Transgenerational plasticity of inducible defences: Combined effects of grand‐parental,parental and current environments

Phenotypic plasticity can occur across generations (transgenerational plasticity) when environments experienced by the previous generations influenced offspring phenotype. The evolutionary importance of transgenerational plasticity, especially regarding within‐generational plasticity, is a currently hot topic in the plasticity framework. How long an environmental effect can persist across generations and whether multigenerational effects are cumulative are primordial—for the evolutionary significance of transgenerational plasticity—but still unresolved questions. In this study, we investigated how the grand‐parental, parental and offspring exposures to predation cues shape the predator‐induced defences of offspring in the Physa acuta snail. We expected that the offspring phenotypes result from a three‐way interaction among grand‐parental, parental and offspring environments. We exposed three generations of snails without and with predator cues according to a full factorial design and measured offspring inducible defences. We found that both grand‐parental and parental exposures to predator cues impacted offspring antipredator defences, but their effects were not cumulative and depended on the defences considered. We also highlighted that the grand‐parental environment did alter reaction norms of offspring shell thickness, demonstrating an interaction between the grand‐parental transgenerational plasticity and the within‐generational plasticity. We concluded that the effects of multigenerational exposure to predator cues resulted on complex offspring phenotypic patterns which are difficult to relate to adaptive antipredator advantages.     

Phenotypic integration plasticity in Daphnia magna: an integral facet of G × E interactions

Phenotypic integration can be defined as the network of multivariate relationships among behavioural, physiological and morphological traits that describe the organism. Phenotypic integration plasticity refers to the change in patterns of phenotypic integration across environments or ontogeny. Because studies of phenotypic plasticity have predominantly focussed on single traits, a G × E interaction is typically perceived as differences in the magnitude of trait expression across two or more environments. However, many plastic responses involve coordinated responses in multiple traits, raising the possibility that relative differences in trait expression in different environments are an important, but often overlooked, source of G × E interaction. Here, we use phenotypic change vectors to statistically compare the multivariate life‐history plasticity of six Daphnia magna clones collected from four disparate European populations. Differences in the magnitude of plastic responses were statistically distinguishable for two of the six clones studied. However, differences in phenotypic integration plasticity were statistically distinguishable for all six of the clones studied, suggesting that phenotypic integration plasticity is an important component of G × E interactions that may be missed unless appropriate multivariate analyses are used.     

Inbreeding and adaptive plasticity: an experimental analysis on predator‐induced responses in the water flea Daphnia

Several studies have emphasized that inbreeding depression (ID) is enhanced under stressful conditions. Additionally, one might imagine a loss of adaptively plastic responses which may further contribute to a reduction in fitness under environmental stress. Here, we quantified ID in inbred families of the cyclical parthenogen Daphnia magna in the absence and presence of fish predation risk. We test whether predator stress affects the degree of ID and if inbred families have a reduced capacity to respond to predator stress by adaptive phenotypic plasticity. We obtained two inbred families through clonal selfing within clones isolated from a fish pond. After mild purging under standardized conditions, we compared life history traits and adaptive plasticity between inbred and outbred lineages (directly hatched from the natural dormant egg bank of the same pond). Initial purging of lineages under standardized conditions differed among inbred families and exceeded that in outbreds. The least purged inbred family exhibited strong ID for most life history traits. Predator‐induced stress hardly affected the severity of ID, but the degree to which the capacity for adaptive phenotypic plasticity was retained varied strongly among the inbred families. The least purged family overall lacked the capacity for adaptive phenotypic plasticity, whereas the family that suffered only mild purging exhibited a potential for adaptive plasticity that was comparable to the outbred population. We thus found that inbred offspring may retain the capacity to respond to the presence of fish by adaptive phenotypic plasticity, but this strongly depends on the parental clone engaging in selfing.     

