A Framework for Predicting Intraspecific Variation in Plant Defense

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Review

A Framework for Predicting Intraspecific Variation in Plant Defense Philip G. Hahn1,* and John L. Maron1 One of the most well-supported theories regarding the evolution of plant defenses is the resource availability hypothesis (RAH). RAH posits that species from high-resource environments grow fast and allocate little to herbivoreresistance traits, whereas those species in low-resource environments grow slow and are highly resistant to herbivores. However, within species, how resources influence defense is unclear and existing theories make opposing predictions. Here, we review studies documenting intraspecific variation in plant defense across resource gradients and find little support for RAH. We outline why RAH does not apply intraspecifically and present a predictive framework for understanding how resources influence intraspecific variation in plant defense. Our framework provides an important step towards reconciling inter- versus intraspecific strategies of defense. Effects of Resource Availability on Plant Growth and Defense: An Overview Herbivores remove substantial amounts of plant tissue in many ecosystems and can negatively affect plant fitness and abundance [1,2]. In response, plants have evolved myriad physical and chemical defenses (see Glossary) to thwart or reduce the deleterious impacts of herbivore attack [3–5]. However, abiotic factors (e.g., climate, nutrients, or light) also exert strong selective pressures on plants and both biotic and abiotic factors likely act in combination to shape plant defensive traits [6–9]. One of the most prominent theories regarding how the abiotic environment influences the evolution of plant defenses against herbivores is the RAH [10]. This theory posits that highresource environments select for faster growth rates and allocation of resources to regrowth at the expense of investment in herbivore resistance. By contrast, low-resource environments dictate slow plant growth rates, but enhanced herbivore resistance because tissue loss to herbivores is costly to replace [10] (Figure 1A). RAH was originally developed to describe interspecific patterns of plant constitutive resistance traits and this theory has enjoyed widespread empirical support in both tropical and temperate ecosystems [11–13]. As such, the RAH serves as a compelling framework for understanding how variation in the resource environment underpins patterns of plant constitutive resistance among species [12]. Due to its intuitively appealing predictions, RAH has frequently been invoked to predict intraspecific patterns of plant resistance across ecological gradients or to describe plastic responses of plants to fluctuating resources [12,14]. To date, there has been no formal evaluation of the degree to which RAH might apply to intraspecific patterns of plant growth and defense across environmental gradients. Just as variation in the abiotic environment can influence interspecific patterns of plant resistance [10,15,16], there is ample scope for variation in

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Trends Intraspecific patterns of plant growth rates across resource gradients are consistent with predictions of theory developed to describe interspecific patterns (RAH). However, constitutive levels of herbivore resistance across resource gradients differ from those predicted by RAH. Furthermore, within species, there is little evidence for genetically based tradeoffs between growth and resistance. Both often covary positively with resource availability. Resource availability may have independent indirect effects on different components of plant defense; tolerance is affected by constraints set by resources on growth rates or physiological traits, whereas the effect of resources on resistance is mediated through variation in herbivore pressure that occurs across gradients. Ecological constraints that shape the growth–resistance tradeoff among species may help predict when such tradeoffs might be found within species. Species that evolve in low-resource environments may be constrained by growth to exhibit intraspecific growth– resistance tradeoffs, whereas species that evolve in high-resource environments may have more inherent capability for allocating to both growth and resistance across resource gradients. Common garden experiments established at multiple locations across resource gradients are needed to fully disentangle genetic and plastic responses of plant defenses to abiotic and biotic factors that vary across plant distributions.

http://dx.doi.org/10.1016/j.tree.2016.05.007 © 2016 Elsevier Ltd. All rights reserved.

