Community Heterogeneity and the Evolution of Interactions Between Plants and Insect Herbivores

Volume 81, No. 4 THE QUARTERLY REVIEW OF BIOLOGY December 2006

COMMUNITY HETEROGENEITY AND THE EVOLUTION OF INTERACTIONS BETWEEN PLANTS AND INSECT HERBIVORES

Anurag A. Agrawal Department of Ecology and Evolutionary Biology and Department of Entomology, Cornell University Ithaca, New York 14853–2701 USA e-mail: [email protected]

Jennifer A. Lau Department of Plant Biology, University of Minnesota St. Paul, Minnesota 55108 USA e-mail: [email protected]

Peter A. Hamba¨ck Department of Botany, Stockholm University SE-106 91 Stockholm Sweden e-mail: [email protected]

keywords associational resistance, coevolution, community ecology, community genetics, diffuse selection, diversity, herbivory, invasive species, plant apparency, plant defense guild hypothesis, plant-herbivore interactions, quantitative genetics

abstract Plant communities vary tremendously in terms of productivity, species diversity, and genetic diversity within species. This vegetation heterogeneity can impact both the likelihood and strength of interactions between plants and insect herbivores. Because altering plant-herbivore interactions will likely impact the ﬁtness of both partners, these ecological effects also have evolutionary consequences. We review several hypothesized and well-documented mechanisms whereby variation in the plant community alters the plant-herbivore interaction, discuss potential evolutionary outcomes of each of these ecological effects, and conclude by highlighting several avenues for future research. The underlying theme of this review is that the neighborhood of plants is an important determinant of insect attack, and this results in feedback effects on the plant community. Because plants exert selection on herbivore traits and, reciprocally, herbivores exert selection on plant-defense traits, variation in the plant community likely contributes to spatial and temporal variation in both plant and insect traits, which could inﬂuence macroevolutionary patterns.

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Introduction and History can strongly impact the interaction between STRIKING feature of most plant and plants and herbivores. A animal communities is that the organ- While the interest in the role of spatial isms are unevenly distributed in nature. This complexity in plant-herbivore interactions phenomenon, which occurs across all spatial may be as old as agriculture, as evidenced by scales, has the additional consequence that the widespread traditional use of intercrop- the strength and identity of interactions be- ping to reduce pest attack, theories to explain tween species show a high degree of spatial these patterns did not begin to mature until variability. As a consequence of individuals the 1960s. During this time, four somewhat moving across space or from spatial variability parallel debates involved the role of plant in population growth rates, individuals of the spatial heterogeneity on plant-herbivore in- same species typically encounter different interactions: (i) effects of plant species diversity teractions at different sites. The study of such on herbivore population stability; (ii) effects spatial variability is a central issue within ecol- of plant stand characteristics on herbivore ogy, as it enters most definitions of the sub- impacts; (iii) consequences of plant appar- ject, and has attracted interest from ecologists ency for the evolution of plant defenses; and since the early days. This paper deals with (iv) associations of plants into guilds that rep- these spatial patterns in communities and resented community defenses. Below we pro- considers their evolutionary consequences vide a brief overview of the main concepts for interactions between insect herbivores that shaped this early research. We use these and plants. ideas, along with more recent hypotheses, as Given that plant communities vary some- the foundation for linking heterogeneity in what predictably in their diversity, structure, plant communities to the evolution of plant- and composition across habitats and biogeo- herbivore interactions (Box 1, Tables 1 and 2). graphic zones (Gurevitch et al. 2002), it is a reasonable hypothesis that the strength of diversity and stability plant-herbivore interactions may also vary Resource diversity has long been predicted predictably. For example, at a global scale, it to increase community stability, in part by has been hypothesized that there is a latitu- reducing runaway consumption of plants. dinal gradient in the intensity of herbivory, Charles Elton (1958) proposed the first hy- which has favored a greater diversity of un- pothesis to explain how simple plant com- palatable plants closer to the equator communities can incur greater losses to herbivory pared to temperate regions (Pennings and than diverse habitats. Based on a combina- Silliman 2005). It also has been argued that tion of theoretical results and empirical ob- herbivores have evolved more specialized strat- servations, he suggested that the reduced her- egies in diverse tropical habitats compared to bivory in complex habitats was a consequence temperate regions due to heterogeneity in the of the higher efficiency of predaceous insects chemical and ecological traits associated with in these environments (Enemies Hypothesis). particular plant species. Though the bulk of The suggested reason for this efficiency is that research in plant-insect interactions over the greater diversity of alternative food sources past decades has focused on binary interac- and habitats increases the persistence and tions independent of the surrounding com- stability of generalist predators. Based on the munity matrix, it is becoming increasingly classic experiment by Carl Huffaker (1958), clear that the plant community as a whole can spatial complexity was argued to enable pred- shape the selective environment for both ator-prey interactions to avoid collapse due to plants and herbivores. Plant communities predators consuming all prey individuals. El- show a high level of variation in genetic di- ton contrasted low diversity habitats such as versity, overall biomass, species richness, and agricultural fields and temperate forests, relative abundance. This variation creates where pest outbreaks frequently occur, to physical and chemical heterogeneity, which high diversity tropical rainforests, where out- December 2006PLANT AND INSECT HERBIVORE INTERACTIONS 351

