Tolerance to deer herbivory and resistance to insect herbivores in the common evening primrose (Oenothera biennis)

The evolution of plant defence in response to herbivory will depend on the fitness effects of damage, availability of genetic variation and potential ecological and genetic constraints on defence. Here, we examine the potential for evolution of tolerance to deer herbivory in Oenothera biennis while simultaneously considering resistance to natural insect herbivores. We examined (i) the effects of deer damage on fitness, (ii) the presence of genetic variation in tolerance and resistance, (iii) selection on tolerance, (iv) genetic correlations with resistance that could constrain evolution of tolerance and (v) plant traits that might predict defence. In a field experiment, we simulated deer damage occurring early and late in the season, recorded arthropod abundances, flowering phenology and measured growth rate and lifetime reproduction. Our study showed that deer herbivory has a negative effect on fitness, with effects being more pronounced for late‐season damage. Selection acted to increase tolerance to deer damage, yet there was low and nonsignificant genetic variation in this trait. In contrast, there was substantial genetic variation in resistance to insect herbivores. Resistance was genetically uncorrelated with tolerance, whereas positive genetic correlations in resistance to insect herbivores suggest there exists diffuse selection on resistance traits. In addition, growth rate and flowering time did not predict variation in tolerance, but flowering phenology was genetically correlated with resistance. Our results suggest that deer damage has the potential to exert selection because browsing reduces plant fitness, but limited standing genetic variation in tolerance is expected to constrain adaptive evolution in O. biennis.     

Genetic variation in herbivore resistance and tolerance: the role of plant life‐history stage and type of damage

Information of the patterns of genetic variation in plant resistance and tolerance against herbivores and genetic trade‐offs between these two defence strategies is central for our understanding of the evolution of plant defence. We found genetic variation in resistance to two specialist herbivores and in tolerance to artificial damage but not to a specialist leaf herbivore in a long‐lived perennial herb. Seedlings tended to have genetic variation in tolerance to artificial damage. Genetic variation in tolerance of adult plants to artificial damage was not consistent in time. Our results suggest that the level of genetic variation in tolerance and resistance depends on plant life‐history stage, type of damage and timing of estimating the tolerance relative to the occurrence of the damage, which might reflect the pattern of selection imposed by herbivory. Furthermore, we found no trade‐offs between resistance and tolerance, which suggests that the two defence strategies can evolve independently.     

Mechanisms of tolerance to herbivore damage:what do we know?

Identifying mechanisms of tolerance to herbivore damage will facilitate attempts to understand the role of tolerance in the evolutionary and ecological dynamics of plants and herbivores. Investigations of the physiological and morphological changes that occur in plants in response to herbivore damage have identified several potential mechanisms of tolerance. However, it is unlikely that all physiological changes that occur following damage are tolerance mechanisms. Few studies have made direct comparisons between the expression of tolerance and the relative expression of putative mechanisms. I briefly review empirical evidence for some of the better-studied potential mechanisms, including increased photosynthetic activity, compensatory growth, utilization of stored reserves, and phenological delays. For each of these mechanisms I discuss reasons why the relationship between tolerance and these characters may be more complicated than it first appears. I conclude by discussing several empirical approaches, including herbivore manipulations, quantitative trait loci (QTL) analysis, and selection experiments, that will further our understanding of tolerance mechanisms. This revised version was published online in July 2006 with corrections to the Cover Date.     

How do plants “notice” attack by herbivorous arthropods?

Precise and deep comprehension of plant responses to herbivorous arthropods requires detailed knowledge of how a plant “notices” the attack. Herbivore attack is not restricted to plant wounding by feeding, but instead different phases of attack that elicit a plant response need to be distinguished: touch, oviposition and feeding. Touch, secretions released with eggs and regurgitate delivered during feeding may act in concert as elicitors of plant defence. Here, we discuss the current knowledge of what a plant “notices” during the different phases of herbivore attack and how it responds at the molecular, physiological and ecological level. Understanding the mechanisms of plant responses to the different phases of herbivore attack will be a key challenge in unravelling the complex communication pathways between plants and herbivores.     

