Generalist Herbivores Research Articles

Potential for biocontrol of Silybum marianum (variegated thistle): 2. Literature search and prioritisation of biocontrol agents

ABSTRACT Silybum marianum (L.) Gaertner (variegated thistle, milk thistle) is one of the worst weeds of hill country pasture in the east coast regions of New Zealand. A recent field survey in New Zealand found low levels of attack from generalist herbivores and minimal attack by the specialist weevil, Rhinocyllus conicus (Frölich). In the native range of Europe there are at least 41 insects and 12 fungi sufficiently specialised to be considered for biocontrol. The literature search revealed some potential biocontrol agents not known during the historical biocontrol surveys for S. marianum. These include the specialised biotypes of the tephritid fly, Terellia fuscicornis Loew, and the seedhead weevil, Larinus latus Herbst. The literature search also revealed the discovery of the stem-galling cynpid wasps, Aulacidea freesei Nieves-Aldrey and Phanacis zwoelferi Nieves-Aldrey, that are likely specific to S. marianum. The discovery of the smut fungus, Microbotryum silybum Vanky & Berner, host specific to Silybum species, is another promising biocontrol candidate. A shortlist of nine priority agents (eight insects and one fungal pathogen) were selected based on reported affinity for S. marianum, evidence for impact on the weed, and niches attacked. In the case of S. marianum, there are sufficiently specialised agents that attack several niches, including seeds, stems, and the root or root collar. Testing for complementary agents that attack different niches is likely to improve the chance of successful biocontrol. It is recommended that S. marianum be considered a priority target for classical biocontrol in New Zealand.

Diet specialization mediates drivers of Cucurbita herbivory in a semi-arid agroecosystem

Herbivory is a major fitness pressure for plants and a key driver of crop losses in agroecosystems. Dense monocultures are expected to favor specialist herbivorous insects, particularly those who primarily consume crop species; yet, levels and types of herbivory are not uniform within regional cropping systems. It is essential to determine which local and regional ecological factors drive variation in herbivory in order to support functional agroecosystems that rely less on chemical inputs. Crops in the genus Cucurbita host a suite of both generalist and specialist herbivores that inflict significant damage, yet little is known about the relative contribution of these herbivores to variation in herbivory and how local- and landscape-scale Cucurbita resource concentrations, management practices, and natural enemies mediate this relationship. In this study, we tested whether three foundational ecological hypotheses influenced Cucurbita herbivory across 20 pumpkin fields in the semi-arid Southern High Plains Region of Texas. We used generalized linear mixed models and confirmatory path analysis to assess whether the Density-dependent Herbivory Hypothesis, Resource Concentration Hypothesis, or the Natural Enemies Hypothesis, could explain variation in Cucurbita herbivory and insect dynamics in the context of conventional agronomic practices. We found that herbivory increased over time, indicating that herbivores were causing sustained damage throughout the growing season. We also found that fields with higher local Cucurbita resources had lower herbivory, suggesting a resource dilution effect. Natural enemy communities were more abundant and taxonomically rich in sites with greater generalist herbivore abundance, though predator abundance declined over time, indicating that late-season crop fields are most at risk given high herbivory and low natural enemy-based control. Our findings also suggest that while local resource availability may drive the abundance and richness of arthropod communities, additional agronomic and phenological information is needed to anticipate herbivory risk in an agriculturally dominated landscape.