Box 1 Definitions of vegetation heterogeneity effects on plant-herbivore interactions Associational resistance: Plants experience reduced herbivory when growing in close proximity to highly defended neighbors or to plants that physically or chemically mask the focal plant, compared to when growing next to other (or no) plants (Hamba¨ck et al. 2000). Associational susceptibility: Plants experience increased herbivory when growing in close proximity to preferred host plants or plants that provide alternate resources for herbivores, compared to when growing next to less preferred plants (Agrawal 2004). Enemy-free space: An herbivore experiences reduced predation or parasitism when feeding on a particular host plant. Typically, it is assumed that enemy-free space comes at the cost of reduced host plant quality (Murphy 2004). Host alternation: An insect herbivore population requires two different host plant species to complete its lifecycle (Dixon and Kundu 1994). Neural constraints hypothesis: Diverse plant communities make host choice problematic for herbivores by causing greater strain on neural processing, which results in either inefficient decision-making (i.e., exposing organisms to predation or other risks) or poor quality decision-making (i.e., choosing plants on which the herbivore has low fitness) (Bernays 2001). Plant apparency hypothesis: Apparent plants are more likely to be defended by quantitative defenses, which typically reduce plant digestability and are not easily overcome by specialist herbivores; unapparent plants are more likely to be defended by qualitative defenses, typically toxins that limit feeding to subset of specialized herbivores (Feeny 1976). Plant defense guild hypothesis: Plants in a community are functionally interdependent with respect to their herbivores, implying that vegetation composition can influence herbivore attack rates and ultimately plant and herbivore evolution (Atsatt and Odowd 1976). Plant resource competition: The presence of plant competitors alters several environmental variables (e.g., water, light nutrients, available space) that may influence the costs or benefits of producing plant defenses (Tiffin 2002). This effect is, in part, mediated by a proposed tradeoff between defense and competitive ability. Plant resistance to herbivory: Traits of the plant that reduce the preference or performance of herbivores (Karban and Baldwin 1997) and that are expected to reduce herbivory. Resistance traits may be chemical, morphological, or phenological in nature and may be expressed constitutively (all of the time) or induced following attack by herbivores. Refuge hypothesis: The presence of susceptible plants in a primarily resistant population may reduce selection on herbivore counteradaptations (Gould 2003). Tolerance to herbivory: The degree to which plant fitness is affected by herbivore damage relative to fitness in the undamaged state (Strauss and Agrawal 1999). When damage levels are continuous, tolerance is measured as the slope of the line relating plant fitness to the level of damage. If damage is experimentally imposed at a single level, or if it is qualitative (such as loss of the apical meristem), then tolerance is typically measured as the ratio of plant fitness in the damaged to the undamaged state. 352 THE QUARTERLY REVIEW OF BIOLOGY Volume 81 Feeny 1976; Silvertown and Dodd 1996 Dolinger et al. 1973; Atsatt and O’Dowd 1976 Tiffin 2002; Uriarte et al. 2002 Lau 2006 None? References more quantitative defenses, while unapparent plants have more qualitative defenses. Selection for herbivore preference/performance on most abundant host. Selection on plants favors rare plant defense phenotypes. defenses) of host 1 should result in selection for increased plant defenses in host 2. on plant defenses varies depending on the presence of competitors. neighbor decreases selection on a focal plant’s defenses. Magnitude or direction of selection Testable prediction Interaction strength Apparent plants have Frequency-dependent selection Costs/benefits Interaction strength Increased abundance (or decreased Mechanism Interaction strength The presence of a resistant TABLE 1 Summary of vegetation heterogeneity effects on the evolution of plants plant defense. diversity. Cyclical change in genotype frequencies. competitive environment. abundance/defense level of alternate host. Plant community shapes type of Maintenance of plant (and defense) Level of plant defense varies with Defense level of 1 host correlated with the Vegetation heterogeneity effectPlant apparency hypothesis Evolutionary outcome Plant defense guild hypothesis Plant resource competition Associational resistance (or susceptibility) Decreased levels of plant defense. Host alternation December 2006PLANT AND INSECT HERBIVORE INTERACTIONS 353 Dolinger et al. 1973; Atsatt and O’Dowd 1976 Hawthorne 1997 Singer et al. 1989 Bernays 2001 Gould 2003 Mira and Bernays 2002; Murphy 2004 Dixon and Kundu 1994 References Selection on herbivore for preference/performance on most abundant host. to novel host plant ismixed greater population from than from single host populations. preference/performance on most available host. herbivore specialization. Plant resistance traits are effective longer in diverse habitats. only in the presence of natural enemies. are correlated with a greaterof percentage host-alternating insect herbivores. Plant diversity correlated with Testable prediction TABLE 2 Ecological opportunity/ Frequency-dependent selection Ecological opportunity Ability or rapidity of adaptation Ecological opportunity/ Insect demography Ecological opportunity More diverse plant communities Costs/benefits Mechanism Ecological opportunity Increased fitness on novel host Summary of vegetation heterogeneity effects on the evolution of insects Cyclical change in herbivore preference. Greater genetic variation maintained. Rate of evolution of offensive herbivore strategies decreased in diverse plant communities. Reduced insect specialization. Host-shifts to readily available hosts. Ecological opportunity Selection on herbivores for Host-shifts to “safe” hosts. herbivore species increases with increasing plant community diversity. prevalent in diverse habitats. Number of host-alternating Herbivore specialization more Vegetation heterogeneity effectPlant defense guild hypothesis Evolutionary outcome Presence of alternate host plants Host plant abundance Enemy-free space Refuge hypothesis and Insect counteradaptation Host alternation Neural constraints hypothesis 354 THE QUARTERLY REVIEW OF BIOLOGY Volume 81 breaks are purportedly less common. Thus, apparency in the evolution of plant defenses, through mechanisms of greater predator ef- herbivore search strategies, and diet breadth. ficiency and population persistence, com- This discussion was initiated by Paul Feeny munity stability may be enhanced by plant (1976), who observed that highly apparent diversity. plants tend to have different plant chemistry than seemingly unapparent plants. In partic- effects of stand characteristics on ular, apparency theory suggests that long- herbivore abundance and impact lived plants, large plants, or plants growing In contrast to the Enemies Hypothesis, Rich- in low diversity communities, will evolve de- ard Root (1973) argued that the higher her- fenses that are effective against most all bivore densities in dense, monospecific, or consumers, and function by reducing the ed- large stands emerge as a consequence of re- ibility or nutritional quality of the plant. Tem- source concentration effects on immigration perate trees typify such apparent plants be- and emigration of insect herbivores. This Re- cause of their lifespan, size, and community source Concentration Hypothesis posits that structure. Thus, oak trees are defended by individuals are more likely to locate and re- low levels of foliar nitrogen and water and main in stands with dense host plants. More- high levels of leaf toughness and tannins— over, the tendency to remain in a patch was considered quantitative defenses because argued to be higher for specialized insect her- they act in a dose-dependent manner on both bivores compared to generalized ones be- generalist and specialist herbivores. These cause a species with a broader host range plants are predicted not to defend with acute would be more likely to drift into the sur- toxins or barriers to feeding (qualitative de- rounding vegetation to feed on other host fenses), which are typically found in unap- plants. The Resource Concentration Hypoth- parent plants. Qualitative barriers to feeding in herbaceous unapparent plants (such as al- esis and the Enemies Hypothesis have become kaloids, cyanides, and cardenolides) are read- the two main hypotheses used to explain ily overcome by specialists herbivores (e.g., lower herbivore loads in diverse agricultural cardenolides in milkweeds, Holzinger and stands (Russell 1989; Andow 1991; Tonhasca Wink 1996). The interplay between ecology and Byrne 1994; Bommarco and Banks 2003). and evolution is intriguing; given that unap- Recent studies suggest that resource concen- parent plants are difficult to find for special- tration effects are also important in natural ists (Root 1973), these plants have the evolu- systems, and perhaps have greater predictive tionary advantage of hiding from their most ability than plant productivity for understand- damaging enemies. Apparent plants, though ing the effects of insect herbivory on plant a concentrated resource, are of poor quality community composition (Long et al. 2003; for nearly all consumers. The general pattern Carson et al. 2004). A consequence of both of divergent patterns of chemical defense in these hypotheses is that the herbivore loads apparent and unapparent plants has stood on a focal plant may be highly context depen- the test of time (Silvertown and Dodd 1996). dent. For example, one plant species may in- Feeny suggested that the mechanism un- directly receive protection from herbivory by derlying the difference between apparent associating with other plants; the main term and unapparent plants was that highly appar- associated with this pattern is “associational ent plants are more likely to experience con- resistance” (Tahvanainen and Root 1972). Of tinuously high herbivory because they are eas- course, several other effects of plant associa- ier to locate, and this would necessitate the tions are possible and are detailed in Box 1. development of general defenses effective against most all consumers. Conversely, the plant apparency and the evolution low and irregular herbivore attack rates on of plant defenses unapparent plants was assumed to reduce se- The third concept arose as an evolutionary lection for more effective defenses; in other consequence of the Resource Concentration words, the qualitative barriers to feeding were Hypothesis, and concerned the role of plant sufficient. An early criticism against this view December 2006PLANT AND INSECT HERBIVORE INTERACTIONS 355 was that counteradaptations in herbivore et al. 2004). Thus, insectary plants can be search behavior should reduce the difference viewed as an update of Elton’s Enemies Hy- in attack rates between apparent and unappar- pothesis, with the notion that specific plant ent plants (Rausher 1978). The argument was species are better neighbors than others. that specialist insects searching for unappar- Second, “repellent plants” are plants that ent plants would experience strong selection deter herbivores via spines, toxins, odors, or for increased host search efficiency. Indeed, shade, causing herbivores to reject or fail to many specialist herbivores of unapparent locate their host plant in the neighborhood. plants use defense-related, long-distance cues The proposal of repellent plants is the most to locate their hosts (Bowers 1991; Giamous- general prediction of Atsatt and O’Dowd taris and Mithen 1995). In addition, qualita- (1976), with many examples indicating strong tive defenses are often breached by generalist influences on plant community structure. Ex- herbivores and can still have dose-dependent amples of associational resistance mediated effects on specialist herbivores (Agrawal 1998, by repellent plants abound from both the ma- 1999; Agrawal and Kurashige 2003). None- rine and terrestrial literature on both verte- theless, despite questionable mechanisms, ap- brate and invertebrate herbivores (Hay 1986; parency theory provides a useful framework Pfister and Hay 1988; Callaway 1995; Ham- for thinking about the evolution of plant ba¨ck et al. 2000; Callaway et al. 2005). This chemical defense in the context of plant com- repellent plants hypothesis was later split into munity heterogeneity. two mechanisms, “masking” (a host plant is not detectable because of the presence of the plant defense guild hypothesis nonhosts) and “repellency” (active avoidance The interdependency of plants, in relation by herbivores of the repellant plant) (Ham- to their interaction with herbivores, prompted ba¨ck and Beckerman 2003). Peter Atsatt and Dennis O’Dowd (1976) to Third, “attractant-decoy” plants are those formulate general ideas about plant defense that can serve as alternative food sources to guilds, describing several mechanisms under- the herbivore, and by their presence reduce lying how plant neighbors impact attack rates the herbivore impact on other plants in the of focal plant species (Tables 1 and 2). Atsatt neighborhood. This hypothesis later served and O’Dowd (1976) introduced three poten- as a founding principle behind the develop- tial underlying mechanisms: insectary, repel- ment of trap cropping systems in agriculture lent, and attractant-decoy plants. Because (Vandermeer 1989). It has largely been re- these ecological mechanisms underlie the po- jected as a mechanism in natural plant-insect tential for evolutionary consequences de- systems, however, because it neglects the tailed below, we, in turn, evaluate the current numerical response of herbivores at larger status of each. spatial scales and assumes suboptimal food First, “insectary plants” are those that at- selection by herbivores (Hja¨lteń et al. 1993; tract predators of herbivores by providing White and Whitham 2000; Rousset and Le- floral or extrafloral nectaries or alternate her- part 2002; Hamba¨ck and Beckerman 2003; bivore hosts. These predators feed on herbi- Rand 2003). Nonetheless, attractant-decoy dy- vores on the insectary plants but, may also namics may be common in natural systems for feed on herbivores attacking plant neighbors. plant interactions with large mobile generalist Insectary plants have widely been employed grazers (Milchunas and Noy-Meir 2002). in agriculture as part of the general principle The attractant-decoy hypothesis can also be that plant diversification typically enhances seen as a precursor to ideas on the effects of predation and parasitism of target pests (Rus- plant mixtures for generalist herbivores, be- sell 1989; Gurr et al. 2003). Two recent stud- cause it identified the possibility that plant ies in natural systems have also demonstrated neighbors may not only reduce, but also en- that plants that host herbivores and parasi- hance herbivory on a focal plant. This can toids increase parasitism of herbivores on occur, for example, when herbivore popula- neighboring plants (Stiling et al. 2003; Morris tions grow on an attractive plant and spill over 356 THE QUARTERLY REVIEW OF BIOLOGY Volume 81 onto neighboring vegetation. In the current cused on tightly linked pairs of interacting ecological literature, the main terms associ- species, both Daniel Janzen (1980) and Lau- ated with such negative effects between plants rel Fox (1981) wrote of “diffuse coevolu- are “apparent competition” (Connell 1990; tion”—situations where reciprocal selection Holt and Lawton 1994) and “associational occurred between groups of plants and groups susceptibility” (Brown and Ewel 1987). A re- of herbivorous insects. In particular, Fox pre- cent set of conceptual observations suggests dicted that diffuse coevolution was most likely that the direction of associational effects for organisms like temperate forest trees, with may be predicted based on two axes, the each individual exposed to many damaging level of host plant specialization and the ex- herbivores over its lifetime. For example, in a tent of resources provided by plant neighbors plant community with several congeneric (Figure 1) (Agrawal 2004). Associational ef- plants, several herbivore species may attack fects on a focal plant are predicted to increas- each plant species, and there is likely some ingly move from susceptibility to resistance as overlap in the attackers on closely related neighbor host quality decreases for generalist plants. Thus, each plant species may be evolv- herbivores, or as alternate resources are not ing resistance, but to a suite of herbivore spe- provided for specialist herbivores. cies. Similarly, each herbivore species may be evolving offense strategies, but these ad- evolutionary impacts of vegetation aptations are shaped by a set of host plants. heterogeneity are likely common Because of ecological interactions between Ample evidence exists that vegetation these suites of interacting community mem- heterogeneity can modify the probability bers, and because of tradeoffs and constraints of a particular plant-herbivore interaction oc- produced by the necessity of adapting to sev- curring and the intensity of that interaction. eral selective agents simultaneously, the net In current community ecology jargon, these selection on a trait will thus depend on the types of interactions are variously described as composition of the community. indirect, trait-mediated, or interaction modi- fications (Wootton 1994; Abrams 1995). If The Plant Community’s Role in the this change in the strength of the interaction Evolution of Plant Defenses alters individual fitness in a nonrandom man- Interactions among plants may influence ner, then vegetation heterogeneity may also the evolution of plant defenses in many ways. alter patterns of natural selection on plant We focus primarily on how competing plants and insect traits involved in the interaction. change environmental variables, such as re- For the ecological interactions outlined in source availability, that in turn affect the this review to have evolutionary consequen- shape of the fitness landscape. We also discuss ces, the traits of interest (in the plants or in- how interactions between plants influence sects) must meet the Darwinian criterion of the evolution of plant defenses by directly al- having heritable variation that affects fitness. tering the probability of herbivore attack. For Nearly all continuously varying traits exhibit example, resource competition may affect se- genetic variance within and between popula- lection on defense by altering the costs of tions, and thus the real challenge becomes plant defenses, influencing the expression of identifying the selective agents, fitness im- plant defense traits, or changing the fitness pacts (i.e., strength and direction of selec- consequences of herbivore damage. We dis- tion), and factors that may limit a response cuss the evidence for each mechanism and to selection. Below, we focus on microevolu- how competitors and herbivores interact to tionary responses in terms of how plant modify patterns of selection on plant de- neighborhood may alter selection on both fenses. Competitors may also influence selec- plants and herbivores. Later, we discuss how tion on plant defenses if there are genetic these responses could shape macroevolution- correlations or pleiotropic effects between ary patterns. traits involved in the competitive and plant- While early studies of coevolution often fo- herbivore interactions; however, we will limit December 2006PLANT AND INSECT HERBIVORE INTERACTIONS 357