The dilemma of foraging herbivores: dealing with food and fear

For foraging herbivores, both food quality and predation risk vary across the landscape. Animals should avoid low-quality food patches in favour of high-quality ones, and seek safe patches while avoiding risky ones. Herbivores often face the foraging dilemma, however, of choosing between high-quality food in risky places or low-quality food in safe places. Here, we explore how and why the interaction between food quality and predation risk affects foraging decisions of mammalian herbivores, focusing on browsers confronting plant toxins in a landscape of fear. We draw together themes of plant–herbivore and predator–prey interactions, and the roles of animal ecophysiology, behaviour and personality. The response of herbivores to the dual costs of food and fear depends on the interplay of physiology and behaviour. We discuss detoxification physiology in dealing with plant toxins, and stress physiology associated with perceived predation risk. We argue that behaviour is the interface enabling herbivores to stay or quit food patches in response to their physiological tolerance to these risks. We hypothesise that generalist and specialist herbivores perceive the relative costs of plant defence and predation risk differently and intra-specifically, individuals with different personalities and physiologies should do so too, creating individualised landscapes of food and fear. We explore the ecological significance and emergent impacts of these individual-based foraging outcomes on populations and communities, and offer predictions that can be clearly tested. In doing so, we provide an integrated platform advancing herbivore foraging theory with food quality and predation risk at its core.     

Cascading effects of induced terrestrial plant defences on aquatic and terrestrial ecosystem function

Herbivores induce plants to undergo diverse processes that minimize costs to the plant, such as producing defences to deter herbivory or reallocating limited resources to inaccessible portions of the plant. Yet most plant tissue is consumed by decomposers, not herbivores, and these defensive processes aimed to deter herbivores may alter plant tissue even after detachment from the plant. All consumers value nutrients, but plants also require these nutrients for primary functions and defensive processes. We experimentally simulated herbivory with and without nutrient additions on red alder (Alnus rubra), which supplies the majority of leaf litter for many rivers in western North America. Simulated herbivory induced a defence response with cascading effects: terrestrial herbivores and aquatic decomposers fed less on leaves from stressed trees. This effect was context dependent: leaves from fertilized-only trees decomposed most rapidly while leaves from fertilized trees receiving the herbivory treatment decomposed least, suggesting plants funnelled a nutritionally valuable resource into enhanced defence. One component of the defence response was a decrease in leaf nitrogen leading to elevated carbon : nitrogen. Aquatic decomposers prefer leaves naturally low in C : N and this altered nutrient profile largely explains the lower rate of aquatic decomposition. Furthermore, terrestrial soil decomposers were unaffected by either treatment but did show a preference for local and nitrogen-rich leaves. Our study illustrates the ecological implications of terrestrial herbivory and these findings demonstrate that the effects of selection caused by terrestrial herbivory in one ecosystem can indirectly shape the structure of other ecosystems through ecological fluxes across boundaries.     

The adaptation of insects to plant protease inhibitors

Plants and herbivores have been co-evolving for thousands of years, and as a result, plants have defence mechanisms that offer protection against many herbivores such as nematodes, insects, birds and mammals. Only when a herbivore has managed to adapt to these defence mechanisms does it have the potential to become a pest. One such method of plant defence involves the production of protease inhibitors (PIs). These inhibitors are proteins that may be found constitutively in various parts of the plant, or may be induced in response to herbivore attack. PIs work at the gut level, by inhibiting the digestion of plant protein. This review focuses on insect herbivores and looks at the mechanisms involved in the role and function of PIs in plant defense against insects, as well as at the ability of well adapted species to overcome the effects of these plant PIs.     

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.     

Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids

Direct and indirect plant defences are well studied, particularly in the Brassicaceae. Glucosinolates (GS) are secondary plant compounds characteristic in this plant family. They play an important role in defence against herbivores and pathogens. Insect herbivores that are specialists on brassicaceous plant species have evolved adaptations to excrete or detoxify GS. Other insect herbivores may even sequester GS and employ them as defence against their own antagonists, such as predators. Moreover, high levels of GS in the food plants of non-sequestering herbivores can negatively affect the growth and survival of their parasitoids. In addition to allelochemicals, plants produce volatile chemicals when damaged by herbivores. These herbivore induced plant volatiles (HIPV) have been demonstrated to play an important role in foraging behaviour of insect parasitoids. In addition, biosynthetic pathways involved in the production of HIPV are being unraveled using the model plant Arabidopsis thialiana. However, the majority of studies investigating the attractiveness of HIPV to parasitoids are based on experiments mainly using crop plant species in which defence traits may have changed through artificial selection. Field studies with both cultivated and wild crucifers, the latter in which defence traits are intact, are necessary to reveal the relative importance of direct and indirect plant defence strategies on parasitoid and plant fitness. Future research should also consider the potential conflict between direct and indirect plant defences when studying the evolution of plant defences against insect herbivory.     

