Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies

Conclusions Contrasting effects of generalist and specialist herbivores can explain why all plants have not evolved high levels of defence. Maintenance of variation in concentration of defence substances can be explained by a shifting balance between natural selection for defence against herbivory by specialists and generalists. Generalist natural enemies will shift the optimal defence curve to lower concentrations of defences. Physiological costs of production of defence substances and selection by specialist herbivores of plant phenotypes with higher levels of defence compounds for sequestration are no essential elements of this model. They may, however, adjust the predicted optimum defence function and contribute to maintenance of variation of concentrations of defence substances.     

Coexistence of trichome variation in a natural plant population: a combined study using ecological and candidate gene approaches

The coexistence of distinct phenotypes within populations has long been investigated in evolutionary ecology. Recent studies have identified the genetic basis of distinct phenotypes, but it is poorly understood how the variation in candidate loci is maintained in natural environments. In this study, we examined fitness consequences and genetic basis of variation in trichome production in a natural population of Arabidopsis halleri subsp. gemmifera. Half of the individuals in the study population produced trichomes while the other half were glabrous, and the leaf beetle Phaedon brassicae imposed intensive damage to both phenotypes. The fitness of hairy and glabrous plants showed no significant differences in the field during two years. A similar result was obtained when sibling hairy and glabrous plants were transplanted at the same field site, whereas a fitness cost of trichome production was detected under a weak herbivory condition. Thus, equivalent fitness of hairy and glabrous plants under natural herbivory allows their coexistence in the contemporary population. The pattern of polymorphism of the candidate trichome gene GLABROUS1 (GL1) showed no evidence of long-term maintenance of trichome variation within the population. Although balancing selection under fluctuating biotic environments is often proposed to explain the maintenance of defense variation, the lack of clear evidence of balancing selection in the study population suggests that other factors such as gene flow and neutral process may have played relatively large roles in shaping trichome variation at least for the single population level.     

Family matters: effect of host plant variation in chemical and mechanical defenses on a sequestering specialist herbivore

Insect herbivores contend with various plant traits that are presumed to function as feeding deterrents. Paradoxically, some specialist insect herbivores might benefit from some of these plant traits, for example by sequestering plant chemical defenses that herbivores then use as their own defense against natural enemies. Larvae of the butterfly species Battus philenor (L.) (Papilionidae) sequester toxic alkaloids (aristolochic acids) from their Aristolochia host plants, rendering larvae and adults unpalatable to a broad range of predators. We studied the importance of two putative defensive traits in Aristolochia erecta: leaf toughness and aristolochic acid content, and we examined the effect of intra- and interplant chemical variation on the chemical phenotype of B. philenor larvae. It has been proposed that genetic variation for sequestration ability is ??invisible to natural selection?? because intra- and interindividual variation in host-plant chemistry will largely eliminate a role for herbivore genetic variation in determining an herbivore??s chemical phenotype. We found substantial intra- and interplant variation in leaf toughness and in the aristolochic acid chemistry in A. erecta. Based on field observations and laboratory experiments, we showed that first-instar larvae preferentially fed on less tough, younger leaves and avoided tougher, older leaves, and we found no evidence that aristolochic acid content influenced first-instar larval foraging. We found that the majority of variation in the amount of aristolochic acid sequestered by larvae was explained by larval family, not by host-plant aristolochic acid content. Heritable variation for sequestration is the predominant determinant of larval, and likely adult, chemical phenotype. This study shows that for these highly specialized herbivores that sequester chemical defenses, traits that offer mechanical resistance, such as leaf toughness, might be more important determinants of early-instar larval foraging behavior and development compared to plant chemical defenses.     