Figure 1. Predicting Associational Effects Associational effects of plant neighbors are predicted to be determined by the diet breadth of insect herbivores and the extent to which the neighboring plants are utilized. Resources gained from plant neighbors extend beyond food resources. Thus, as specialists gain less from neighbors, focal plants are increasingly predicted to provide associational resistance. For generalist herbivores, as the quality of neighboring plants declines from a good host to poor host, so will the associational effect on a focal plant change from susceptibility to resistance. (Adapted from Agrawal 2004.) our discussion to evolutionary consequences et al. 2002, 2003; Tiffin 2002; Julia Koricheva, arising from ecological effects (see Iwao and personal communication). Thus, the pres- Rausher 1997 for a discussion of effects due ence of competitors does indeed alter the to genetic architecture). While we focus on costs of defense, though there is still no gen- negative relationships between plants in this erality regarding the direction of the effect, section, positive plant-plant interactions (i.e., and this requires further study. We nonethe- facilitation) could also produce evolutionary less agree with the general prediction that the effects and deserve further attention. presence of competitors will alter selection Competition is often thought to increase on plant defenses due to changes in the re- the costs of defense (i.e., a reduction in plant source investment strategy. fitness associated with defense in absence of Also, competition can alter the phenotypic herbivores) because competing plants have expression of plant defense traits, which al- fewer resources available for allocation to de- ters the variation on which selection can act. fense compared to plants growing without Such indirect effects are often referred to as competitors. Although this prediction has “trait-mediated” because the presence of been confirmed in phenotypic studies (i.e., competitors changes the plant phenotype studies that have estimated the cost of in- (i.e., phenotypic plasticity) in a manner that duced responses to herbivory in the presence influences levels of herbivore attack (Agrawal and absence of competitors) (van Dam and 2001; Callaway et al. 2003). Changes may oc- Baldwin 1998; Agrawal 2000), the reverse has cur directly in defense traits or in other traits been found for quantitative genetic studies that influence herbivore attack, such as leaf of costs of constitutive defenses (Siemens physiology or plant architecture (Morgan and 358 THE QUARTERLY REVIEW OF BIOLOGY Volume 81