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(A) RAHinter

(B)

Figure 1. Framework for Understanding the Evolution of Intraspecific Plant Growth and Defense along Resource Gradients. Arrows indicate

RAHintra

Resistance

Tolerance

Inducibility

Defense Resistance

Constuve

– Growth rate

+

+ Growth or physiological traits

+ Resource availability

Herbivore pressure

+

+

Resource availability

direct (+ or–) effects. (A) Schematic of the resource availability hypothesis (RAHinter). (B) Schematic of intraspecific variation in plant defense (RAHintra). Resource availability affects the components of plant defenses (tolerance and resistance) through different pathways; the effect on tolerance is mediated through plant growth rate or other physiological traits, whereas the effect of resource availability on constitutive resistance is mediated through herbivore pressure. Note that constitutive resistance and inducibility should trade off, such that constitutive resistances are expected in highresource environments and induced defenses are expected in low-resource environments.

environmental conditions to drive intraspecific variation in plant defense. The distributions of many species span steep environmental gradients [17] and there can be considerable intraspecific variation in plant defensive traits. For example, leaf phenolics in the species Pinus pinaster varied approximately 1.5-fold among 33 genetic families grown in a common environment [18], whereas mean phenolics varied by approximately 4.5-fold among 18 species of Pinus [16]. Similarly, latex production in 22 populations of Asclepias syriaca varied nearly sixfold [9], which was about half the variation among 38 species of Asclepias [19]. Clines in plant growth and defense can occur across relatively small spatial scales, such as a few degrees of latitude [20] or a few hundred meters in elevation [6]. Whether abiotic processes that govern macroevolutionary patterns in herbivore resistance among species drive similar patterns within species has not been well quantified [21,22]. In fact, existing theories that predict how the environment should influence intraspecific patterns of plant damage and defense are often contradictory (Table 1), clouding our basic ability to understand how variation in abiotic conditions might influence herbivore impacts on plants [23]. In this paper, we review the literature that deals with intraspecific variation in plant defense against herbivores. Although phenotypic changes in plant traits in response to resource pulses

Table 1. Hypotheses that Describe Intraspecific Variation in Plant Defense Hypothesis

Prediction for Defense Levels (Resistance or Tolerance) in High-Resource Environments

Refs

Carbon–nutrient balance hypothesis

Mixed

[85]

Compensatory continuum model

High

[86]

Defense–stress benefit hypothesis

High

[87]

Defense–stress cost hypothesis

Low

[87]

Differential growth rate hypothesis

Low

[88]

Growth–differentiation balance hypothesis

Low

[34]

Plant stress hypothesis

High

[89]

Plant vigor hypothesis

Low

[67]

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1 Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA

*Correspondence: [email protected] (P.G. Hahn).

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can have important influences on plant defense [24–26], here we are concerned with how resource availability might influence genetically based population-level variation in plant defense. We ask whether predictions from the RAH regarding differences among species might apply to intraspecific variation among plant populations in[1_TD$IF] growth and defense. More specifically, we ask whether high-resource environments, compared with low-resource environments select for: (i) faster-growing plants; and (ii) reduced constitutive resistance, increased tolerance, and higher inducibility of resistance traits. Tolerance and inducible resistance were implicitly part of the RAH [10,27] and we include them because they are important components of plant defense that have recently been explicitly tested under RAH [13,16,28]. We also evaluate whether variation in herbivore pressure across resource gradients might drive intraspecific patterns of plant growth and defense. Implicit to the above predictions, but often untested, are: (i) a positive relation between growth and tolerance; (ii) a tradeoff between tolerance and constitutive resistance; (iii) a tradeoff between constitutive resistance and inducibility; and (iv) a positive relation between tolerance and induced resistance [10,27]. We then develop a framework for understanding the factors that likely drive genetically based among-population variation in plant defenses. We conclude by outlining experimental designs best able to test our framework and by summarizing some central unanswered questions.

Effects of Resource Availability on Intraspecific Variation in Plant Growth and Defense: A Synthesis of the Literature We reviewed the small but growing literature focusing on intraspecific variation in plant growth and defense across resource gradients. To test whether the main predictions of the RAH apply within species, we searched for studies that measured intraspecific variation in plant growth and defense among genotypes sampled across an identified resource gradient that were grown in a common environment. In other words, we searched for studies that quantified genetically based variation in plant growth and defense that corresponded with variation in the resource environment. Although observational studies of plant–insect interactions across gradients can provide some insight into how resources shape plant defense (Box 1), we restricted our synthesis to common garden studies because we were interested in how environmental gradients influence genetically based variation in plant growth and defense rather than plastic responses. Furthermore, these studies are methodologically parallel to the most robust interspecific tests of RAH, which were also conducted under common environmental conditions or using reciprocal transplant experiments (e.g., [11,13,16]). For our synthesis, we relied on the author's descriptions of resource availability for their study system. However, we note that resources identified within particular studies might not be those that are most limiting and, therefore, may not affect plant fitness or allocation of resources to defense. It is important to consider the limiting resources and how herbivores can affect the ability of a plant to acquire resources, because these could differ among habitats and species [29,30].