Untargeted metabolic profiling reveals geography as the strongest predictor of metabolic phenotypes of a cosmopolitan weed

Plants produce a multitude of metabolites that contribute to their fitness and survival and play a role in local adaptation to environmental conditions. The effects of environmental variation are particularly well studied within the genus Plantago; however, previous studies have largely focused on targeting specific metabolites. Studies exploring metabolome‐wide changes are lacking, and the effects of natural environmental variation and herbivory on the metabolomes of plants growing in situ remain unknown. An untargeted metabolomic approach using ultra‐high‐performance liquid chromatography–mass spectrometry, coupled with variation partitioning, general linear mixed modeling, and network analysis was used to detect differences in metabolic phenotypes of Plantago major in fifteen natural populations across Denmark. Geographic region, distance, habitat type, phenological stage, soil parameters, light levels, and leaf area were investigated for their relative contributions to explaining differences in foliar metabolomes. Herbivory effects were further investigated by comparing metabolomes from damaged and undamaged leaves from each plant. Geographic region explained the greatest number of significant metabolic differences. Soil pH had the second largest effect, followed by habitat and leaf area, while phenological stage had no effect. No evidence of the induction of metabolic features was found between leaves damaged by herbivores compared to undamaged leaves on the same plant. Differences in metabolic phenotypes explained by geographic factors are attributed to genotypic variation and/or unmeasured environmental factors that differ at the regional level in Denmark. A small number of specialized features in the metabolome may be involved in facilitating the success of a widespread species such as Plantago major into such wide range of environmental conditions, although overall resilience in the metabolome was found in response to environmental parameters tested. Untargeted metabolomic approaches have great potential to improve our understanding of how specialized plant metabolites respond to environmental change and assist in adaptation to local conditions.     

Plant chemistry and local adaptation of a specialized folivore

Local adaptation is central for creating and maintaining spatial variation in plant-herbivore interactions. Short-lived insect herbivores feeding on long-lived plants are likely to adapt to their local host plants, because of their short generation time, poor dispersal, and geographically varying selection due to variation in plant defences. In a reciprocal feeding trial, we investigated the impact of geographic variation in plant secondary chemistry of a long-lived plant, Vincetoxicum hirundinaria, on among-population variation in local adaptation of a specialist leaf-feeding herbivore, Abrostola asclepiadis. The occurrence and degree of local adaptation varied among populations. This variation correlated with qualitative and quantitative differences in plant chemistry among the plant populations. These findings provide insights into the mechanisms driving variation in local adaptation in this specialized plant-herbivore interaction.     

Selection Mosaic Exerted by Specialist and Generalist Herbivores on Chemical and Physical Defense of Datura stramonium

Selection exerted by herbivores is a major force driving the evolution of plant defensive characters such as leaf trichomes or secondary metabolites. However, plant defense expression is highly variable among populations and identifying the sources of this variation remains a major challenge. Plant populations are often distributed across broad geographic ranges and are exposed to different herbivore communities, ranging from generalists (that feed on diverse plant species) to specialists (that feed on a restricted group of plants). We studied eight populations of the plant Datura stramonium usually eaten by specialist or generalist herbivores, in order to examine whether the pattern of phenotypic selection on secondary compounds (atropine and scopolamine) and a physical defense (trichome density) can explain geographic variation in these traits. Following co-evolutionary theory, we evaluated whether a more derived alkaloid (scopolamine) confers higher fitness benefits than its precursor (atropine), and whether this effect differs between specialist and generalist herbivores. Our results showed consistent directional selection in almost all populations and herbivores to reduce the concentration of atropine. The most derived alkaloid (scopolamine) was favored in only one of the populations, which is dominated by a generalist herbivore. In general, the patterns of selection support the existence of a selection mosaic and accounts for the positive correlation observed between atropine concentration and plant damage by herbivores recorded in previous studies.     

Can plant resistance to specialist herbivores be explained by plant chemistry or resource use strategy?