Smith 1981; Kurashige and Agrawal 2005). 2004; Lau and Strauss 2005; Linhart et al. For example, Richard Karban et al. (1989) 2005). For example, Agrawal (2004) showed demonstrated that cotton plants express that the effects of root-feeding herbivores and lower levels of induced resistance when grow- competition were greater than additive (i.e., ing in highly competitive environments com- synergistic) in reducing components of fitness, pared to less competitive ones. Such effects potentially leading to more intense selection may be due to resource availability (Cipollini for plant defenses in the presence of compet- and Bergelson 2001) or plant responses to itors. This result also raises the possibility that competitors irrespective of resources (Kura- selection for traits that reduce competition shige and Agrawal 2005). Similarly, Agrawal may be an alternative evolutionary response (2004) showed that a combination of plant to the joint selective pressures of competitors competition and root herbivory altered leaf and herbivores. In contrast, Yan Linhart et al. miner abundance on milkweed. In this case, (2005) showed that aphid herbivores on while neither competition nor root herbivory thyme only decrease plant growth and repro- alone affected leaf miner abundance, com- duction in the absence of competition. Be- petition and root herbivory combined re- cause aphids differentially affect the fitness of duced abundance by 40% compared to con- particular plant chemotypes (which are ge- trols. Thus, the interactive effects of plant netically determined), selective pressures im- competition and past herbivore attack may ei- posed by aphid herbivores on plant defenses ther decrease or increase subsequent plant will likely vary with the competitive environ- resistance. ment. Third, the presence of competitors may al- The three mechanisms by which competi- ter selection on plant defenses by changing tors affect selection on plant defenses may, of the fitness consequences of herbivore damage. course, act simultaneously. For example, in This would occur when the negative fitness im- the milkweed system, competition alters the pacts of herbivory are intensified in competi- phenotypic expression of plant defenses as tive environments because any photosynthetic well as the fitness effects of herbivory (Agra- material removed by herbivores may further wal 2004). To determine the net effect of limit the plant’s ability to compete for limiting these mechanisms, however, the intensity of resources. In other words, competitors may al- natural selection on plant defenses must ter selection on plant defenses (i.e., selection be measured in the various competitive envi- will be diffuse) when interactive fitness effects ronments. The first rigorous examination of occur between competition and herbivory, selection on plant defense as influenced that is, when fitness effects are either synergis- by plant neighborhood was conducted by tic or substitutive. More specifically, selection Peter Tiffin (2002). Consistent with plant al- will be diffuse provided that there are inter- location theory (Strauss and Agrawal 1999), active effects on the relationship between Tiffin found that common morning glory plant traits and fitness and not on fitness alone plants (Ipomoea purpurea) were less tolerant of (Strauss and Irwin 2004; Strauss et al. 2005 for herbivore damage when grown in high com- a more detailed explanation). However, a re- petition environments than in low competi- cent review demonstrates that only one of ten tion ones. Given that Tiffin also reported that studies shows synergistic effects of herbivory genetic families of the morning glory varied and competition on focal plants, with a second in their fitness and defense levels, it is reason- study showing a substitutive effect, that is, the able to ask how competition affected selec- cumulative effect of herbivory and competition on plant defenses. Tiffin found no tion was less than additive (Hamba¨ck and evidence, however, that selection on resis- Beckerman 2003). While the low incidence of tance or tolerance was affected by plant interactive effects documented in this review competitors. suggests that they are rare, additional recent Only a few theoretical investigations have studies demonstrate both synergistic and sub- considered the effects of plant competition stitutive interactions between herbivory and on selection for plant defense. A combination competition on plant performance (Agrawal of simulations and analytical results by Arthur December 2006PLANT AND INSECT HERBIVORE INTERACTIONS 359