Masting behaviour in a Mediterranean pine tree alters seed predator selection on reproductive output

• Context‐dependency in species interactions is widespread and can produce concomitant patterns of context‐dependent selection. Masting (synchronous production of large seed crops at irregular intervals by a plant population) has been shown to reduce seed predation through satiation (reduction in rates of seed predation with increasing seed cone output) and thus represents an important source of context‐dependency in plant‐animal interactions. However, the evolutionary consequences of such dynamics are not well understood.
• Here we describe masting behaviour in a Mediterranean model pine species (Pinus pinaster) and present a test of the effects of masting on selection by seed predators on reproductive output. We predicted that masting, by enhancing seed predator satiation, could in turn strengthen positive selection by seed predators for larger cone output. For this we collected six‐year data (spanning one mast year and five non‐mast years) on seed cone production and seed cone predation rates in a forest genetic trial composed by 116 P. pinaster genotypes.
• Following our prediction, we found stronger seed predator satiation during the masting year, which in turn led to stronger seed predator selection for increased cone production relative to non‐masting years.
• These findings provide evidence that masting can alter the evolutionary outcome of plant‐seed predator interactions. More broadly, our findings highlight that changes in consumer responses to resource abundance represent a widespread mechanism for predicting and understanding context dependency in plant‐consumer evolutionary dynamics.

     

Molecular mechanisms of tolerance to cyanobacterial protease inhibitors revealed by clonal differences in Daphnia magna

Protease inhibitors of primary producers are a major food quality constraint for herbivores. In nutrient‐rich freshwater ecosystems, the interaction between primary producers and herbivores is mainly represented by Daphnia and cyanobacteria. Protease inhibitors have been found in many cyanobacterial blooms. These inhibitors have been shown (both in vitro and in situ) to inhibit the most important group of digestive proteases in the daphnid's gut, that is, trypsins and chymotrypsins. In this study, we fed four different Daphnia magna genotypes with the trypsin‐inhibitor‐containing cyanobacterial strain Microcystis aeruginosa PCC 7806 Mut. Upon exposure to dietary trypsin inhibitors, all D. magna genotypes showed increased gene expression of digestive trypsins and chymotrypsins. Exposure to dietary trypsin inhibitors resulted in increased activity of chymotrypsins and reduced activity of trypsin. Strong intraspecific differences in tolerance of the four D. magna genotypes to the dietary trypsin inhibitors were found. The degree of tolerance depended on the D. magna genotype. The genotypes' tolerance was positively correlated with the residual trypsin activity and the different IC₅₀ values of the trypsins. On the genetic level, the different trypsin loci varied between the D. magna genotypes. The two tolerant Daphnia genotypes that both originate from the same lake, which frequently produces cyanobacterial blooms, clustered in a neighbour‐joining phylogenetic tree based on the three trypsin loci. This suggests that the genetic variability of trypsin loci was an important cause for the observed intraspecific variability in tolerance to cyanobacterial trypsin inhibitors. Based on these findings, it is reasonable to assume that such genetic variability can also be found in natural populations and thus constitutes the basis for local adaptation of natural populations to dietary protease inhibitors.     

Diverse genotypes of the amphibian‐killing fungus produce distinct phenotypes through plastic responses to temperature

Phenotypes are the target of selection and affect the ability of organisms to persist in variable environments. Phenotypes can be influenced directly by genes and/or by phenotypic plasticity. The amphibian‐killing fungus Batrachochytrium dendrobatidis (Bd) has a global distribution, unusually broad host range, and high genetic diversity. Phenotypic plasticity may be an important process that allows this pathogen to infect hundreds of species in diverse environments. We quantified phenotypic variation of nine Bd genotypes from two Bd lineages (Global Pandemic Lineage [GPL] and Brazil) and a hybrid (GPL‐Brazil) grown at three temperatures (12, 18 and 24°C). We measured five functional traits including two morphological traits (zoospore and zoosporangium sizes) and three life history traits (carrying capacity, time to fastest growth and exponential growth rate) in a phylogenetic framework. Temperature caused highly plastic responses within each genotype, with all Bd genotypes showing phenotypic plasticity in at least three traits. Among genotypes, Bd generally showed the same direction of plastic response to temperature: larger zoosporangia, higher carrying capacity, longer time to fastest growth and slower exponential growth at lower temperatures. The exception was zoospore size, which was highly variable. Our findings indicate that Bd genotypes have evolved novel phenotypes through plastic responses to temperature over very short timescales. High phenotypic variability likely extends to other traits and may facilitate the large host range and rapid spread of Bd.     