SEQUESTRATION OF TROPANE ALKALOIDS FROM <i>Brugmansia suaveolens</i> (SOLANACEAE): NEW RECORDS FOR ORTHOPTERA AND COLEOPTERA

Tropane alkaloids (TAs) are the main secondary metabolites found in Datureae (Solanaceae). These compounds are neurotoxic to many organisms. However, some insect species can sequester and accumulate TAs in their bodies. Brugmansia suaveolens (Humb. and Bonpl. ex Willd.) Bercht. and J.Presl, a Neotropical shrub, is known to produce TAs. In this study, we report the sequestration of TAs from B. suaveolens by Chromacris speciosa (Thunberg, 1824) (Orthoptera: Rhomaleidae) and Lema daturaphila Kogan & Goeden (Coleoptera: Chrysomelidae). Both of these insects have been observed feeding on leaves from various species of Solanaceae in the study site. We analyzed extracts from insects and the host plant using gas chromatography and mass spectrometry (GC-MS). In B. suaveolens, we identified five TAs, while in the insect bodies, we found four. Scopolamine was the most abundant alkaloid in all the samples. This is the first report of TAs in these insects. While TAS may play a role in defense against generalist herbivores, further investigation is needed to understand the association between TAs and predators since both insects exhibit moderately aposematic features

How generalist insect herbivores respond to alien plants? The case of Aphis fabae-Myzus persicae-Rhododendron ponticum.

The enemy release hypothesis (ERH) predicts that alien plant species are unsuitable hosts for native phytophagous insects. However, the biotic resistance hypothesis (BRH) predicts that generalist herbivores may prefer an alien plant over their common host plant. In this study, we have tested these two hypotheses by comparing the potential colonization of the invasive Pontic rhododendron (Rhododendron ponticum L.) versus the common rearing host plants by two generalist aphid species (Aphis fabae and Myzus persicae). We assessed (i) the probing behavior using the electrical penetration graph (EPG) technique and (ii) survival and fecundity in Petri dishes. The results showed the inability of A. fabae and Myzus persicae to immediately colonize R. ponticum. Despite their ability to feed on this invasive plant, the two aphid species hardly survived and poorly reproduced. Our results are consistent with the ERH, since R. ponticum appeared as an unsuitable host for native phytophagous insects. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Selection pressure by specialist and generalist insect herbivores leads to optimal constitutive plant defense. A mathematical model.

Brassicaceae plants have the glucosinolate-myrosinase defense system, jointly active against herbivory. However, constitutive glucosinolate (GLS) defense is observed to occur at levels that do not deter all insects from feeding. That prompts the question of why Brassicaceae plants have not evolved a higher constitutive defense. The answer may lie in the contrasting relationship between plant defense and host plant preference of specialist and generalist herbivores. GLS content increases a plant's susceptibility to specialist insects. In contrast, generalists are deterred by the plant GLSs. Although GLSs can attract the natural enemies (predators and parasitoids) of these herbivores, enemies can reduce herbivore pressure to some extent only. So, plants can be overrun by specialists if GLS content is too high, whereas generalists can invade the plants if it is too low. Therefore, an optimal constitutive plant defense can minimize the overall herbivore pressure. To explain the optimal defense theoretically, we model the contrasting host selection behavior of insect herbivores and the emergence of their natural enemies by non-autonomous ordinary differential equations, where the independent variable is the plant GLS concentration. From the model, we quantify the optimal amount of GLSs, which minimizes total herbivore (specialists and generalists) pressure. That quite successfully explains the evolution of constitutive defense in plants from the perspective of optimality theory.

Linking Anthropogenic Landscape Perturbation to Herbivory and Pathogen Leaf Damage in Tropical Tree Communities.