Weis and Michael Hochberg (2000) demon- these microevolutionary effects were driven strated that plant competition can indeed al- by strong species specific effects of Medicago ter selection on defense. This occurs, in part, on the Lotus/Hypera interaction. because herbivory not only damages a suscep- Juha Tuomi and colleagues (Augner et al. tible plant, but resistant plants may seize re- 1991; Tuomi and Augner 1993) took a theo- sources and then further suppress the fitness retical approach to model the evolution of of susceptible individuals. Not surprisingly, plant defense as influenced by neighbor iden- the authors found that the type of competi- tity. They used game theoretical models to tion (symmetric versus asymmetric) and de- investigate associational effects influencing fense (herbivore avoidance versus reduction selection (in addition to competition). In par- in damage once a plant is found) had strong ticular, they assume that herbivores not only consequences for the evolution of defense. avoid unpalatable plants, but also neighbors In another theoretical study, the evolution of of unpalatable plants. This has the potential resistance, as parameterized from empirical to lead to “synergistic selection for defense” data on tall goldenrod (Solidago altissima) (i.e., palatable plants gain a greater advantage from eastern North America, appeared to be than unpalatable plants do when both are independent of competition (Uriarte et al. neighboring an unpalatable plant) (Tuomi 2002). In general, selection on the plant was and Augner 1993) or the maintenance of de- dominated by competition, and resistance fended and undefended plants in a popula- was only favored under conditions of very tion (Augner et al. 1991). Unfortunately, like low costs of resistance. The authors conclude the other entirely theoretical study (Weis and that because plant traits associated with Hochberg 2000), these game theory models competitive ability also tend to enhance tol- predict many possible outcomes of neighbor- erance to herbivory (Strauss and Agrawal ing plants on selection for defense, with few 1999), Solidago may rely heavily on a tolerance general predictions. strategy. As these examples illustrate, the structure While the above reviewed studies assume of a plant community will likely have a strong that effects of plant neighbors on selection influence on the evolution of plant defenses. for plant defenses largely depend on general The selective impact on defense can be both plant characteristics, such as plant biomass qualitative and quantitative in nature. For ex- and growth rate, other studies suggest that ample, plant community composition can the specific identity of the plant competitor change the level of defense that is favored ei- may alter selection on plant traits. Lau (2006, ther by altering the strength of an interaction unpublished data) recently reported a study or the expression of defense costs. Vegetation demonstrating that an introduced plant, Med- heterogeneity can also alter the actual types icago polymorpha, alters selection for plant of defenses that are favored in a focal plant defenses in the co-occurring native plant species, as predicted by apparency theory. Lotus wrangelianus. An exotic weevil (Hypera Similarly, Lau’s work suggests that tolerance brunneipennis), which feeds on both plants, may be selected in the presence of one spe- exerts greater damage to native Lotus in the cies (Medicago), while increasing resistance presence of Medicago than in the presence of may be favored when that species is absent only the native plant community (Lau and from the neighborhood. Such findings sug- Strauss 2005). This associational effect caused gest that vegetation heterogeneity could be a stronger positive directional selection for tol- strong force in maintaining variation in both erance to herbivory and competitive ability in the type and level of plant defense in natural the presence of Medicago than in the presence plant populations. While relatively few studies of native plants. Medicago also reduced the se- have investigated this possibility, we suspect it lection for resistance in native Lotus, however, may be a common phenomenon. In particu- which suggests that the presence of Medicago lar, it would be instructive to determine the altered the type of defense that was favored. scale at which vegetation heterogeneity influ- Because Medicago removal treatments did not ences these evolutionary responses and to affect total plant biomass, it appears that further investigate the mechanisms underly- 360 THE QUARTERLY REVIEW OF BIOLOGY Volume 81 ing the empirical patterns. For example, in Lau’s work, the type of defense that is favored may shift because: (1) the presence of Medi- cago alters the costs of tolerance and resistance in different ways; (2) the existence of genetic correlations between defense traits and other ecologically relevant traits, such as competitive ability; or (3) the relative benefits of the different defense strategies depend on the presence and abundance of alternate hosts.

The Plant Community’s Role in the Evolution of Insect Traits The microevolution of herbivore strategies and, in particular, how this process is altered Figure 2. Predicting Host Shifts by plant community structure has been rela- Conceptual model of how phenotypic differences tively little studied compared to the evolu- and physical association (or ecological opportunity) tion of plant defense. Although tradeoffs in between plants affect the likelihood of specialist her- fitness on alternate host plants has been the bivores host-shifting between those plants. Host shifts are most likely between plants that are phenotypically primary focus of studies on specialization of similar and that are consistently in close physical and herbivores, when the plant neighborhood is phenological association. Additional ecological oppor- considered, other possibilities emerge (see tunity arises from the novel host being of high food Tables 1 and 2). For example, local speciali- quality, abundant in the nearby environment, or a zation by generalist species, where one popu- habitat that is relatively free of enemies. (Modified lation tends to feed on one host plant while from Mooney 2003). another population in a different location feeds primarily on an alternate host plant, has logical constraints (Bernays 2001). When ex- long been reported, and such effects are amining phylogenies of closely related insect likely the result of variation in plant commu- herbivores, two patterns emerge: host shifts nity structure (Fox and Morrow 1981). Ad- occur onto either taxonomically related spe- ditionally, plant diversity may alter host cies (Becerra 1997; Janz and Nylin 1998; Mur- choice and use as well as availability of enemy- phy 2004) or species within the same habitat free space for herbivores. Finally, plant neigh- (Pappers et al. 2002a,b). For example, her- bors may also affect the evolutionary re- bivores of parasitic plants often have close sponse of herbivores to changes in host plant relatives that feed on the hosts of parasitic defenses. Below we outline several different plants (Anderson 1970; Mooney 2003). Al- possibilities of how plant complexity influ- though parasitic plants are usually taxonom- ences selection on herbivores, progress to ically quite distant from their hosts, they often date, and methodological suggestions. share chemical defense similarity (Adler 2000); therefore, host shifts may be facilitated ecological opportunity by both a shared chemistry and ecological op- The key concept for how the plant com- portunity. The reason why some lineages munity may influence insect evolution is mainly proliferate on taxonomically related “ecological opportunity” (Strong et al. 1984) plants while others shift to taxonomically un- (Figure 2), or how the presence of other related plants is still unclear, but it is likely plant species in the neighborhood provides due to both the propensity for egg-laying mis- an opportunity for both host shifts and diet takes by females and to physiological con- expansion. Whether these opportunities are straints during feeding. For instance, the leaf realized depends on multiple factors, such as beetle genus Galerucella has been shown to chemical similarity and genetic and physio- use taxonomically distant plants within the December 2006PLANT AND INSECT HERBIVORE INTERACTIONS 361 same or nearby habitats (e.g., Pappers et al. cause a larger mismatch between herbivore 2002b), and this may be related to their in- and host plant odor cues. For example, this ability to use long distance odor cues for host mismatch could particularly cause problems finding (Hamba¨ck et al. 2003), which in- for parasitoid species that use specific increases the probability of females landing on duced plant volatiles for locating herbivore nonhost plant species (Wiklund 1984). host species (Vet and Dicke 1992). The ability of an insect herbivore to host- Finally, the ecological opportunity afforded shift depends on whether its population con- by diverse plant communities extends to tains sufficient genetic variation, which may benefits of a diet mixing strategy. Some her- be linked to the diversity (and opportunity) bivores, including several Arctiid moth cat- of the plant community. For example, it has erpillars, are so-called toxic plant generalists. been generally predicted that herbivore pop- Individuals of such species typically feed on ulations experiencing a diverse host plant several plant species over the course of their community will retain a greater reservoir of lifetime, including hosts that are apparently genetic variability than herbivore populations quite noxious. Several hypotheses have been on single host plant species (Hawthorne put forth for why such apparent suboptimal 1997). If true, then herbivores from diverse choices are made (Singer 2001; Singer et al. plant populations may show a greater ability 2002; Singer and Stireman 2003). After reject- or rapidity in adapting to new host plants. ing alternative hypotheses, Michael S Singer The single test of these hypotheses, however, and colleagues have recently discovered that found no difference in the ability of the caterpillars of Grammia geneura sacrifice high dipteran leafminer (Liriomyza trifolii) to adapt growth by choosing a mixed diet that includes to novel hosts when replicate populations toxic plants, but that this strategy increased were maintained for 20 generations in mixed resistance against parasitoids (Singer et al. versus single host plant arenas (Hawthorne 2004). Thus, although generalist herbivores 1997). may find nutritionally adequate (or even su- While host shifts necessitate that an insect perior) resources in less diverse host plant is able to use the novel host as a resource, stands, there may be underappreciated tri- extending the resource base may not be the trophic benefits of diet mixing which can only primary fitness benefit from the host shift. be realized in diverse host communities. Several studies suggest that an ecological opportunity for enemy-free space on an alter- host plant abundance nate host plant may outweigh a fitness cost of reduced host plant quality (Bernays and Gra- The probability of taking advantage of eco- ham 1988). Two recent studies describe an logical opportunity will naturally increase both apparent host shift of relatively specialized with a diversity of options and with the relative herbivores onto plants taxonomically unre- abundance of nonhost plants. While host shifts lated to the primary hosts (Mira and Bernays and diet expansions are possible when novel 2002; Murphy 2004). The important result of hosts are rare, they are likely to be more com- these studies is that in the presence of pred- mon when nonhost plants are abundant, thus ators, larval fitness is greater on the novel providing substantial ecological opportunity. hosts than on the ancestral host; but, in the These possibilities have been extensively stud- absence of predators, larval fitness is greater ied by Michael C Singer and colleagues on on the ancestral host. It is unclear whether Euphydryas editha butterflies. Singer (1971) such enemy-free space mediated hosts shifts showed that oviposition preferences differed are more likely to occur in diverse compared among conspecific butterfly populations, and to less diverse plant communities, although suggested that these preferences might inter- this prediction stems from our discussion of act with the relative abundance of potential ecological opportunity. In addition, the eco- host plants to generate patterns of host logical opportunity for enemy-free space may use. Later work demonstrated this through be particularly large when host shifts involve extensive surveys and experiments of numer- taxonomically unrelated plants, as this would ous butterfly populations. At one site, a plant 362 THE QUARTERLY REVIEW OF BIOLOGY Volume 81 species that was not the most preferred by any population that increased preference for the insect (in choice tests) received 80% of the novel host. Quite amazingly, in many of these eggs, presumably because it was abundant populations where host shifts have occurred, and the preferred plant was rare (Singer et preference for the original host has been ev- al. 1989). At a second site, a plant species pre- olutionarily lost or severely reduced. Thus, ferred over all others by 25% of the butter- human-induced activities that have altered flies received only 5% of the eggs in the field, plant community composition have created presumably because of its rarity (Singer ecological opportunity for host shifts and evo- 1983). Examples in which the most abundant lutionary responses in insects. local host is not the preferred host suggest Because host plant abundance changes that variation among sites in relative density over time, so do ecological opportunities, and of the various hosts is not the only factor tied this may cause temporal dynamics in host to variation in host preference (Singer and shifts. This was discussed in the 1970s in re- Wee 2005). lation to the plant defense guild hypothesis, In this system, the importance of variable because such temporal changes may have re- plant abundance among sites is that it com- ciprocal effects on plant defense evolution. bines with genetic variation of both insect Peter Dolinger et al. (1973) suggested that a preference and plant resistance to generate Lycaenid butterfly (Glaucopsyche lygdamus), spatial variation in the pattern of plant-insect which utilizes six potential local hosts in Col- associations (Singer and Parmesan 1993). orado (all legumes), was prevented from spe- Plant abundance is apparently less important cializing on any one due to frequency depen- than plant quality to the evolution of insect dent selection (Figure 3). As any one plant preferences, but plant abundance interacts species evolved defenses, escaped herbivory, strongly with those evolved preferences to and became the dominant plant, selection produce observed patterns of egg deposition would favor the evolution of preference and and host use. Perhaps the strongest pattern counter adaptations by the herbivore for that for E. editha is that wherever the host plant plant, and thus the dominant plant would Collinsia torreyi occurs in large persistent eventually be suppressed by herbivory. There patches suitable for the complete butterfly would typically be a lag time in the subse- lifecycle, the butterfly is locally adapted to quent herbivore response; the herbivores have this as the preferred host (irrespective would still prefer the previously dominant of density). If this host is not sufficiently long- species even though a different species is now lived at a site, however, then the insects lay dominant (and represents ecological oppor- eggs on another host to which they then be- tunity in terms of an underused food source). come adapted, and essentially ignore C. torreyi. Ultimately, we expect that the herbivore will Where human activities have altered the be selected for increased preference and relative quality of available hosts, rapid evo- performance on this new abundant host lution of preference and diet has also ensued. (Figure 3). This evolutionary cycle of plant In one case, this alteration was the invasion escape and subsequent resource concentra- of an exotic host plant Plantago lanceo- tion would be countered by adaptation and lata (Thomas et al. 1987; Singer et al. 1993). short-term specialization by the herbivores. Although larvae from communities with and Nonetheless, long-term dynamics predict the without Plantago grew equally well on this maintenance of plant species diversity and re- novel plant, adult acceptability of Plantago has duced species-level specialization in the in- only evolved in populations with the novel sect. Frances Chew (1979) advanced a similar host. In a second case, logging caused a idea for the coevolutionary interaction be- change in environment that rendered an tween Pierid butterflies and their Brassica- abundant and suitable host phenologically ceous host plants; in communities with mul- available to the insects (Singer et al. 1993; tiple potential hosts, butterflies may show Boughton 1999). This environmental change local adaptation to one plant depending on resulted in genetic changes in the butterfly the relative abundance of others. December 2006PLANT AND INSECT HERBIVORE INTERACTIONS 363