Glossary Cline: a trait (growth, defense, etc.) that correlates with an environmental gradient. Common garden: an experimental approach that controls for environmental variation and tests for genetic differentiation in traits among populations. This involves rearing two or more genotypes or populations in a common environment. Defense: plant traits that reduce negative fitness impacts of herbivores, which can include both tolerance and resistance. Inducibility: a change in levels of resistance traits in response to herbivory, measured as the difference between resistance traits present in undamaged minus damaged plant relatives. Interspecific: among species. Intraspecific: within a species. Local adaptation: evolutionary process that increases fitness by bringing the phenotypes of a population in closer correspondence with its local environment. Reciprocal transplant: a type of common garden experiment in which individuals from different populations are reared in their own environment and the environment of the other population(s). Resistance: a trait that is a component of plant defense that reduces herbivore attacks, herbivore performance, or herbivore damage. Constitutive resistances are levels of a resistant trait that are always expressed. Tolerance: a plant trait that reduces the negative impact of a given amount of herbivore damage on fitness, relative to an undamaged plant.

We found 20 such studies (four did not measure growth rate) that were published since RAH (see Table S1 in the supplemental information online). Gradients studied included latitude (n = 11), precipitation (n = 5), elevation (n = 4), temperature (n = 1), and day length (n = 1). For latitudinal studies that did not provide additional climate information with regards to latitude, we assumed that resources decreased with latitude since all reviewed studies came from temperate systems. For elevation studies, we assumed higher resource availability at lower elevations [31]. Most studies examined herbaceous plants species (n = 14 studies), although six examined woody species. Most studies quantified chemical (n = 13) or physical (n = 7) resistance traits or conducted a bioassay or choice experiment with live herbivores (n = 12), whereas only four studies had estimates of induced resistance and only two study directly quantified tolerance. Most studies were conducted in controlled greenhouse conditions and had no estimate of natural herbivore damage (n = 11).

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Box 1. Observational Studies on Plant–Herbivore Interactions Observational studies examining intraspecific variation in plant–herbivore interactions have largely focused on patterns of herbivore damage across latitudinal gradients (e.g., [90,91]) or, to a lesser degree, across elevation [92]. Considerably fewer studies have examined latitudinal [93,94] or elevational [31] patterns in plant defense. Most of the latitudinal studies attempted to test whether herbivore pressure increases towards the equator, as has long been predicted [17,95,96]. Thus far, these studies have produced mixed results with regards to how plant defenses vary across latitude [93,94]. More recently, however, studies have begun to explicitly examine the effects of abiotic variables on plant–herbivore interactions instead of, or in addition to, using latitude as a proxy for variation in climate variables [7,9,20]. As we outline in our framework (Figure 1B, main text), incorporating the potential effects of abiotic variables on plant growth and defense traits as well as on herbivore pressure (or other biotic interactions, such as competition), should provide more robust inference into the mechanisms regulating patterns of herbivore damage and plant defense. To evaluate the support for our framework from these observational studies, we reviewed 15 observational studies that examined intraspecific variation in plant resistance along environmental gradients, published between 2000 and 2016 (Table S2 in the supplemental information online). Six studies examined latitudinal gradients, four examined precipitation gradients, and five examined multiple environmental factors. We found mixed support for the relation between resource availability and constitutive resistance traits, with six studies reporting some support for both positive and negative resource–resistance relations and three studies finding mixed or no relations (Table S2 in the supplemental information online). Most of these studies did not measure growth rate, herbivore pressure, or test for growth–defense tradeoffs. Herbivore pressure can vary considerably across gradients, but not always in a consistent or predictable manner [7,90,97]. Observational studies also have the limitation of not being able to separate responses that are phenotypically plastic from genetic responses. As such, the confounded nature of observational studies may partially explain the mixed support for patterns of both herbivore damage and plant defenses across environmental gradients.