On the fate of seasonally plastic traits in a rainforest butterfly under relaxed selection

Many organisms display phenotypic plasticity as adaptation to seasonal environmental fluctuations. Often, such seasonal responses entails plasticity of a whole suite of morphological and life‐history traits that together contribute to the adaptive phenotypes in the alternative environments. While phenotypic plasticity in general is a well‐studied phenomenon, little is known about the evolutionary fate of plastic responses if natural selection on plasticity is relaxed. Here, we study whether the presumed ancestral seasonal plasticity of the rainforest butterfly Bicyclus sanaos (Fabricius, 1793) is still retained despite the fact that this species inhabits an environmentally stable habitat. Being exposed to an atypical range of temperatures in the laboratory revealed hidden reaction norms for several traits, including wing pattern. In contrast, reproductive body allocation has lost the plastic response. In the savannah butterfly, B. anynana (Butler, 1879), these traits show strong developmental plasticity as an adaptation to the contrasting environments of its seasonal habitat and they are coordinated via a common developmental hormonal system. Our results for B. sanaos indicate that such integration of plastic traits – as a result of past selection on expressing a coordinated environmental response – can be broken when the optimal reaction norms for those traits diverge in a new environment.     

Is there plasticity in developmental instability? The effect of daily thermal fluctuations in an ectotherm

Diversified bet‐hedging (DBH) by production of within‐genotype phenotypic variance may evolve to maximize fitness in stochastic environments. Bet‐hedging is generally associated with parental effects, but phenotypic variation may also develop throughout life via developmental instability (DI). This opens for the possibility of a within‐generation mechanism creating DBH during the lifetime of individuals. If so, DI could in fact be a plastic trait itself; if a fluctuating environment indicates uncertainty about future conditions, sensing such fluctuations could trigger DI as a DBH response. However, this possibility has received little empirical attention. Here, we test whether fluctuating environments may elicit such a response in the clonally reproducing crustacean Daphnia magna. Specifically, we exposed genetically identical individuals to two environments of different thermal stability (stable vs. pronounced daily realistic temperature fluctuations) and tested for effects on DI in body mass and metabolic rate shortly before maturation. Furthermore, we also estimated the genetic variation in DI. Interestingly, fluctuating temperatures did not affect body mass, but metabolic rate decreased. We found no evidence for plasticity in DI in response to environmental fluctuations. The lack of plasticity was common to all genotypes, and for both traits studied. However, we found considerable evolvability for DI, which implies a general evolutionary potential for DBH under selection for increased phenotypic variance.     

Species concept and nomenclatural changes within the genera Elliptochloris and Pseudochlorella (Trebouxiophyceae) based on an integrative approach

The genera Elliptochloris and Pseudochlorella were erected for Chlorella‐like green algae producing two types of autospores and cell packages, respectively. Both genera are widely distributed in different soil habitats, either as free living or as photobionts of lichens. The species of these genera are often difficult to identify because of the high phenotypic plasticity and occasional lack of characteristic features. The taxonomic and nomenclatural status of these species, therefore, remains unclear. In this study, 34 strains were investigated using an integrative approach. Phylogenetic analyses demonstrated that the isolates belong to two independent lineages of the Trebouxiophyceae (Elliptochloris and Prasiola clades) and confirmed that the genera are not closely related. The comparison of morphology, molecular phylogeny, and analyses of secondary structures of SSU and ITS rDNA sequences revealed that all of the strains belong to three genera: Elliptochloris, Pseudochlorella, and Edaphochlorella. As a consequence of the taxonomic revisions, we propose two new combinations (Elliptochloris antarctica and Pseudochlorella signiensis) and validate Elliptochloris reniformis, which is invalidly described according to the International Code for Nomenclature (ICN), by designating a holotype. To reflect the high phenotypic plasticity of P. signiensis, two new varieties were described: P. signiensis var. magna and P. signiensis var. communis. Chlorella mirabilis was not closely related to any of these genera and was, therefore, transferred to the new genus Edaphochlorella. All of the taxonomic changes were highly supported by all phylogenetic analyses and were confirmed by the ITS‐2 Barcodes using the ITS‐2/CBC approach.     