et al. 2003). Although there are many hypotheses for the evolution of such complex life cycles, the dominant idea focuses on the max- imization of ﬁtness on host plants, where plant quality (and potentially enemy-free space) radically changes seasonally (Moran 1992). Anthony Dixon and Ranajit Kundu (1994) have further proposed that the evolution of host alternation is dependent on herbivores living in diverse plant communities. As evidence, they report that few (6%) aphids on “dominant” tree hosts in Britain are host- alternating; conversely, over half (58%) of Figure 3. Frequency Dependence in the aphids on “subdominant” trees are host- MultiSpecies Coevolution alternating. Dixon and Kundu speculate that Conceptual model of the frequency dependent se- climax woodland communities, composed of lection that promotes the maintenance of both plant and insect diversity, as suggested by the Plant Defense one or a few dominant species, provide little Guild Hypothesis (Atstatt and O’Dowd 1976). The ecological opportunity for the evolution of solid black line represents the abundance of plant spe- host alternation. cies A. Initially, when A is rare there are few herbivores Host alternation also has ecological and that prefer to feed on it (1); however, as A becomes evolutionary implications for the plant spe- relatively more abundant, the number of herbivores cies involved. Because both plant species are that prefer to feed on plant species A (dashed black required for the persistence of an insect line) increases (2). As the frequency of herbivore ge- population, herbivore attack rates on one notypes that feed on A increases, they decrease the host plant are likely tightly linked to those on population growth rate of A, allowing competing the other. If, for example, one host plant is plant species B (gray line) to increase in abundance (3). Again, after a time delay, the number of herbivore very abundant, it may boost herbivore popu- genotypes that prefer to feed on B (dashed gray line) lation growth rates, thereby increasing dam- begins to increase, due to selection on the insect her- age on the second host plant. Similarly, one bivores to preferentially feed on the most abundant can imagine that the two host plants are also host plant (4). This frequency dependent selection tightly linked evolutionarily, albeit indirectly. produces stable cycles of alternating plant (and her- If one host plant is highly resistant to the herbivore) abundance. bivore, it may depress herbivore population growth rates, thus decreasing damage levels on the second host. This second plant would host-alternation strategies then be released from intense herbivore pres- An extreme example of how ecological op- sure and may be under selection for reduced portunity and plant community interactions defense levels. Thus, the effects of one host may shape the evolution of insect life histories on the other may not depend only on is the host-alternation strategy. The herbi- presence and abundance, but also on its level vores are quite specialized, but usually re- of defense. While strong indirect effects be- quire two taxonomically and phenotypically tween plant species mediated by host- different hosts at different times of the season alternating herbivores seem plausible, we are (often woody host plants during spring and aware of only one study observing such inter- herbaceous plants during summer). Host al- actions. Carsten Thies et al. (2005) reported ternation is restricted to 10% of the some that densities of Rhopalosiphum padi aphids 4,000 species of aphids, and has also been re- on cereals were positively correlated with the ported from other hemiptera (e.g., leaf hop- proportion of neighboring noncrop areas pers and membracids) (Moran 1992) and a with Prunus padus (the winter host for the couple of diptera (Cook et al. 2002; Yukawa aphid). 364 THE QUARTERLY REVIEW OF BIOLOGY Volume 81