Rethinking the role of many plant phenolics – protection from photodamage not herbivores?

Phenolics have been considered classic defence compounds for protecting plants from herbivores, ever since plant secondary metabolites were suggested to have evolved for that reason. The resource availability and carbon-nutrient balance hypotheses proposed that variation in phenolic levels between and within plant species reflects environmental availability of nutrients and light, and represents a trade-off in allocation by plants to growth and defence against herbivores. In contrast to these concepts, we suggest that (1) the main role of many plant phenolics may be to protect leaves from photodamage, not herbivores; (2) they can achieve this by acting as antioxidants; and (3) their levels may vary with environmental conditions in order to counteract this potential photodamage. We therefore suggest that patterns in phenolic levels, often used to support the concept of trade-off between growth and herbivore defence in relation to resource availability, may actually reflect different risks of photodamage. We suggest that the level of many phenolics is low under some environmental conditions, not because resources to produce them are limited, but simply because the risk of photodamage is low and they are not required. If our photodamage hypothesis is correct, a reassessment of the ecological and evolutionary role of many phenolics in plant defence theory is required.     

Future directions in the ontogeny of plant defence: understanding the evolutionary causes and consequences

Plant defence often varies by orders of magnitude as plants develop from the seedling to juvenile to mature and senescent stages. Ontogenetic trajectories can involve switches among defence traits, leading to complex shifting phenotypes across plant lifetimes. While considerable research has characterised ontogenetic trajectories for now hundreds of plant species, we still lack a clear understanding of the molecular, ecological and evolutionary factors driving these patterns. In this study, we identify several non‐mutually exclusive factors that may have led to the evolution of ontogenetic trajectories in plant defence, including developmental constraints, resource allocation costs, multi‐functionality of defence traits, and herbivore selection pressure. Evidence from recent physiological studies is highlighted to shed light on the underlying molecular mechanisms involved in the regulation and activation of these developmental changes. Overall, our goal is to promote new research avenues that would provide evidence for the factors that have promoted the evolution of this complex lifetime phenotype. Future research focusing on the questions and approaches identified here will advance the field and shed light on why defence traits shift so dramatically across plant ontogeny, a widespread but poorly understood ecological pattern.     

Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities

Background Plants are hotbeds for parasites such as arthropod herbivores, which acquire nutrients and energy from their hosts in order to grow and reproduce. Hence plants are selected to evolve resistance, which in turn selects for herbivores that can cope with this resistance. To preserve their fitness when attacked by herbivores, plants can employ complex strategies that include reallocation of resources and the production of defensive metabolites and structures. Plant defences can be either prefabricated or be produced only upon attack. Those that are ready-made are referred to as constitutive defences. Some constitutive defences are operational at any time while others require activation. Defences produced only when herbivores are present are referred to as induced defences. These can be established via de novo biosynthesis of defensive substances or via modifications of prefabricated substances and consequently these are active only when needed. Inducibility of defence may serve to save energy and to prevent self-intoxication but also implies that there is a delay in these defences becoming operational. Induced defences can be characterized by alterations in plant morphology and molecular chemistry and are associated with a decrease in herbivore performance. These alterations are set in motion by signals generated by herbivores. Finally, a subset of induced metabolites are released into the air as volatiles and function as a beacon for foraging natural enemies searching for prey, and this is referred to as induced indirect defence.Scope The objective of this review is to evaluate (1) which strategies plants have evolved to cope with herbivores and (2) which traits herbivores have evolved that enable them to counter these defences. The primary focus is on the induction and suppression of plant defences and the review outlines how the palette of traits that determine induction/suppression of, and resistance/susceptibility of herbivores to, plant defences can give rise to exploitative competition and facilitation within ecological communities “inhabiting” a plant.Conclusions Herbivores have evolved diverse strategies, which are not mutually exclusive, to decrease the negative effects of plant defences in order to maximize the conversion of plant material into offspring. Numerous adaptations have been found in herbivores, enabling them to dismantle or bypass defensive barriers, to avoid tissues with relatively high levels of defensive chemicals or to metabolize these chemicals once ingested. In addition, some herbivores interfere with the onset or completion of induced plant defences, resulting in the plant’s resistance being partly or fully suppressed. The ability to suppress induced plant defences appears to occur across plant parasites from different kingdoms, including herbivorous arthropods, and there is remarkable diversity in suppression mechanisms. Suppression may strongly affect the structure of the food web, because the ability to suppress the activation of defences of a communal host may facilitate competitors, whereas the ability of a herbivore to cope with activated plant defences will not. Further characterization of the mechanisms and traits that give rise to suppression of plant defences will enable us to determine their role in shaping direct and indirect interactions in food webs and the extent to which these determine the coexistence and persistence of species.     