Anthropogenic disturbance of tropical humid forests leads to habitat loss, biodiversity decline, landscape fragmentation, altered nutrient cycling and carbon sequestration, soil erosion, pest/pathogen outbreaks, among others. Nevertheless, the impact of these alterations in multitrophic interactions, including host-pathogen and vector-pathogen dynamics, is still not well understood in wild plants. This study aimed to provide insights into the main drivers for the incidence of herbivory and plant pathogen damage, specifically, into how vegetation traits at the local and landscape scale modulate such interactions. For this purpose, in the tropical forest of Calakmul (Campeche, Mexico), we characterised the foliar damage caused by herbivores and pathogens in woody vegetation of 13 sampling sites representing a gradient of forest disturbance and fragmentation in an anthropogenic landscape from well preserved to highly disturbed and fragmented areas. We also evaluated how the incidence of such damage was modulated by the vegetation and landscape attributes. We found that the incidence of damage caused by larger, mobile, generalist herbivores, was more sensitive to changes in landscape configuration, while the incidence of damage caused by small and specialised herbivores with low dispersal capacity was more influenced by vegetation and landscape composition. In relation to pathogen symptoms, the herbivore-induced foliar damage seems to be the main factor related to their incidence, indicating the enormous importance of herbivorous insects in the modulation of disease dynamics across tropical vegetation, as they could be acting as vectors and/or facilitating the entry of pathogens by breaking the foliar tissue and the plant defensive barriers. The incidence of pathogen damage also responded to vegetation structure and landscape configuration; the incidence of anthracnose, black spot, and chlorosis, for example, were favoured in sites surrounded by smaller patches and a higher edge density, as well as those with a greater aggregation of semi-evergreen forest patches. Fungal pathogens were shown to be an important cause of foliar damage for many woody species. Our results indicate that an increasing transformation and fragmentation of the tropical forest of southern Mexico could reduce the degree of specialisation in plant-herbivore interactions and enhance the proliferation of generalist herbivores (chewers and scrapers) and of mobile leaf suckers, and consequently, the proliferation of some symptoms associated with fungal pathogens such as fungus black spots and anthracnose. The symptoms associated with viral and bacterial diseases and to nutrient deficiency, such as chlorosis, could also increase in the vegetation in fragmented landscapes with important consequences in the health and productivity of wild and cultivated plant species. This is a pioneering study evaluating the effect of disturbances on multitrophic interactions, offering key insights on the main drivers of the changes in herbivory interactions and incidence of plant pathogens in tropical forests.

Soil cadmium pollution facilitated the invasion of alligator weed through enhanced herbivore resistance and competitive ability over a congeneric species.

A number of invasive plant species, such as Alternanthera philoxeroides, have been documented to be able to accumulate trace metal elements in their tissues. Since metal accumulation in plants can serve as a defence against herbivores, we hypothesized that metal pollution will increase herbivore resistance of metal-accumulating invasive plant species and such a benefit will grant them a competitive advantage over local co-occurring plants. In this study, we compared the differences in plant growth and herbivore feeding preference between A. philoxeroides and its native congener Alternanthera sessilis in single and mixed cultures with and without soil cadmium (Cd) pollution. The results showed that A. philoxeroides plants were more tolerant to Cd stress and accumulated more Cd in the leaves than A. sessilis. Cd exposure increased the resistance of A. philoxeroides against a specialist and a generalist herbivore compared withA. sessilis. Competition experiments indicated that Cd stress largely increased the competitive advantage of A. philoxeroides over A. sessilis with or without herbivore pressures. The differences in herbivore resistance between the two plant species under soil Cd stress are most likely due to the deterring effect of Cd accumulation and Cd-enhanced mechanical defences rather than changes in leaf specialized metabolites.

Explaining variation in plant‐herbivore associational effects in a tree biodiversity experiment

Abstract Within biodiversity‐ecosystem function research, a major outstanding question is how herbivory, a critical ecosystem function at the base of the food web, changes along gradients of plant biodiversity. Neighbourhood‐level associational effects are hypothesised to be a strong driver of biodiversity‐herbivory relationships, but we lack a successful framework that explains the wide variation observed in the sign and magnitude of plant‐herbivore associational effects. In this study, we combine measurements from a tree biodiversity field experiment with simulation to provide a framework for explaining variation in plant‐herbivore associational effects, particularly when herbivores that feed on many different species (e.g. generalists) cause most damage. We show that monoculture herbivory levels of focal species and their neighbours predict the direction and strength of associational effects. We provide evidence that this may be due to a “spillover effect”, in which some insect herbivores attracted to focal individuals ultimately end up feeding on neighbouring individuals. With an empirically parameterised simulation, we explain how spatial organisation modifies biodiversity‐ecosystem function relationships when associational effects operate. We suggest a set of experiments to test the generality of our conceptual framework, to elucidate the underlying mechanisms that produce the patterns we find, and to ultimately increase the predictability of plant‐herbivore associational effects. We conclude by discussing how our results might inform pest management in diversified agroecosystems and reforestation sites. Synthesis. Our results provide a potential framework for explaining why positive and negative plant‐herbivore associational effects are often balanced in systems with primarily generalist herbivores and point to a path forward for predicting when increased plant biodiversity will be associated with increased, decreased or unchanged levels of insect herbivory on individual plant species in such systems.