Prediction 1: High Resource Availability Selects for Faster-Growing Plants compared with Low-Resource Environments Most of the studies we reviewed (63%) showed that high-resource environments select for faster growth (Table 2, Table S1 in the supplemental information online). This finding is consistent with the RAH for comparisons among species and also[2_TD$IF] with many studies showing that plants have evolved clinal patterns in growth rates [32,33]. Three studies found no or mixed evidence for clines in growth rates and three studies found a negative effect of resource availability on growth rate (Table S1in the supplemental information online).

Table 2. Summary of the Predictions of the RAH and their Applicability to the Within-Species Studies that We Review here Category

Predictions Comparing High-Resource Habitats to Low-Resource Habitats

Summary of Findings

Growth[3_TD$IF] rate

Selects for faster growth rates

Well supported that plant growth rate typically increases with increased resource availability (supported by ten of 16 studies)

Defense type

Selects for decreased resistance

Not well supported (supported by five of 19 studies); most studies imply herbivore pressure as the major force selecting for resistance traits

Selects for increased tolerance

Not well examined: two studies invoke tolerance

Selects for higher induced resistance

Not well examined: two studies support this hypothesis and two studies suggest the opposite, that inducibility might be more likely to evolve under low-resource conditions where herbivore pressure is sparse

No consideration of herbivore pressure along resource gradients

Nine of 11 studies that [4_TD$IF]measure herbivore pressure suggest that insects are more abundant in highresource environments[5_TD$IF], one at range centers[6_TD$IF], and one found mixed patterns

Herbivore pressure

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Prediction 2: High Resource Availability Corresponds with Reduced Resistance, Increased Tolerance, and Higher Induced Resistance We found little support for the RAH prediction that plants growing in high-resource environments or with higher inherent growth rates should be more poorly defended than conspecifics from low-resource environments with slower growth rates. Only 26% of studies found the predicted negative relation between resources and resistance, where resistance was lower in plant genotypes originating from high-resource environments compared with low-resource environments (Table 2, Table S1in the supplemental information online). Eleven studies (58%) found a positive relation between resources and resistance and three (16%) studies found no or mixed relations (Table S1in the supplemental information online). Of the studies that found higher resistance in low-resource environments, one also found faster growth rates in low-resource environments [20], which violates the tradeoff between growth and defense assumed by most theories of plant defense [10,24,34]. Five studies supported both increased growth and reduced (or mixed) resistance in highresource environments. Of these, three were conducted with the perennial herb Asclepias syriaca and two were conducted with boreal tree species [35,36]. One of the Asclepias studies used only five populations, two collected in southern Wisconsin and three collected in northern Wisconsin [37], while another used ten populations collected across a temperature gradient in the eastern USA [38]. A larger study using 22 populations of A. syriaca found reduced growth with increasing latitude and some evidence for increased resistance traits at higher latitudes [9], which supports the RAH. However, when these data were analyzed using precipitation instead of latitude (a direct measure of climate, instead of a proxy), these patterns did not hold. Although these studies support the extended RAH predictions of lower growth and higher resistance in low-resource environments, only one study with Betula neoalaskana exhibited the predicted growth–resistance tradeoffs [35]. Of the 11 studies that found that plants in high-resource environments had higher levels of resistance traits compared with low-resource environments, most suggested that herbivore pressure is positively related to resource availability and subsequently drives patterns of resistance in plants [6,39–45]. Of the four studies that evaluated inducibility, two found patterns opposite of those predicted by existing theory, with more induced resistance in low-resource environments (thorns [41] and volatile organic compounds [46]). Two studies supported predictions of higher inducibility in high-resource environments [38,47], but only one exhibited a tradeoff between constitutive and induced resistance [38]. Inducibility can be promoted in lowresource environments if herbivore pressure is low and herbivory is sparse and variable [48,49]. We were not able to adequately address predictions related to tolerance due to low sample sizes. If tolerance is positively related to growth rate [50], we expect tolerance to be greater in high- versus low-resource environments, as predicted by the RAH [10]. However, of the two studies that directly assessed tolerance from plants originating along a resource gradient, one found no difference in tolerance among populations [47], while the other found the opposite of what is predicted by the RAH: tolerance increased with latitude and was negatively related to growth rates [43]. Other studies suggest that tolerance is not related to growth rate but rather to other physiological traits, such as nutrient content or allocation patterns [51–53]. We conclude that intraspecific patterns of plant growth across resource gradients are consistent with theory developed to describe interspecific patterns. Although fairly limited, the evidence also suggests that there is no consistent tradeoff between growth and resistance, and that both can covary positively with resource availability. Importantly, however, intraspecific patterns of constitutive and induced resistance, and likely tolerance, often differ from predictions of interspecific theory (Figure 1). The relation between resource availability and resistance, both constitutive and induced, appears to be mediated through herbivore pressure, whereas the effect of[7_TD$IF] resources

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on tolerance [8_TD$IF]is more likely to be mediated through growth rate or other physiological traits (Figure 1B).