At both a macro- and micro-evolutionary level, selection of and performance on host plants by specialist herbivores are thought to be governed partially by host plant chemistry. Thus far, there is little evidence to suggest that specialists can detect small structural differences in secondary metabolites of their hosts, or that such differences affect host choice or performance of specialists. We tested whether phytochemical differences between closely related plant species are correlated with specialist host choice. We conducted no-choice feeding trials using 17 plant species of three genera of tribe Senecioneae (Jacobaea, Packera, and Senecio; Asteraceae) and a more distantly related species (Cynoglossum officinale; Boraginaceae) containing pyrrolizidine alkaloids (PAs), and four PA-sequestering specialist herbivores of the genus Longitarsus (Chrysomelidae). We also assessed whether variation in feeding by specialist herbivores is attributable to different resource use strategies of the tested plant species. Plant resource use strategy was quantified by measuring leaf dry matter content, which is related to both plant nutritive value and to plant investment in quantitative defences. We found no evidence that intra-generic differences in PA profiles affect feeding by specialist herbivores. Instead, our results indicate that decisions to begin feeding are related to plant resource use strategy, while decisions to continue feeding are not based on any plant characteristics measured in this study. These findings imply that PA composition does not significantly affect host choice by these specialist herbivores. Leaf dry matter content is somewhat phylogenetically conserved, indicating that plants may have difficulty altering resource use strategy in response to selection pressure by herbivores and other environmental factors on an evolutionary time scale.     

Arbuscular mycorrhizal fungi influence life history traits of a lepidopteran herbivore

Results from pot and microcosm studies in the greenhouse have shown that plant growth and foliar chemistry is altered by the presence and species composition of arbuscular mycorrhizal fungi (AMF). The growth and survival of herbivores which feed on plants could, as a consequence, also be affected by these mutualistic soil fungi. Consequently, interactions between AMF, plants and herbivores could occur. To test this, larvae of the common blue butterfly, Polyommatus icarus (Lycaenidae), were fed with sprigs of Lotus corniculatus (Fabaceae) plants which were inoculated with one of two different AMF species, with a mixture of these AMF species or with sprigs of plants which were not inoculated with AMF. Survival and larval weight of third instar larvae fed with plants colonised by AMF were greater than those of larvae fed with non-mycorrhizal plants. Survival of larvae feeding on non-mycorrhizal plants was 1.6 times lower than that of larvae feeding on plants inoculated with a mixture of AMF species and 3.8 times lower than that of larvae feeding on plants inoculated with single AMF species. Furthermore, larvae fed with non-mycorrhizal plants attained only about half the weight of larvae fed with mycorrhizal plants after 11 days of growth. These differences in larval performance might be explained by differences in leaf chemistry, since mycorrhizal plants had a 3 times higher leaf P concentration and a higher C/N-ratio. Our results, thus, show that the presence of belowground mutualistic soil fungi influences the performance of aboveground herbivores by altering their food quality. Larval consumption, larval food use and adult lipid concentrations of the common blue butterfly differed between larvae which were fed with plants inoculated with different AMF species. This suggests that the performance of herbivores is not only influenced by the presence of AMF but also depends on the identity of the AMF species colonising the host plants. Moreover, a significant interaction term between AMF species and maternal identity of the larvae occurred for adult dry weight, indicating that the performance of offspring from different females was differently influenced by AMF species composition. To our knowledge, these results show for the first time that the species composition of AMF communities can influence life-history traits of butterfly larvae and possibly herbivores in general.     

Does the differential seedling mortality caused by slugs alter the foliar traits and subsequent susceptibility of hybrid willows to a generalist herbivore?