Herbivore and native plant diversity synergistically resist alien plant invasion regardless of nutrient conditions

Alien plant invasion success can be inhibited by two key biotic factors: native herbivores and plant diversity. However, few studies have experimentally tested whether these factors interact to synergistically resist invasion success, especially factoring in changing global environments (e.g. nutrient enrichment). Here we tested how the synergy between native herbivores and plant diversity affects alien plant invasion success in various nutrient conditions. For this purpose, we exposed alien plant species in pot-mesocosms to different levels of native plant diversity (4 vs. 8 species), native generalist herbivores, and high and low soil nutrient levels. We found that generalist herbivores preferred alien plants to native plants, inhibiting invasion success in a native community. This inhibition was amplified by highly diverse native communities. Further, the amplified effect between herbivory and native plant diversity was independent of nutrient conditions. Our results suggest that a higher diversity of native communities can strengthen the resistance of native generalist herbivores to alien plant invasions by enhancing herbivory tolerance. The synergistic effect remains in force in nutrient-enriched habitats that are always invaded by alien plant species. Our results shed light on the effective control of plant invasions using multi-trophic means, even in the face of future global changes.

Plant defences as functional traits: A comparison across savannas differing in herbivore specialization

Abstract Top‐down and bottom‐up forces in tropical savannas have shaped the evolution of traits that enable plants to thrive in environments where soils are poor, dry seasons are long, fire is frequent, woody plants and grasses compete and herbivores range from cryptic caterpillars to elephants that topple entire trees. African savannas and the South American cerrado have similar climates and fire regimes, but differ in the presence of large mammal herbivores, which are mostly extinct in the cerrado. These biomes offer an instructive comparison to understand how plant defence traits evolved in response to differential herbivore pressure. Within Africa, mammalian herbivore pressure also differs across savannas, being lower in the miombo relative to more open, mixed savannas. The dominance of specialist insect herbivores in the cerrado, relative to the more generalist mammalian herbivores in Africa, suggests that defence traits will differ between savannas in accordance with herbivore identity and pressure. Wood is densest in mixed African savannas, as expected because large mammals often damage trees. Specific leaf area, related to palatability, is higher in mixed African savannas and the cerrado relative to the miombo, while leaf N is surprisingly higher in miombo species. Ant mutualists are important defences in mixed African savannas and the cerrado. Defensive chemistry has received less attention in the trait literature. Foliar phenolics, the most commonly studied chemical defences in savannas, vary in their efficacy. New analyses isolating specific compounds are informative as is the evaluation of phytochemical diversity as a defence. There are indications that phytochemical defences are more diverse in the cerrado, which may be related to greater specialization of cerrado herbivores. Synthesis. The dominance of specialist insect herbivores in the cerrado, relative to generalist mammalian herbivores in Africa, selected for different plant defence traits, contributing to the separation of species along the leaf economics spectrum and demonstrating the importance of plant defences as plant functional traits. African savanna species seem to follow a more acquisitive strategy, followed by miombo species. Cerrado species appear to follow a more conservative strategy with greater investments in tough leaves and chemical defences.

Are rare plant species less resistant than common ones to herbivores? A multi-plant species study using above- and below-ground generalist herbivores.