Defence on demand: mechanisms behind optimal defence patterns

Background

The optimal defence hypothesis (ODH) predicts that tissues that contribute most to a plant''s fitness and have the highest probability of being attacked will be the parts best defended against biotic threats, including herbivores. In general, young sink tissues and reproductive structures show stronger induced defence responses after attack from pathogens and herbivores and contain higher basal levels of specialized defensive metabolites than other plant parts. However, the underlying physiological mechanisms responsible for these developmentally regulated defence patterns remain unknown.

Scope

This review summarizes current knowledge about optimal defence patterns in above- and below-ground plant tissues, including information on basal and induced defence metabolite accumulation, defensive structures and their regulation by jasmonic acid (JA). Physiological regulations underlying developmental differences of tissues with contrasting defence patterns are highlighted, with a special focus on the role of classical plant growth hormones, including auxins, cytokinins, gibberellins and brassinosteroids, and their interactions with the JA pathway. By synthesizing recent findings about the dual roles of these growth hormones in plant development and defence responses, this review aims to provide a framework for new discoveries on the molecular basis of patterns predicted by the ODH.

Conclusions

Almost four decades after its formulation, we are just beginning to understand the underlying molecular mechanisms responsible for the patterns of defence allocation predicted by the ODH. A requirement for future advances will be to understand how developmental and defence processes are integrated.     

Herbivores and plant defences affect selection on plant reproductive traits more strongly than pollinators

Pollinators and herbivores can both affect the evolutionary diversification of plant reproductive traits. However, plant defences frequently alter antagonistic and mutualistic interactions, and therefore, variation in plant defences may alter patterns of herbivore‐ and pollinator‐mediated selection on plant traits. We tested this hypothesis by conducting a common garden field experiment using 50 clonal genotypes of white clover (Trifolium repens) that varied in a Mendelian‐inherited chemical antiherbivore defence—the production of hydrogen cyanide (HCN). To evaluate whether plant defences alter herbivore‐ and/or pollinator‐mediated selection, we factorially crossed chemical defence (25 cyanogenic and 25 acyanogenic genotypes), herbivore damage (herbivore suppression) and pollination (hand pollination). We found that herbivores weakened selection for increased inflorescence production, suggesting that large displays are costly in the presence of herbivores. In addition, herbivores weakened selection on flower size but only among acyanogenic plants, suggesting that plant defences reduce the strength of herbivore‐mediated selection. Pollinators did not independently affect selection on any trait, although pollinators weakened selection for later flowering among cyanogenic plants. Overall, cyanogenic plant defences consistently increased the strength of positive directional selection on reproductive traits. Herbivores and pollinators both strengthened and weakened the strength of selection on reproductive traits, although herbivores imposed ~2.7× stronger selection than pollinators across all traits. Contrary to the view that pollinators are the most important agents of selection on reproductive traits, our data show that selection on reproductive traits is driven primarily by variation in herbivory and plant defences in this system.     

On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds

Species comparisons are a cornerstone of biology and there is a long tradition of using the comparative framework to study the ecology and evolution of plant defensive traits. Early comparative studies led to the hypothesis that plant chemistry plays a central role in plant defence, and the evolution of plant secondary chemistry in response to insect herbivory remains a classic example of coevolution. However, recent comparative work has disagreed with this paradigm, reporting little connection between plant secondary chemicals and herbivory across distantly related plant taxa. One conclusion of this new work is that the importance of secondary chemistry in plant defence may have been generally overstated in earlier research. Here, we attempt to reconcile these contradicting viewpoints on the role of plant chemistry in defence by critically evaluating the use and interpretation of species correlations as a means to study defence–herbivory relationships. We conclude that the notion that plant primary metabolites (e.g. leaf nitrogen content) are the principal determinants of herbivory (or the target of natural selection by herbivores) is not likely to be correct. Despite the inference of recent community‐wide studies of herbivory, strong evidence remains for a prime role of secondary compounds in plant defence against herbivores.     