Abstract 1. Many Salicaceae species naturally form hybrid swarms with parental and hybrid taxa that differ in secondary chemical profile and in resistance to herbivores. Theoretically, the differential mortality in the seedling stage can lead to changes in trait expression and alter subsequent interactions between plants and herbivores. This study examines whether herbivory by the generalist slug Arion subfuscus, which causes extensive mortality in young willow seedlings, causes shifts in (a) the foliar chemistry of F2 willow hybrids (Salix sericea and Salix eriocephala), and (b) the subsequent susceptibility to Japanese Beetles, Popillia japonica. 2. In 2001, two populations of F2 seedlings were generated: those that survived slug herbivory (80–90% of seedlings placed in the field were killed by the slugs) were designated as S-plants, whereas C-plants (controls) experienced no mortality. 3. Common garden experiments with cuttings from these populations, in 2001 and 2002, revealed extensive variation in the phenolic chemistry of F2 hybrids, but revealed no significant difference between S- and C-plants, although the levels of foliar nutrients, proteins and nitrogen tended to be higher in S-plants. 4. Concentrations of salicortin and 2′-cinnamoylsalicortin explained 55 and 38% of the the variation in leaf damage caused by Japanese beetles, and secondary chemistry was highly correlated within replicate clones (salicortin R²= 0.85, 2-cinnamoylsalicortin R²= 0.77, condensed tannins R²= 0.68). 5. Interestingly, Japanese beetle damage and condensed tannins were positively correlated within the S-plants, but not in the C-plants, suggesting that slugs had selected for plants with a positive relationship between tannins and P. japonica damage. This is unlikely to be a consequence of a preference for tannins, but is suggested to be related to the elevated nutrient levels in the S-plants, perhaps in combination with the complex-binding properties of tannins. 6. The damage was highly correlated within replicate clones and a model choice analysis suggested that Japanese beetle damage may be explained by four factors: concentrations of salicortin, condensed tannins, and nitrogen, as well as the specific leaf area (thick leaves were damaged less).     

A quantitative evaluation of major plant defense hypotheses, nature versus nurture, and chemistry versus ants

Variation in plant secondary metabolite content can arise due to environmental and genetic variables. Because these metabolites are important in modifying a plant’s interaction with the environment, many studies have examined patterns of variation in plant secondary metabolites. Investigations of chemical defenses are often linked to questions about the efficacies of plant defenses and hypotheses on their evolution in different plant guilds. We performed a series of meta-analyses to examine the importance of environmental and genetic sources of variation in secondary metabolites as well as the antiherbivore properties of different classes of defense. We found both environmental and genetic variation affect secondary metabolite production, supporting continued study of the carbon-nutrient balance and growth-differentiation balance hypotheses. Defenses in woody plants are more affected by genetic variation, and herbaceous plant defenses are more influenced by environmental variation. Plant defenses in agricultural and natural systems show similar responses to manipulations, as do plants in laboratory, greenhouse, or field studies. What does such variation mean to herbivores? A comparison of biotic, physical, and chemical defenses revealed the most effective defensive strategy for a plant is biotic mutualisms with ants. Fast-growing plants are most often defended with qualitative defenses and slow-growing plants with quantitative defenses, as the plant apparency and resource availability hypotheses predict. However, we found the resource availability hypothesis provides the best explanation for the evolution of plant defenses, but the fact that there is considerable genetic and environmental variation in defenses indicates herbivores can affect plant chemistry in ecological and evolutionary time.     

Simultaneous inbreeding modifies inbreeding depression in a plant–herbivore interaction

Because inbreeding is common in natural populations of plants and their herbivores, herbivore‐induced selection on plants, and vice versa, may be significantly modified by inbreeding and inbreeding depression. In a feeding assay with inbred and outbred lines of both the perennial herb, Vincetoxicum hirundinaria, and its specialist herbivore, Abrostola asclepiadis, we discovered that plant inbreeding increased inbreeding depression in herbivore performance in some populations. The effect of inbreeding on plant resistance varied among plant and herbivore populations. The among‐population variation is likely to be driven by variation in plant secondary compounds across populations. In addition, inbreeding depression in plant resistance was substantial when herbivores were outbred, but diminished when herbivores were inbred. These findings demonstrate that in plant–herbivore interactions expression of inbreeding depression can depend on the level of inbreeding of the interacting species. Furthermore, our results suggest that when herbivores are inbred, herbivore‐induced selection against self‐fertilisation in plants may diminish.     