Rare plant species are suggested to be less resistant to herbivores than common species. Their lower apparency and the fact that they often live in isolated populations, resulting in fewer herbivore encounters, might have led to the evolution of reduced defences. Moreover, their frequent lower levels of genetic diversity compared with common species could negatively affect their resistance against enemies. However, the hypothesis that plant resistance depends on plant regional and local rarity, independently of habitat and competitive and growth strategy, lacks evidence. To test this hypothesis, we assessed the performance and preference of one belowground and three aboveground generalist invertebrate herbivores from different taxonomic groups as indicators of plant resistance. Herbivores were fed a total of 62 regionally and locally rare and common plant species from Switzerland. We accounted for differences in a plant's growth and competitive strategy and habitat resource availability. We found that regionally and locally rare and common plant species did not generally differ in their resistance to most generalist herbivores. However, one herbivore species even performed better and preferred locally and regionally common plant species over rarer ones, indicating that common species are not more resistant, but tend to be less resistant. We also found that all herbivore species consistently performed better on competitive and large plant species, although different herbivore species generally preferred and performed better on different plant species. The latter indicates that the use of generalist herbivores as indicators of plant-resistance levels can be misleading. Synthesis: Our results show that rare plant species are not inherently less resistant than common ones to herbivores. Instead, our results suggest that the ability of plants to allocate resources away from defence towards enhancing their competitive ability might have allowed plants to tolerate herbivory, and to become locally and regionally common.

A nuclear receptor HR96-related gene underlies large trans-driven differences in detoxification gene expression in a generalist herbivore

The role, magnitude, and molecular nature of trans-driven expression variation underlying the upregulation of detoxification genes in pesticide resistant arthropod populations has remained enigmatic. In this study, we performed expression quantitative trait locus (eQTL) mapping (n = 458) between a pesticide resistant and a susceptible strain of the generalist herbivore and crop pest Tetranychus urticae. We found that a single trans eQTL hotspot controlled large differences in the expression of a subset of genes in different detoxification gene families, as well as other genes associated with host plant use. As established by additional genetic approaches including RNAi gene knockdown, a duplicated gene with a nuclear hormone receptor HR96-related ligand-binding domain was identified as causal for the expression differences between strains. The presence of a large family of HR96-related genes in T. urticae may enable modular control of detoxification and host plant use genes, facilitating this species’ known and rapid evolution to diverse pesticides and host plants.

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.

Evolutionary signatures of a trade-off in direct and indirect defenses across the wild grape genus Vitis.

Evolutionary correlations between chemical defense and protection by mutualist bodyguards have been long predicted, but tests of these pattern remain rare. We use a phylogenetic framework to test for evolutionary correlations indicative of trade-offs or synergisms between direct defense in the form of plant secondary metabolism, and indirect defense in the form of leaf domatia, across 33 species in the wild grape genus, Vitis. We also performed a bioassay with a generalist herbivore to associate our chemical phenotypes with herbivore palatability. Finally, we tested whether defensive traits correlate with the average abiotic characteristics of each species' contemporary range and whether these correlations were consistent with plant defense theory. We found a negative evolutionary correlation between domatia size and the diversity of secondary metabolites in Vitis leaf tissue across the genus, and also that leaves with a higher diversity and richness of secondary metabolites were less palatable to a generalist herbivore, consistent with a trade-off in chemical and mutualistic defense investment. Predictions from plant defense theory were not supported by associations between investment in defense phenotypes and abiotic variables. Our work demonstrates an evolutionary pattern indicative of a trade-off between indirect and direct defense strategies across the Vitis genus.

Adult presence does not ameliorate juvenile feeding challenges in a leaf-footed bug.