Why Does Interspecific Theory Fail to Predict Intraspecific Patterns? Among species, there are strong tradeoffs whereby different species can either grow or defend via resistance [11,12,28,54]. However, within species, tradeoffs between growth and resistance are not always observed (Table 2). This could be due to methodological differences between inter- and intraspecific studies (Box 2), but it could also be explained by differences in the way that ecological processes act on microevolutionary processes within a species compared with how they shape macroevolutionary patterns that generate genetic tradeoffs among species [55,56]. For instance, ecological processes might operate at smaller spatial scales within a species relative to comparisons made among species, as has been shown by studies of intraspecific trait variation [57–59]. Spatial scale is important because the geographic ranges of single species are smaller than the potential geographic ranges encompassed by comparisons among multiple species (Box 2). Traits that have competing demands for resources or are functionally redundant can create tradeoffs among species [60]. These demands might not be the same within species if the distribution of a species does not encompass a large enough resource gradient to impose the same constraints among species [56]. Other factors that operate at smaller scales could be more important for selecting growth–defense strategies within a species [57]. Such processes might include herbivore community composition, climate variability, or growing season length, among others [7,9,20,43,61]. Variation in resource acquisition among individuals or populations could also mask tradeoffs within a species that are commonly observed among species [62,63]. The above factors notwithstanding, the ecological constraints that shape the growth–resistance tradeoff among species potentially shed some light on predicting which species should and should not exhibit these growth–resistance tradeoffs intraspecifically. For instance, highly defended species often originate from low-resource, stressful environments (Figure 2A) [11,13,27]. For these species, growth is constrained by physiological stress and we might expect to find a negative relation between resource environment and resistance within these species (Figure 2B). Interestingly, the intraspecific studies that[9_TD$IF] provide any evidence for a

Box 2. Methodical Differences between Inter- and Intraspecific Studies Several methodological explanations exist for why we found little congruence between theory developed to describe how resource availability affects interspecific and intraspecific patterns of plant growth and defense. First, within-species studies might not have adequate sampling power in terms of number of populations or distributions of traits to detect tradeoffs [98]. In other words, interspecific comparisons often involve many species that inhabit very different habitats, with substantial variation in underlying abiotic conditions. By contrast, intraspecific studies often compare fewer populations (than species in interspecific studies) and there might be less variation in abiotic conditions than is the case for interspecific comparisons. Second is the issue of comparisons used among- versus within-species studies. Among-species studies compare the average defense among species, typically from sites that are broadly representative of where those species occur. That is, they focus on comparing macroevolutionary differences in species originating from different resource environments, either within a habitat (e.g., shade-tolerant species versus gap specialists) or among habitats (e.g., low-resource versus high-resource soils) [11,13,28,66]. By contrast, single species are often exposed to steep environmental gradients across their ranges and examining quantitative variation in defenses across resource gradients is typically the goal of intraspecific studies (i.e., clinal variation [7,9,20]). Herbivore pressure likely differs substantially across resource gradients and herbivore distributions often do not completely overlap with the distributions of a plant species [17,91,97]. These gradients in herbivore pressure are less extreme between adjacent habitats that can differ in soil resource availability or light [11]. The type of resource gradient used for inter- versus intraspecific comparisons also differs. Interspecific comparisons usually involve soil nutrients or light [12], whereas the intraspecific studies we reviewed typically involved latitude and elevation. The type of resource gradient might also be important for driving trait relations [57]. Finally, we reiterate that the small number of intraspecific studies testing for genetically based relations between resource availability and defense limits the degree to which robust comparisons between intra- and interspecific comparisons can be made. In sum, explicit consideration of other factors that covary along environmental gradients (e.g., herbivore pressure) is likely critical for understanding intraspecific variation in plant growth and defense [7,9,43,61].