Variable responses of natural enemies to Salix triandra phenotypes with different secondary chemistry

Plant phenotypes often differ in their resistance to natural enemies, but the mechanism for this has seldom been identified. The aim of this study was to determine if the spatial patterns of phenotype use of a highly specialized insect herbivore (the galling sawfly Pontania triandrae ) in a natural willow population can be related to phenotypic variation in plant secondary chemistry. Furthermore, we tested if traits that confer resistance to one type of natural enemy, i.e. the galling sawfly, also confer resistance to others, in our case a leaf beetle Gonioctena linnaeana and the rust fungus Melampsora amygdalinae . We identified 18 phenotypes with high and 18 phenotypes with low gall density in our field population and determined gall densities, the degree of leaf damage and rust infection on each phenotype and collected leaves for chemical analyses. The concentration of phenolics was higher in phenotypes with high density of galls suggesting that this galling sawfly may use phenolics as oviposition cues. Rust infection showed the opposite pattern, with lower levels on clones with high concentration of phenolics, while leaf damage by G. linnaeana did not differ between clone types. This indicates that these important natural enemies may assert divergent selection on willow phenotypes and that this might provide a mechanism for maintaining phenotypic variation within willow populations.     

Chemical and Mechanical Defenses Vary among Maternal Lines and Leaf Ages in Verbascum thapsus L. (Scrophulariaceae) and Reduce Palatability to a Generalist Insect

Intra-specific variation in host-plant quality affects herbivore foraging decisions and, in turn, herbivore foraging decisions mediate plant fitness. In particular, variation in defenses against herbivores, both among and within plants, shapes herbivore behavior. If variation in defenses is genetically based, it can respond to natural selection by herbivores. We quantified intra-specific variation in iridoid glycosides, trichome length, and leaf strength in common mullein (Verbascum thapsus L, Scrophulariaceae) among maternal lines within a population and among leaves within plants, and related this variation to feeding preferences of a generalist herbivore, Trichopulsia ni Hübner. We found significant variation in all three defenses among maternal lines, with T. ni preferring plants with lower investment in chemical, but not mechanical, defense. Within plants, old leaves had lower levels of all defenses than young leaves, and were strongly preferred by T. ni. Caterpillars also preferred leaves with trichomes removed to leaves with trichomes intact. Differences among maternal lines indicate that phenotypic variation in defenses likely has a genetic basis. Furthermore, these results reveal that the feeding behaviors of T. ni map onto variation in plant defense in a predictable way. This work highlights the importance of variation in host-plant quality in driving interactions between plants and their herbivores.     

Geographic association and temporal variation of chemical and physical defense and leaf damage in Datura stramonium

The evolution of plant defense traits has traditionally been explained trough the “coevolutionary arms race” between plants and herbivores. According to this, specialist herbivores have evolved to cope effectively with the defensive traits of their host plants and may even use them as a cue for host location. We analyzed the geographic association between leaf trichomes, two tropane alkaloids (putative resistance traits), and leaf damage by herbivores in 28 populations of Datura stramonium in central Mexico. Since the specialist leaf beetles Epitrix parvula and Lema trilineata are the main herbivores of D. stramonium in central Mexico, we predicted a positive association between plant defense and leaf damage across populations. Also, if physical environmental conditions (temperature or precipitation) constrain the expression of plant defense, then the geographic variation in leaf damage should be explained partially by the interaction between defensive traits and environmental factors. Furthermore, we studied the temporal and spatial variation in leaf trichome density and leaf damage in five selected populations of D. stramonium sampled in two periods (1997 vs. 2007). We found a positive association between leaf trichomes density and atropine concentration with leaf damage across populations. The interaction between defensive traits and water availability in each locality had a significant effect on the geographic variation in leaf damage. Differences among populations in leaf trichome density are maintained over time. Our results indicate that local plant–herbivore interaction plays an important role in shaping the geographic and temporal variation in plant defense in D. stramonium.     