The unfolding of plant growth form‐defence syndromes along elevation gradients

Understanding the functional economics that drives plant investment of resources requires investigating the interface between plant phenotypes and the variation in ecological conditions. While allocation to defence represents a large portion of the carbon budget, this axis is usually neglected in the study of plant economic spectrum. Using a novel geometrical approach, we analysed the co‐variation in a comprehensive set of functional traits related to plant growth strategies, as well as chemical defences against herbivores on all 15 Cardamine species present in the Swiss Alps. By extracting geometrical information of the functional space, we observed clustering of plants into three main syndromes. Those different strategies of growth form and defence were also distributed within distinct elevational bands demonstrating an association between the functional space and the ecological conditions. We conclude that plant strategies converge into clear syndromes that trade off abiotic tolerance, growth and defence within each elevation zone.     

The jasmonic acid-amino acid conjugates JA-Val and JA-Leu are involved in rice resistance to herbivores

The phytohormone jasmonic acid (JA) plays a core role in plant defence against herbivores. When attacked by herbivores, JA and its bioactive derivatives are accumulated at the damage site, and subsequently perceived by the jasmonate co-receptors COI1 and JAZ proteins. The (+)-7-iso-jasmonoyl-L-isoleucine (JA-Ile) is known to be the main active JA derivative controlling vascular plant responses to herbivores as well as other JA-regulated processes. However, whether other endogenous JA-amino acid conjugates (JA-AAs) are involved in herbivore-induced defence responses remain unknown. Here, we investigated the role of herbivore-elicited JA-AAs in the crop plant rice. The levels of five JA-AAs were significantly increased under the armyworm, leaf folder and brown planthopper attack. Of the elicited JA derivatives, JA-Ile, JA-Val and JA-Leu could serve as ligands to promote the interaction between rice COI1 and JAZs, inducing OsJAZ4 degradation in vivo. JA-Val or JA-Leu treatment increased the expression of JA- and defence-related pathway genes but not JA-Ile levels, suggesting that these JA-AAs may directly function in JA signalling. Furthermore, the application of JA-Val or JA-Leu resulted in JA-mediated plant growth inhibition, while enhancing plant resistance to herbivore attack. This study uncovers that JA-Val and JA-Leu also play a role in rice defence against herbivores.     

Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens

Plants frequently suffer attack from herbivores and microbial pathogens, and have evolved a complex array of defence mechanisms to resist defoliation and disease. These include both preformed defences, ranging from structural features to stores of toxic secondary metabolites, and inducible defences, which are activated only after an attack is detected. It is well known that plant defences against pests and pathogens are commonly affected by environmental conditions, but the mechanisms by which responses to the biotic and abiotic environments interact are only poorly understood. In this review, we consider the impact of light on plant defence, in terms of both plant life histories and rapid scale molecular responses to biotic attack. We bring together evidence that illustrates that light not only modulates defence responses via its influence on biochemistry and plant development but, in some cases, is essential for the development of resistance. We suggest that the interaction between the light environment and plant defence is multifaceted, and extends across different temporal and biological scales.     

The resource regulation hypothesis and positive feedback loops in plant–herbivore interactions

Resource regulation occurs when herbivory maintains or increases plant susceptibility to further herbivory by the same species. A review of the literature indicates it is a widespread plant–animal interaction involving a diverse array of herbivores. At least three mechanisms can produce this positive feedback cycle. First, phytophagous insect and mammalian herbivore damage can stimulate dormant buds to produce vigorous juvenile growth, which is preferred for further attack. Juvenilization cycles may have repeatedly evolved because herbivores are able to take advantage of a generalized plant compensatory response to any type of damage. Second, herbivores can manipulate plant source–sink relationships to attain more resources, and this alteration of plant growth may benefit subsequent herbivore generations. Third, herbivory can alter plant nutrition or defensive chemistry in a way that makes a plant susceptible to more herbivory. Resource regulation probably occurs because damage to resources preferred by the herbivores induces a generalized plant response that produces more preferred resources. Alternatively, manipulation of plant resources to induce resource regulation may have evolved in herbivores with a high degree of philopatry due to selection to alter plant resources to benefit their offspring. Resource regulation can stabilize insect population dynamics by maintaining a supply of high-quality plant resources. It can also increase the heterogeneity of host-plant resources for herbivores by altering the physiological age structure and the distribution of resources within plants. Resource regulation may have strong plant-mediated effects on other organisms that use that host plant, but these effects have not yet been explored.