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Resistance

Herbivore pressure Physiological stress

(A)

Resources

(B)

(C)

Resources

Figure 2. Hypothetical Relations between Resources and Resistance among and within Nine Species across a Single Resource Gradient. (A) Each dot represents the mean trait values for a species; colored lines represent relations between growth and constitutive resistance for that species. The thick black line is fitted to the mean values for each species. Individual species might deviate predictably from this interspecific trend. (B) Species at the low-resource, high-defense end of the continuum that have evolved slow growth rates might be more likely to exhibit growth–resistance tradeoffs because growth is constrained by resource availability, making defenses more valuable than growth. (C) Species at the high-resource, low-resistance end of the continuum should not be constrained by physiological stress and, thus, might exhibit a positive growth–resistance relation that is selected by biotic components of the environments, such as herbivory.

negative relation between resources and resistance were with a notoriously well-defended plant (Asclepias syriaca [9,37,38]), a shrub from arid environments [20], and trees from a low-resource environment (i.e., boreal forests [35,36,64]). By contrast, physiological stress might not be applicable to fast-growing species that originate from high-resource environments. As such, biotic factors might be important for selecting growth and defensive traits, such as competition and herbivore pressure, resulting in positive growth–resistance relations for fast-growing species originating from high-resource environments (Figure 2 C). In sum, we suggest that the resource environment selects for different growth–resistance strategies (i.e., growers or defenders) across species, and that intraspecific growth–resistance relations are then selected by smaller-scale environmental factors from these different growth–resistance strategies.

A Framework for Predicting Intraspecific Patterns of Plant Growth and Defense Along Environmental Gradients We extend the predictions of the RAH (Figure 1A) to develop a working framework for understanding the drivers of intraspecific geographic variation in plant defense. Specifically, we propose that selection pressures imposed by resource availability can act independently on different components of defense and be mediated through biotic agents (Figure 1B). As predicted by RAH and generally supported by our review, we predict that: (i) with increasing resource availability across an environmental gradient, there should be increased selection for faster intraspecific growth rates. However, herbivore pressure is often positively related to resource availability, both because high-resource environments support more herbivores (particularly generalists) [17,65] and because plants growing in high-resource environments can have higher tissue quality than plants growing in low-resource environments [66,67]. Thus, within species, high-resource environments might also exert greater selection on plant resistance compared with low-resource environments, by increasing herbivore pressure [40,45]. Differences in herbivore pressure might not be as evident among species, because different plant species have different insect associates [68,69]. As such, we also predict that: (ii) the effect of resources on intraspecific levels of constitutive resistance should be positive and indirect, mediated by herbivore pressure. Resources could also directly constrain the evolution of resistance traits and act in conjunction with biotic pressures to set levels of resistance. Disentangling the relative influences of abiotic and biotic drivers of resistance across resource

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gradients remains a central challenge in uncovering the drivers of spatial variability in plant defense [7]. Inducibility should trade off with constitutive resistance within species [49,60,70] and should be more effective in environments with low and unpredictable rates of herbivory [48,49]. Thus, we expect: (iii) induced resistance to be favored in low-resource environments or other environments with low herbivore pressure. Tolerance can be affected by resources through the constraining effect of resources on growth rate or other physiological traits [51,53,71]; in this case we would expect: (iv) (a) a positive relation between resource availability and tolerance (Figure 1B). However, traits that are adaptive in stressful environments, such as allocation to belowground organs [52] or a more rapid phenology [43], might also facilitate greater tolerance to herbivory. In this case, we would expect: (iv) (b) a negative indirect relation between resources and tolerance mediated by plant traits.