Seasonality and edge effect determine herbivory risk according to different plant association models

We report evidence of hierarchical resource selection by large herbivores and plant neighbouring effects in a Mediterranean ecosystem. Plant palatability was assessed according to herbivore foraging decisions. We hypothesize that under natural conditions large herbivores follow a hierarchical foraging pattern, starting at the landscape scale, and then selecting patches and individual plants. A between- and within-patch selection study was carried out in an area formed by scrubland and pasture patches, connected by habitat edges. With regard to between-patch selection, quality-dependent resource selection is reported: herbivores mainly consume pasture in spring and woody plants in winter. Within-patch selection was also observed in scrub habitats, influenced by season, relative patch palatability and edge effect. We defined a Proximity Index (PI) between palatable and unpalatable plants, which allowed verification of neighbouring effects. In spring, when the preferred food resource (i.e. herbs) is abundant, we observed that in habitat edges large herbivores basically select the relatively scarce palatable shrubs, whereas inside scrubland, unpalatable shrub consumption was related to increasing PI. In winter, a very different picture was observed; there was low consumption of palatable species surrounded by unpalatable species in habitat edges, where the latter were more abundant. These outcomes could be explained though different plant associations described in the literature. We conclude that optimal foraging theory provides a conceptual framework behind the observed interactions between plants and large herbivores in Mediterranean ecosystems.     

Food preference and performance of the larvae of a specialist herbivore: variation among and within host-plant populations

Specialist herbivores are suggested to be unaffected by or attracted to the defense compounds of their host-plants, and can even prefer higher levels of certain chemicals. Abrostola asclepiadis is a specialist herbivore whose larvae feed on the leaves of Vincetoxicum hirundinaria, which contains toxic alkaloids and is unpalatable to most generalist herbivores. The food choice, leaf consumption and growth of A. asclepiadis larvae were studied to determine whether there is variation among and within host-plant populations in their suitability for this specialist herbivore. There was significant variation in food preference and leaf consumption among host-plant populations, but no differences were found in larval growth and feeding on different host-plant populations. A. asclepiadis larvae preferred host-plant populations with higher alkaloid concentrations, but did not consume more leaf material from plants originating from such populations in a no-choice experiment. There was also some variation in food preference of larvae among host-plant individuals belonging to the same population, suggesting that there was variability in leaf chemistry also within populations. Such variation in larval preference among host-plant genotypes and populations may create potential for coevolutionary dynamics in a spatial mosaic.     

Relative importance of drought,soil quality,and plant species in determining the strength of plant–herbivore interactions

1. Although studies on plant–herbivore interactions comparing different plant species are common, little is known about the importance of environmental conditions in determining variation in herbivory within single plant species. 2. This study assessed the effects of experimentally manipulated nutrient and water availability on plant palatability, and compared these differences with differences among species. The extent to which these patterns can be explained by leaf toughness and specific leaf area was also investigated. Six plant species from the subfamily Carduoideae and four free‐living leaf chewing invertebrates were used in the study. 3. Herbivore preferences were significantly affected by soil nutrients and water regime and varied among plant as well as herbivore species. Generally, herbivores preferred watered plants and plants from nutrient‐poor soil. The effects of soil nutrients and water regime differed between the plant and herbivore species. The differences between the plant species were greater than those between the environmental treatments. Differences at both levels could be partly explained by leaf toughness and specific leaf area. Leaf toughness, in particular, turned to be an important predictor indicating that herbivores preferred species with softer leaves, and species from wetter conditions with reduced leaf toughness. 4. The environmental conditions in which plants are growing have significant effects on plant palatability. Between‐species comparisons thus need to pay attention to this variation. Future studies may consider how the effects of current conditions interact with conditions of plant origin to predict possible effects of changes in environmental conditions on the intensity of plant–herbivore interactions.     