Interactions between a pollinating seed predator and its host plant: the role of environmental context within a population

Plant–insect interactions often are important for plant reproduction, but the outcome of these interactions may vary with environmental context. Pollinating seed predators have positive and negative effects on host plant reproduction, and the interaction outcome is predicted to vary with density or abundance of the partners. We studied the interaction between Silene stellata, an herbaceous perennial, and Hadena ectypa, its specialized pollinating seed predator. Silene stellata is only facultatively dependent upon H. ectypa for pollination because other nocturnal moth co‐pollinators are equally effective at pollen transfer. We hypothesized that for plants without conspecific neighbors, H. ectypa would have higher visitation rates compared to co‐pollinators, and the plants would experience lower levels of H. ectypa pollen deposition. We predicted similar oviposition throughout the study site but greater H. ectypa predation in the area without conspecific neighbors compared to plants embedded in a naturally high density area. We found that H. ectypa had consistently higher visitation than moth co‐pollinators in all host plant contexts. However, H. ectypa pollinator importance declined in areas with low conspecific density because of reduced pollen deposition, resulting in lower seed set. Conversely, oviposition was similar across the study site independent of host plant density. Greater likelihood of very high fruit predation combined with lower pollination by H. ectypa resulted in reduced S. stellata female reproductive success in areas with low conspecific density. Our results demonstrate local context dependency of the outcomes of pollinating seed predator interactions with conspecific host plant density within a population.     

Phylogeny and assemblage composition of Frankia in Alnus tenuifolia nodules across a primary successional sere in interior Alaska

In nitrogen (N) fixing symbioses, host‐symbiont specificity, genetic variation in bacterial symbionts and environmental variation represent fundamental constraints on the ecology, evolution and practical uses of these interactions, but detailed information is lacking for many naturally occurring N‐fixers. This study examined phylogenetic host specificity of Frankia in field‐collected nodules of two Alnus species (A. tenuifolia and A. viridis) in interior Alaska and, for A. tenuifolia, distribution, diversity, spatial autocorrelation and correlation with specific soil factors of Frankia genotypes in nodules collected from replicated habitats representing endpoints of a primary sere. Frankia genotypes most commonly associated with each host belonged to different clades within the Alnus‐infective Frankia clade, and for A. tenuifolia, were divergent from previously described Frankia. A. tenuifolia nodules from early and late succession habitats harboured distinct Frankia assemblages. In early succession, a single genotype inhabited 71% of nodules with no discernable autocorrelation at any scale, while late succession Frankia were more diverse, differed widely among plants within a site and were significantly autocorrelated within and among plants. Early succession Frankia genotype occurrence was strongly correlated with carbon/nitrogen ratio in the mineral soil fraction, while in late succession, the most common genotypes were correlated with different soil variables. Our results suggest that phylogenetic specificity is a significant factor in the A. tenuifolia‐Frankia interaction and that significant habitat‐based differentiation may exist among A. tenuifolia‐infective genotypes. This is consistent with our hypothesis that A. tenuifolia selects specific Frankia genotypes from early succession soils and that this choice is attenuated in late succession.     

Local adaptation and embryonic plasticity affect antipredator traits in hatchling pond snails

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Local genetic adaptation generates latitude‐specific effects of warming on predator–prey interactions

Temperature effects on predator–prey interactions are fundamental to better understand the effects of global warming. Previous studies never considered local adaptation of both predators and prey at different latitudes, and ignored the novel population combinations of the same predator–prey species system that may arise because of northward dispersal. We set up a common garden warming experiment to study predator–prey interactions between Ischnura elegans damselfly predators and Daphnia magna zooplankton prey from three source latitudes spanning >1500 km. Damselfly foraging rates showed thermal plasticity and strong latitudinal differences consistent with adaptation to local time constraints. Relative survival was higher at 24 °C than at 20 °C in southern Daphnia and higher at 20 °C than at 24 °C, in northern Daphnia indicating local thermal adaptation of the Daphnia prey. Yet, this thermal advantage disappeared when they were confronted with the damselfly predators of the same latitude, reflecting also a signal of local thermal adaptation in the damselfly predators. Our results further suggest the invasion success of northward moving predators as well as prey to be latitude‐specific. We advocate the novel common garden experimental approach using predators and prey obtained from natural temperature gradients spanning the predicted temperature increase in the northern populations as a powerful approach to gain mechanistic insights into how community modules will be affected by global warming. It can be used as a space‐for‐time substitution to inform how predator–prey interaction may gradually evolve to long‐term warming.     