Designing Experiments to Test for Clinal Patterns in Plant Defenses Fully disentangling the relative influences of abiotic and biotic factors driving intraspecific evolutionary patterns of plant defense will require research that couples a dynamic adaptive landscape approach [56] with common gardens or reciprocal transplants [72,73]. Dynamic adaptive landscapes are used to predict the trait values of different genotypes in different habitats or across environmental gradients. Testing the adaptive value of traits in different environments requires data that links traits and environment to fitness; essentially testing for trait  environment interactive effects on fitness [56]. Ideal tests of dynamic adaptive landscapes would be conducted using multiple common garden experiments or reciprocal transplant experiments to uncover differences in selection pressures and heritable traits among populations across gradients. Observational data or in situ experiments could also be useful in testing our framework, particularly the notion that resources set the template that drives genetically based intraspecific variation in plant defense. For instance, manipulating a focal resource at different sites along an environmental gradient would provide insight into the degree to which growth and defense traits respond to environmental variables (i.e., how plastic the traits are). Estimates of variation in plant defenses across natural environmental gradients or estimates of within-population variation in defense traits can give some clues as to the putative selective forces among populations that are obtainable from observational studies. That is, if defense is under consistently strong directional selection, one might expect less within-population variation compared with a population where herbivore pressure is reduced and defense is not under strong directional selection. Finally, population genetic approaches are becoming more powerful for detecting the genes, loci, traits, and environmental drivers responsible for local adaptation [74]. Integrative approaches that couple selection experiments or surveys of resistance traits in natural populations with population genetics would be particularly powerful for uncovering the genes involved in increasing fitness across resource gradients. The most robust test of our framework would involve growing multiple species that differ in inherent growth rates, collected across the same environmental gradient, in multiple common gardens at each end of the gradient. Recent frameworks have been developed for examining how intraspecific trait variation contributes to assembly of multispecies communities [56]. However, to determine whether patterns in plant defense across gradients are the result of local adaptation or plastic responses to environmental conditions, common garden studies are necessary. Studies of multiple species that occur across the same or similar geographic ranges (and also the same resource gradient) would be particularly helpful in determining whether there are predictable broad constraints among species that set growth–defense relations within species (Figure 2). Multi-garden studies of multiple species would be most appropriate for testing this hypothesis because they could capture the relative importance of herbivore pressure or abiotic factors across gradients for different species. Observational estimates of herbivore abundance would be particularly useful to supplement common garden experiments. For instance, the best-documented estimates of herbivore pressure comprise observations of

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herbivores and damage to plants naturally occurring across the gradients coupled with damage to sentinel plants from different origins placed at multiple sites across the gradient [40,45,46]. Identifying the dominant herbivore type (i.e., generalists or specialists) will shed further light on the evolution of different defensive strategies (e.g., tolerance versus resistance [75–77]).

Outstanding Questions Do particular environmental gradients (i.e., precipitation, soil nutrients, elevation, etc.) have stronger or more consistent effects on genetically based growth–defense relations than others?

Concluding Remarks There has been recent and growing interest in going beyond documenting the consequences of species interactions to understanding when and where species interactions will have different ecological or evolutionary consequences [78,79]. A continuing challenge with regards to how resource gradients affect intraspecific variation in plant defense, and understanding ecological and evolutionary processes along gradients generally, is properly identifying which environmental variables are the main drivers in different systems. This includes both abiotic gradients [57,79,80] and biotic gradients in herbivore pressure, competition, and herbivore community composition [76,81]. The general concepts of our framework should also have applications to a variety of subdisciplines, including release from enemies by invasive plants [82], changes in range distributions and the strength of species interactions under climate change [31,83], or variation in mutualistic or pathogenic interactions across gradients [79,84]. As such, our testable framework provides an important step towards reconciling inter- versus intraspecific patterns of trait variation beyond just defense against herbivores[10_TD$IF] (see Outstanding Questions). Acknowledgments We thank A. Agrawal, K. Baer, A. Dehnel, R. Hegstad, L. Larios, J. Orrock, M. Spasojevic, A. Woods, and three reviewers for

How strongly does growth rate constrain the evolution of defense and how does this vary across environments? How do herbivore communities, herbivore pressure, and the intensity of selection on plant defense traits change across resource gradients? Do generalist and specialist herbivores differ in their responses to environmental variation, in terms of abundance, community composition, or degree of local adaptation? How do the relative influences of plasticity and local adaptation contribute to patterns of growth and defense along resource gradients?

helpful discussions and comments. MPG Ranch provided funding.

Appendix A Supplemental information Supplemental information related to this article can be found, in the online version, at http://dx.doi.org/10.1016/j.tree.2016.

Do overarching intraspecific growth and defense strategies exist across a variety of species, or do species differ in growth–defense strategies?

05.007.

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