Herbivores often grapple with structural defences in their host plants, which may pose especially difficult challenges for juveniles due to their underdeveloped feeding morphology. The degree to which juvenile herbivore survival is limited by structural defences as well as the strategies used to overcome them are not well understood. We hypothesized that juveniles benefit from feeding near adults because adults pierce through physical barriers while feeding, enabling juveniles to access nutrients that they otherwise could not. We tested this feeding facilitation hypothesis in the leaf-footed bug Leptoglossus zonatus (Hemiptera: Coreidae). Bugs were raised with an adult or a juvenile conspecific and fed a diet of pecans with or without shells. As predicted, we found that juveniles suffered greater mortality when fed nuts with shells than when fed nuts without shells. Contrary to our expectations, the presence of an adult feeding on the same nut did not lessen this effect. Therefore, the presence of an adult does not ameliorate the feeding difficulties faced by juvenile L. zonatus, despite evidence for feeding facilitation in related insect species. This study adds to our understanding of how host plant defences can limit the survival of even highly generalist herbivores.

Generalist dietary responses to individual versus combined plant toxin odors: an African elephant study

Abstract The detoxification limitation hypothesis posits that, unless plant defense compounds interact synergistically or additively to increase their harmful effects, generalist herbivores will prefer consuming combinations of these compounds more than singular compounds. Monoterpenes are odoriferous defense compounds that may be toxic to mammalian herbivores when ingested in sufficient quantities. Previous research has shown that the addition of individual monoterpenes to food sources reduces consumption by generalist mammalian herbivores. By using African elephants as a case study, we aimed to determine whether odors from monoterpene combinations (i.e., two or more monoterpenes) also deter generalist mammalian herbivory, and whether generalist herbivores prefer the odors of monoterpene combinations more than individual monoterpenes. First, we tested whether the odor of monoterpene combinations that resemble the monoterpene profiles of a high-acceptability, intermediate-acceptability, and low-acceptability plant deter herbivory. We found that elephants preferred plants without the added odors of the monoterpene combinations. Second, we explored how elephants responded to individual monoterpenes found within the combinations compared with the combinations at the same set concentration, and found that the elephants did not always prefer the combinations more than the individual monoterpenes. Moreover, the more diverse the combination, the less frequently it was preferred when compared with the individual monoterpene odors. Our results imply that generalist herbivores do not necessarily prefer combinations of plant chemical defenses at comparatively lower concentrations and that, consequently, the composition and diversity of monoterpene profiles in plants likely determine the efficacy of these compounds as an olfactory defense against mammalian herbivory.

Assessment of the role of an ABCC transporter TuMRP1 in the toxicity of abamectin to Tetranychus urticae

The rapid evolution of pest resistance threatens the sustainable utilization of bioinsecticides such as abamectin, and so deciphering the molecular mechanisms affecting toxicity and resistance is essential for their long-term application. Historical studies of abamectin resistance in arthropods have mainly focused on mechanisms involving the glutamate-gated chloride channel (GluCl) targets, with the role of metabolic processes less clear. The two-spotted spider mite, Tetranychus urticae, is a generalist herbivore notorious for rapidly developing resistance to pesticides worldwide, and abamectin has been widely used for its control in the field. After reanalyzing previous transcriptome and RNA-seq data, we here identified an ABC transporter subfamily C gene in T. urticae named multidrug resistance-associated protein 1 (TuMRP1), whose expression differed between susceptible and resistant populations. Synergism bioassays with the inhibitor MK-571, the existence of a genetic association between TuMRP1 expression and susceptibility to abamectin, and the effect of RNA interference mediated silencing of TuMRP1 were all consistent with a direct role of this transporter protein in the toxicity of abamectin. Although ABC transporters are often involved in removing insecticidal compounds from cells, our data suggest either an alternative role for these proteins in the mechanism of action of abamectin or highlight an indirect association between their expression and abamectin toxicity.

Nutrient supply and accessibility in plants: effect of protein and carbohydrates on Australian plague locust (Chortoicetes terminifera) preference and performance.