neural constraints hypothesis effects of plant heterogeneity on According to Elizabeth Bernays’s Neural insect counteradaptation Constraints hypothesis, diverse plant com- While the effects of the surrounding plant munities make host choice problematic for community on diet choice have received the herbivores, thereby imposing selection for spe- most attention, plant community heteroge- cialization (Bernays 2001). Although more neity can also interact with insect demogra- choices in diverse habitats may result in eco- phy to influence the rates of insect counter- logical opportunity for host shifts, in the short adaptation to plant defenses. In this scenario, term such plant diversity is suggested to im- the level of variation in the magnitude or type pose a greater strain on neural processing, of plant defense (either interspecific or intra- causing either inefficient decision making (ex- specific variation) interacts with insect demography to influence the intensity of selec- posing organisms to predation or other risks) tion on herbivore offensive strategies. This or poor quality decision making (choosing occurs because resistant plant genotypes suc- plants on which the herbivore has low fitness). cessfully depress insect population growth Despite limited direct support for more di- rates, while susceptible genotypes serve as res- verse plant communities imposing a different ervoirs for insect population growth. Because shape or strength of selection on herbivores the vast majority of insect population growth compared to less diverse communities, cir- occurs on susceptible genotypes, and because cumstantial evidence from mesocosm exper- insect traits that permit feeding on resistant iments is suggestive. Bernays (1999) reported genotypes can be costly, insect counteradap- that the whitefly (Bemisia tabaci) had lower tation to resistant plant genotypes may be performance in mixtures of host plants com- overwhelmed by the demographic vigor and pared to when with only the best of the hosts; competitive advantage of insect populations. observations demonstrated that in mixtures While this phenomenon has been docu- whiteflies moved more and switched between mented in agricultural systems and is com- plants more frequently compared to when monly applied to extend the lifespan of resis- with single plant species. The Neural Con- tant crop cultivars (Gould 2003), it may be straints hypothesis suggests that patterns, such rare in natural ecosystems. Because plants as the level of specialization, should vary with can also evolve in natural systems, one might community diversity. Although these patterns expect susceptible genotypes to be selected have not been investigated, examination of against and to continually decrease in fre- host races of herbivores from agricultural ver- quency, thereby eliminating the susceptible sus natural populations would provide an ex- refuges. If another selective force can main- cellent test. Specifically, if agricultural popu- tain low, but stable, frequencies of susceptible lations (i.e., evolving in low diversity habitats) genotypes, however, then this mechanism remain behavioral generalists while natural could occur in natural ecosystems as well. Such populations (i.e., evolving in higher diversity a case may be especially likely when the variation in susceptible versus resistant genotypes is habitats) are more specialized, then this would interspecific in nature and the susceptible spe- be consistent with the Neural Constraints hy- cies cannot be competitively excluded from pothesis driving specialization. These some- the community (Figure 3), or if external en- what counterintuitive predictions for choice vironmental forces alter the relative attractive- and host-use type experiments would need to ness of various host plants, as suggested by At- be followed up with behavioral, physiological, satt and O’Dowd (1976). Intraspecific cases in and fitness assays (Bernays 2001). In particu- which (1) tolerance and resistance are mutu- lar, the Neural Constraints hypothesis makes ally exclusive defense strategies and strongly these predictions about specialization for negatively correlated (Fineblum and Rausher preference as mechanisms to avoid ecological 1995) or (2) there is genetic variation in the pitfalls, as opposed to traditional perspectives strength of induced defenses (Gardner and on specialization that focus on physiological Agrawal 2002) could also possibly slow the evo- adaptations to plant defenses. lution of insect offensive strategies. December 2006PLANT AND INSECT HERBIVORE INTERACTIONS 365

