to currents to account for the presence of tortoises on so many western Indian Ocean islands. The existing phylogeny, with dating considered uncertain, does not rule out rapid evolution in recent millenia as some tortoise mtDNA is known to mutate very rapidly. Hence, they imply that it is more likely that humans populated the Mascarene and Seychelles islands with tortoises. Specifically, they propose that Austronesian transoceanic colonists, with implied identity to settlers on Madagascar c. 4000 yr bp, distributed tortoises from Madagascar or Africa to Aldabra and the Mascarenes (Mauritius, Reunion, Rodrigues) as a food resource; the granitic Seychelles, oddly, are unmentioned. There are numerous reasons to reject this hypothesis. While Austronesians may have taken chickens and various crops from the Sunda Islands to East Africa and Madagascar (e.g. Boivin et al., 2013; but see Anderson et al., in press), there is no archaeological evidence that they discovered or visited the Mascarenes, granitic Seychelles or the Aldabra group atolls (Blench, 2010; Anderson et al., in press). In addition, the phylogeographical, ecological, evolutionary, palaeontological and archaeological evidence all strongly indicates the contrary. (Resume d'auteur)

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

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 β-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.

Keystone Herbivores and the Evolution of Plant Defenses.

Plants need to defend themselves against a diverse and dynamic herbivore community. Such communities may be shaped by keystone herbivores that through their feeding alter the plant phenotype as well as the likelihood of attack by other herbivores. Here, we discuss such herbivores that have a large effect on the interaction network structure with associated fitness consequences for the plant, as dominant agents of selection on plant defense traits. Merging the keystone herbivore concept with plant fitness and trait selection frameworks will provide an approach to identify which herbivores drive selection in complex multispecies interactions in natural and agricultural systems.

Evolutionary Interactions Between Plant Reproduction and Defense Against Herbivores

Coevolution is among the most important evolutionary processes that generate biological diversity. Plant–pollinator interactions play a prominent role in the evolution of reproductive traits in flowering plants. Likewise, plant–herbivore interactions select for myriad defenses that protect plants from damage. These mutualistic and antagonistic interactions, respectively, have traditionally been considered in isolation from one another. Here, we consider whether reproductive traits and antiherbivore defenses are interdependent as a result of pollinator- and herbivore-mediated selection. The evolution of floral traits, self-fertilization, and separate sexes frequently affects the expression and evolution of plant defenses. In turn, the evolution of defense can affect allocation to reproductive traits, and herbivores often impose strong selection directly on floral traits. Theory and empirical evidence suggest that herbivores can influence the evolution of selfing from outcrossing and potentially the evolution of separate sexes from combined sexes. We identify several areas in which future research is needed to increase our understanding of the evolutionary interplay between reproduction and defense in plants.