Thermal tolerance in the keystone species Daphnia magna—a candidate gene and an outlier analysis approach

Changes in temperature have occurred throughout Earth's history. However, current warming trends exacerbated by human activities impose severe and rapid loss of biodiversity. Although understanding the mechanisms orchestrating organismal response to climate change is important, remarkably few studies document their role in nature. This is because only few systems enable the combined analysis of genetic and plastic responses to environmental change over long time spans. Here, we characterize genetic and plastic responses to temperature increase in the aquatic keystone grazer Daphnia magna combining a candidate gene and an outlier analysis approach. We capitalize on the short generation time of our species, facilitating experimental evolution, and the production of dormant eggs enabling the analysis of long‐term response to environmental change through a resurrection ecology approach. We quantify plasticity in the expression of 35 candidate genes in D. magna populations resurrected from a lake that experienced changes in average temperature over the past century and from experimental populations differing in thermal tolerance isolated from a selection experiment. By measuring expression in multiple genotypes from each of these populations in control and heat treatments, we assess plastic responses to extreme temperature events. By measuring evolutionary changes in gene expression between warm‐ and cold‐adapted populations, we assess evolutionary response to temperature changes. Evolutionary response to temperature increase is also assessed via an outlier analysis using EST‐linked microsatellite loci. This study provides the first insights into the role of plasticity and genetic adaptation in orchestrating adaptive responses to environmental change in D. magna.     

High‐resolution melting analysis: a genotyping tool for population studies on Daphnia

Determining genetic variation at the DNA level within and between natural populations is important for understanding the role of natural selection on phenotypic traits, but many techniques of screening for genetic variation are either cost intensive, not sensitive enough or too labour‐ and time‐consuming. Here, we demonstrate high‐resolution melting analysis (HRMA) as a cost‐effective and powerful tool for screening variable target genes in natural populations. HRMA is based on monitoring the melting of PCR amplicons. Owing to saturating concentrations of a dye that binds at high concentrations to double‐stranded DNA, it is possible to genotype high numbers of samples rapidly and accurately. We analysed digestive trypsins of two Daphnia magna populations as an application example for HRMA. One population originated from a pond containing toxic cyanobacteria that possibly produce protease inhibitors and the other from a pond without such cyanobacteria. The hypothesis was that D. magna clones from ponds with cyanobacteria have undergone selection by these inhibitors, which has led to different trypsin alleles. We first sequenced pooled genomic PCR products of trypsins from both populations to identify variable DNA sequences of active trypsins. Second, we screened variable DNA sequences of each D. magna clone from both populations for single nucleotide polymorphisms via HRMA. The HRMA results revealed that both populations exhibited phenotypic differences in the analysed trypsins. Our results indicate that HRMA is a powerful genotyping tool for studying the variation of target genes in response to selection within and between natural Daphnia populations.     

Caterpillar‐induced plant volatiles attract conspecific herbivores and a generalist predator

Plants release volatiles in response to caterpillar feeding that attracts natural enemies of the herbivores, a tritrophic interaction which has been considered to be an indirect plant defence against herbivores. On the other hand, the caterpillar‐induced plant volatiles have been reported to either repel or attract conspecific adult herbivores. This work was undertaken to investigate the response of both herbivores and natural enemies to caterpillar‐induced plant volatiles in apple orchards. We sampled volatile compounds emitted from uninfested apple trees, and apple trees infested with generalist herbivore the pandemis leafroller moth, Pandemis pyrusana (Lepidoptera, Tortricidae) larvae using headspace collection and analysed by gas chromatography/mass spectrometry. Infested apple trees uniquely release six compounds (benzyl alcohol, phenylacetonitrile, phenylacetaldehyde, 2‐phenylethanol, indole and (E)‐nerolidol). These compounds were tested on two species of herbivores and one predator in apple orchards. Binary blends of phenylacetonitrile + acetic acid or 2‐phenylethanol + acetic acid attracted a large number of conspecific male and female adult herbivores. The response of pandemis leafroller to herbivore‐induced plant volatiles (HIPVs) was so pronounced that over one thousand and seven hundred conspecific male and female adult herbivores were caught in traps baited with HIPVs in three‐day trapping period. In addition, significantly higher number of male and female obliquebanded leafroller, Choristoneura rosaceana (Lepidoptera, Tortricidae), was caught in traps baited a binary blend of 2‐phenylethanol + acetic acid, or a ternary blend contains 2‐phenylethanol and phenylacetonitrile + acetic acid. This result challenges the current paradigm hypothesized that HIPVs repel herbivores and question the indirect defensive function proposed for these compounds. On the other hand, a ternary blend of phenylacetonitrile and 2‐phenylethanol + acetic acid attracted the largest numbers of the general predator, the common green lacewing, Chrysoperla plorabunda. To our knowledge, this is the first record of the direct attraction of conspecific adult herbivores as well as a predator to the caterpillar‐induced plant volatiles in the field.     