Temporal consistency in herbivore responses to glucosinolate polymorphism in populations of wild cabbage (Brassica oleracea)

Natural populations of wild cabbage (Brassica oleracea) show significant qualitative diversity in heritable aliphatic glucosinolates, a class of secondary metabolites involved in defence against herbivore attack. One candidate mechanism for the maintenance of this diversity is that differential responses among herbivore species result in a net fitness balance across plant chemotypes. Such top-down differential selection would be promoted by consistent responses of herbivores to glucosinolates, temporal variation in herbivore abundance, and fitness impacts of herbivore attack on plants varying in glucosinolate profile. A 1-year survey across 12 wild cabbage populations demonstrated differential responses of herbivores to glucosinolates. We extended this survey to investigate the temporal consistency of these responses, and the extent of variation in abundance of key herbivores. Within plant populations, the aphid Brevicoryne brassicae consistently preferred plants producing the glucosinolate progoitrin. Among populations, increasing frequencies of sinigrin production correlated positively with herbivory by whitefly Aleyrodes proletella and negatively with herbivory by snails. Two Pieris butterfly species showed no consistent response to glucosinolates among years. Rates of herbivory varied significantly among years within populations, but the frequency of herbivory at the population scale varied only for B. brassicae. B. brassicae emerges as a strong candidate herbivore to impose differential selection on glucosinolates, as it satisfies the key assumptions of consistent preferences and heterogeneity in abundance. We show that variation in plant secondary metabolites structures the local herbivore community and that, for some key species, this structuring is consistent over time. We discuss the implications of these patterns for the maintenance of diversity in plant defence chemistry.     

Chemical ecology of host-plant selection by herbivorous arthropods: a multitrophic perspective

Most herbivorous arthropods are specialists that feed on one or a few related plant species. To understand why this is so, both mechanistic and functional studies have been carried out, predominantly restricted to bitrophic aspects. Host-selection behaviour of herbivorous arthropods has been intensively studied and this has provided ample evidence for the role of secondary plant chemicals as source of information in behavioural decisions of herbivores. Many evolutionary studies have regarded co-evolution between plants and herbivores to explain the diversity of secondary plant chemicals and host specialisation of herbivores. However, many cases remain unexplained where herbivores select host plants that are suboptimal in terms of fitness returns. A stimulating paper by Bernays and Graham [(1988) Ecology 69, 886-892)] has initiated a discussion on the need of a multitrophic perspective to understand the evolution of host-plant specialisation by herbivorous arthropods. However, this has hardly resulted in ecological studies on host-selection behaviour that take a multitrophic perspective. Yet, evidence is accumulating that constitutive and induced infochemicals from natural enemies and competitors can affect herbivore behaviour. These cues may constitute important information on fitness prospects, just as plant cues can do. In this paper I selectively review how information from organisms at different trophic levels varies in space and time and how herbivores can integratively exploit this information during host selection. In doing so, research areas are identified that are likely to provide important new insights to explain several of the questions in herbivore host selection that remain unanswered so far. These research areas are at the interface of evolutionary ecology, behavioural ecology and chemical ecology.     

Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study

1.  There are myriad ways in which pollinators and herbivores can interact via the evolutionary and behavioural responses of their host plants.
2.  Given that both herbivores and pollinators consume and are dependent upon plant-derived nutrients and secondary metabolites, and utilize plant signals, plant chemistry should be one of the major factors mediating these interactions.
3.  Here we build upon a conceptual framework for understanding plant-mediated interactions of pollinators and herbivores. We focus on plant chemistry, in particular plant volatiles and aim to unify hypotheses for plant defence and pollination. We make predictions for the evolutionary outcomes of these interactions by hypothesizing that conflicting selection pressures from herbivores and pollinators arise from the constraints imposed by plant chemistry.
4.  We further hypothesize that plants could avoid conflicts between pollinator attraction and herbivore defence through tissue-specific regulation of pollinator reward chemistry, as well as herbivore-induced changes in flower chemistry and morphology.
5.  Finally, we test aspects of our predictions in a case study using a wild tomato species, Solanum peruvianum , to illustrate the diversity of tissue-specific and herbivore-induced differences in plant chemistry that could influence herbivore and pollinator behaviour, and plant fitness.