In contrast to predictions from nitrogen limitation theory, recent studies have shown that herbivorous migratory insects tend to be carbohydrate (not protein) limited, likely due to increased energy demands, leading them to preferentially feed on high carbohydrate plants. However, additional factors such as mechanical and chemical defenses can also influence host plant choice and nutrient accessibility. In this study, we investigated the effects of plant protein and carbohydrate availability on plant selection and performance for a migratory generalist herbivore, the Australian plague locust, Chortoicetes terminifera. We manipulated the protein and carbohydrate content of seedling wheat (Triticum aestivum L.) by increasing the protein:carbohydrate ratio using nitrogen (N) fertilizer, and manipulated the physical structure of the plants by grinding and breaking down cell walls after drying the plants. Using a full factorial design, we ran both choice and no-choice experiments to measure preference and performance. We confirmed locust preference for plants with a lower protein-carbohydrate ratio (unfertilized plants). Unlike previous studies with mature wild grass species, we found that intact plants supported better performance than dried and ground plants, suggesting that cell wall removal may only improve performance for tougher or more carbohydrate-rich plants. These results add to the growing body of evidence suggesting that several migratory herbivorous species perform better on plants with a lower protein:carbohydrate ratio.

Host adaptation and specialization in Tetranychidae mites.

Composite generalist herbivores are comprised of host-adapted populations that retain the ability to shift hosts. The degree and overlap of mechanisms used by host-adapted generalist and specialist herbivores to overcome the same host plant defenses are largely unknown. Tetranychidae mites are exceptionally suited to address the relationship between host adaptation and specialization in herbivores as this group harbors closely related species with remarkably different host ranges-an extreme generalist the two-spotted spider mite (Tetranychus urticae Koch [Tu]) and the Solanaceous specialist Tetranychus evansi (Te). Here, we used tomato-adapted two-spotted spider mite (Tu-A) and Te populations to compare mechanisms underlying their host adaptation and specialization. We show that both mites attenuate induced tomato defenses, including protease inhibitors (PIs) that target mite cathepsin L digestive proteases. While Te solely relies on transcriptional attenuation of PI induction, Tu and Tu-A have elevated constitutive activity of cathepsin L proteases, making them less susceptible to plant anti-digestive proteins. Tu-A and Te also rely on detoxification of tomato constitutive defenses. Te uses esterase and P450 activities, while Tu-A depends on the activity of all major detoxification enzymatic classes to disarm tomato defensive compounds to a lesser extent. Thus, even though both Tu-A and Te use similar mechanisms to counteract tomato defenses, Te can better cope with them. This finding is congruent with the ecological and evolutionary times required to establish mite adaptation and specialization states, respectively.

Effect of Plant Defenses and Plant Nutrients on the Performance of Specialist and Generalist Herbivores of Datura: A Macroevolutionary Study.

Macroevolutionary patterns in the association between plant species and their herbivores result from ecological divergence promoted by, among other factors, plants' defenses and nutritional quality, and herbivore adaptations. Here, we assessed the performance of the herbivores Lema trilineata daturaphila, a trophic specialist on Datura, and Spodoptera frugiperda, a polyphagous pest herbivore, when fed with species of Datura. We used comparative phylogenetics and multivariate methods to examine the effects of Datura species' tropane alkaloids, leaf trichomes, and plant macronutrients on the two herbivores´ performances (amount of food consumed, number of damaged leaves, larval biomass increment, and larval growth efficiency). The results indicate that species of Datura do vary in their general suitability as food host for the two herbivores. Overall, the specialist performs better than the generalist herbivore across Datura species, and performance of both herbivores is associated with suites of plant defenses and nutrient characteristics. Leaf trichomes and major alkaloids of the Datura species are strongly related to herbivores' food consumption and biomass increase. Although hyoscyamine better predicts the key components of the performance of the specialist herbivore, scopolamine better predicts the performance of the generalist; however, only leaf trichomes are implicated in most performance components of the two herbivores. Nutrient quality more widely predicts the performance of the generalist herbivore. The contrasting effects of plant traits and the performances of herbivores could be related to adaptive differences to cope with plant toxins and achieve nutrient balance and evolutionary trade-offs and synergisms between plant traits to deal with a diverse community of herbivores.