Effects of predator density and duration of predator occupancy on crustacean abundance and diversity in experimental pools

Keystone predators, by reducing the abundance of competitively superior prey, may have indirect positive effects on weak competitors, possibly increasing their abundance or preventing local competitive exclusion. By analogy to the Intermediate Disturbance Hypothesis, we would expect species diversity to peak at intermediate predator densities. In a replicated artificial pool experiment, we examined the relationships between density of the backswimmer Notonecta maculata (0, 1, 2, and 4 per 30 l pool) and invertebrate taxon diversity over an 11-week period of predator occupancy. Diversity reached high levels at high predator density sooner than at intermediate density. At the end of the experiment, taxon diversity was greatest at densities of 2 and 4 Notonecta per pool. While the overall predator density–diversity curve was in line with the intermediate disturbance hypothesis, the reduction in diversity from intermediate to high predator density was not statistically significant. Density of the preferred prey Daphnia magna decreased with Notonecta density, while densities of the smaller cladocerans Moina brachiata and Ceriodaphnia spp. increased. Suppression of Daphnia at high Notonecta densities may partially explain the increase in Moina and Ceriodaphnia densities. However, most of the relationship between Notonecta and the smaller cladocerans appears to be independent of Daphnia, suggesting complex interactions within the community. Our results suggest that keystone predation plays a strong role in structuring this community. Although diversity did not decrease significantly at the highest predator density as predicted, such a decrease may be more likely for pools with longer durations of predator occupancy or with higher predator densities.     

The effect of top‐predator presence and phenotype on aquatic microbial communities

The presence of predators can impact a variety of organisms within the ecosystem, including microorganisms. Because the effects of fish predators and their phenotypic differences on microbial communities have not received much attention, we tested how the presence/absence, genotype, and plasticity of the predatory three‐spine stickleback (Gasterosteus aculeatus) influence aquatic microbes in outdoor mesocosms. We reared lake and stream stickleback genotypes on contrasting food resources to adulthood, and then added them to aquatic mesocosm ecosystems to assess their impact on the planktonic bacterial community. We also investigated whether the effects of fish persisted following the removal of adults, and the subsequent addition of a homogenous juvenile fish population. The presence of adult stickleback increased the number of bacterial OTUs and altered the size structure of the microbial community, whereas their phenotype affected bacterial community composition. Some of these effects were detectable after adult fish were removed from the mesocosms, and after juvenile fish were placed in the tanks, most of these effects disappeared. Our results suggest that fish can have strong short‐term effects on microbial communities that are partially mediated by phenotypic variation of fish.     

Do insect pests perform better on highly defended plants? Costs and benefits of induced detoxification defences in the aphid Sitobion avenae

Induced defences are a typical case of phenotypic plasticity, involving benefits for ‘plastic’ phenotypes under environments with variable degree of stress. Defence induction, in turn, could be energetically expensive incurring costs on growth and reproduction. In this study, we investigated the genetic variation and induction of detoxification enzymes mediated by wheat chemical defences (hydroxamic acids; Hx), and their metabolic and fitness costs using five multilocus genotypes of the grain aphid (Sitobion avenae). Cytochrome P450 monooxygenases and glutathione S‐transferases activities were seen to increase with Hx levels, whereas esterases activity and standard metabolic rate increased in wheat hosts with low Hx levels. Additionally, the intrinsic rate of increase (a fitness proxy) increased in highly defended hosts. However, we did not find significant genetic variation or genotype–host interaction for any studied trait. Therefore, aphids feeding on host plants with elevated chemical defences appeared to reduce their detoxification costs and to increase their reproductive performance, which we interpret as a novel adaptation to defended plants. In brief, this study supports the notion that aphids perform better on highly defended host plants, probably related to the selective pressures during the colonization of New World agroecosystems, characterized by highly defended host plants.