The above examples document effects of mosaic coevolution (Thompson 1988, 1994, plant community variation on the evolution 1999). John Thompson argues that geo- of host preference or performance. However, graphic variation in the intensity of the plant- evolutionary responses in other traits could herbivore association interacts with patterns also occur. For example, if vegetation hetero- of gene flow to produce evolutionary “hot- geneity influences predation rates on the her- spots” (where the plant-herbivore interaction bivores, one might expect to observe altered is a tightly coevolved dynamic) and evolution- selection on antipredator behaviors of the ary “coldspots” (where the plant traits and herbivores. Vegetation heterogeneity may herbivore traits are mismatched and not also affect selection on traits such as dispersal tightly coevolved). While Thompson has ability and life-history characters (Carroll criticized diffuse coevolution as a catchall et al. 2003). Thus, the microevolutionary dy- phrase that trivializes coevolutionary pro- namics between plants and herbivores, and cesses (Thompson 1988, 1994, 1999), it seems the evolution of a wide variety of both plant apparent that diffuse selection can be a mech- and herbivore traits, may be predictably anism that generates geographic variation in shaped by plant community characteristics. the interactions between species. This reali- zation suggests that the concepts of diffuse Macroevolutionary Consequences of selection and geographic mosaics are indeed Plant Community Heterogeneity compatible. Most of the examples we cite are tests of As a preliminary example of how diffuse the hypothesis that selection on plant defense selection may generate geographic variation or insect feeding behavior is diffuse. Each of in plant-herbivore coevolution, Art Zangerl the plant examples in this paper illustrates and May Berenbaum (2003) have demon- that selection imposed on a plant by an her- strated that the plant defensive phenotype of bivore is not independent of the presence of wild parsnip (Pastinaca sativa) matches the other community members. This diffuse se- detoxification abilities of the parsnip web- lection may generate variation in the appar- worm (Depressaria pastinacella) in 12 of 20 pop- ent adaptations that plants have to herbivores ulations studied across Illinois and Wisconsin. and vice versa. In fact, this level of variation This matching is suggestive of reciprocal ad- in interactions was surmised 25 years ago, and aptation. In four populations, an alternative the result was a general prediction that the host, cow parsnip (Heracleum lanatum), was local community members will influence se- present, and in each of these populations lection on plant defense and host-plant spe- there was a “mismatch” between the level of cialization by herbivores, and that interac- plant defense and insect counterdefense. Al- tions may be highly geographically variable though these four populations with an alter- (Fox and Morrow 1981). These basic predic- nate host were not spatially independent (they tions imply that geographic variation in com- are regionally clustered), the authors argue munity composition will likely result in geo- that the presence of the alternate host may graphic variation in species interactions. disrupt reciprocal selection between the wild Thus, variation in community composition parsnip and the webworm. If this is the case, derived from both stochastic processes and then plant community members are acting as abiotic environmental conditions may play a agents of diffuse selection, which results in a role in promoting the genetic differentiation pattern of geographic variation in the coe- and local adaptation that are the first steps to volutionary interaction between two species. speciation. A definitive test would involve a reciprocal transplant study to assess whether differential geographic mosaics local selection has, in fact, occurred. Further work on the idea that community composition (and, therefore, species inter- local adaptation and speciation actions) is geographically variable has led to- Because vegetation heterogeneity can the formulation of the concept of geographic cause spatial variation in plant-herbivore in- 366 THE QUARTERLY REVIEW OF BIOLOGY Volume 81 teractions and variation in species traits, this populations on different hosts may represent heterogeneity could promote genetic differ- potential incipient species. A similar case has entiation and adaptation to local environ- been argued within the Galerucella nymphaea mental conditions. If selection is strong complex (Nokkala and Nokkala 1998). enough or if gene flow is disrupted for long Within this species complex, individuals feed- enough to promote reproductive isolation, ing on marsh species such as Comarum palustre then this vegetation heterogeneity, and the may breed in the laboratory with individuals resulting genetic differentiation, could result collected from water lilies (Nuphar and Nym- in speciation. For example, we might expect phaea). Interbreeding rarely occurs in the vegetation heterogeneity to promote specia- field, however, and hybrid larvae have re- tion in insects because different herbivore duced survival because of apparent larval ad- populations may become locally adapted to aptations for feeding on aquatic versus marsh different host plants, as suggested by the plants. concept of geographic mosaics. Populations of a walking-stick insect (Timema cristinae) that macroevolution and the escape use different host-plant species have evolu- and radiate model tionarily diverged in several traits including In an attempt to explain the diversification host preference (Nosil et al. 2002); divergent of plants and butterflies, Paul Ehrlich and Pe- selection for host adaptation has apparently ter Raven (1964) proposed a model that led to the repeated evolution of reproduc- strongly links the microevolutionary pro- tively isolated populations in this species. Sev- cesses discussed above to macroevolutionary eral of the best examples of recent speciation patterns. Their Escape and Radiate model of events involve insects feeding on different coevolution hypothesized that the evolution- host plants, where speciation (or at least host- ary innovation of a defense in plants results race formation) resulted from a host shift in freedom from attack, and this freedom onto an alternate host that is a common com- causes adaptive radiation of the plant lineage. munity member (Bush 1994; Nason et al. Similarly, they argued that the evolution of a 2002; Via and Hawthorne 2002; Stireman novel offensive trait (or counteradaptations et al. 2006). to plant defenses) will allow unencumbered In other cases, expansion to novel host exploitation of plants (Karban and Agrawal plants has occurred, followed by adaptive 2002), and ultimately adaptive radiation of changes in feeding traits. For example, over herbivore lineages onto a set of closely related the past 50 years, soapberry bugs have taken plants. Despite the broad appeal of this hy- advantage of ecological opportunity and col- pothesis and its lasting impact, the logical link onized several exotic plant species as novel between escape of plants from herbivory and hosts (Carroll and Boyd 1992). The soap- speciation is still unclear. The hypothesis is berry bugs feeding on novel hosts have di- that reduced herbivory allows for larger plant verged with respect to beak length, a trait that populations to colonize new habitats and be influences feeding ability on the different less prone to extinction, and for greater ge- food sources. Populations that have colonized netic variation available for selection. The lat- introduced plants with smaller fruits than the ter point is especially important as constraints original host have evolved shorter beaks, associated with adaptation (i.e., negative plei- while those that have colonized introduced otropy) to one selective agent may limit the species with larger fruits have evolved longer ability of plants to adapt to other novel envi- beaks. Although there is no current evidence ronments. If large persistent populations with that the host races are reproductively iso- high genetic variability are more likely to un- lated, populations on the different host dergo adaptive radiation than smaller popu- plants are locally adapted to their plants and lations with constrained genetic variability, the rarely interbreed because of large distances Escape and Radiate model may be reflected in between host plant populations (Carroll et al. nature. 1997, 1998). Thus, the soapberry bugs may be As far as the macroevolutionary patterns in the earliest stages of speciation, and the are concerned, there is some evidence that December 2006PLANT AND INSECT HERBIVORE INTERACTIONS 367 novel plant defenses are indeed associated erogeneity may shape the evolution of plant- with diversification. For example, Brian Far- herbivore interactions. rell et al. (1991) report that plant taxa with defensive latex or resin canals (e.g., Dussourd interdependency of plant and Eisner 1987) are more speciose than sis- and insect diversity ter taxa that lack these defenses; this pattern We believe that more work linking broad was consistent in 13 of 16 paired lineage com- patterns of plant diversity with insect diversity parisons. The reciprocal logic of adaptive ra- and attack rates is one of the first steps to dis- diation in herbivores following from the evo- cover the ecological effects (and potential lution of counteradaptations is strongly evolutionary outcomes) of variation in plant supported by the pattern that closely related diversity. Observational (Murdoch et al. 1972; insect species tend to consume closely related Hawkins and Porter 2003) and experimental plant species (Ehrlich and Raven 1964; (Siemann et al. 1998; Knops et al. 1999) stud- Strong et al. 1984). Although the specific of- ies have demonstrated a positive relationship fensive tactics that allow these radiations are between plant species richness in communi- poorly understood, the pattern has been ties and total arthropod species richness. found for diverse groups of butterflies ( Janz Similar work has recently been reported from and Nylin 1998) and specific lineages of bee- intraspecific genetic diversity in plant popula- tles (Becerra 1997). The likely radiation of tions (Wimp et al. 2004; Johnson et al. 2006). herbivore lineages onto closely related plant The work by Marc Johnson et al. (2006), in species will depend, at least in part, on the particular, demonstrates experimentally that ecological opportunity for the herbivores. In fine-scale intraspecific genetic diversity in other words, at least at a regional scale, there plant patches generates enough phenotypic must be related host plants available for col- variability to shape arthropod communities. onization. This work is unique in identifying a potential In some cases, the colonization and radia- coevolutionary feedback between plant ge- tion will occur irrespective of the relatedness netic diversity, enemy attack, and plant fit- of host plants available in the vegetation com- ness. Thus, when plant diversity (at any scale) munity. For example, after bananas invaded shapes the herbivore community, and the the Hawaiian Islands some 1000 years ago, a herbivores are important selective agents on species of Hedylepta moths adopted them as a the plant community, there is strong potential host plant (Zimmerman 1960). The moths for community-wide feedbacks. then radiated, and at least five species fed on The interplay between plant diversity, in- various introduced hosts (Zimmerman sect diversity, and herbivore attack rates is a 1960). Elwood Zimmerman speculated that complex and important area of research. this host shift and subsequent radiation re- While there tends to be a positive correlation sulted, in part, from changes in the plant between plant diversity and insect diversity, community: native host plants declining in there tends to be a negative relationship be- abundance due to human activity and being tween plant diversity and levels of herbivore replaced by bananas and coconuts. damage on focal plant species. These con- trasting patterns likely result from a discon- Future Directions nection between insect diversity and abun- While the empirical study of the evolution- dance that may be caused by either a greater ary consequences of plant community com- abundance of predators in diverse habitats position is just beginning, the accumulating (Enemies Hypothesis) or to decreased her- observational and experimental evidence bivore population growth rates and higher suggests that vegetation heterogeneity can be emigration rates from diverse habitats (Re- important not only to interactions among source Concentration Hypothesis) (Root plants, but also to interactions between plants 1973). Additionally, the host range of herbi- and their enemies. We outline emerging ar- vores (Andow 1991), search modality (Ham- eas of research on how plant community het- ba¨ck and Beckerman 2003; Hamba¨ck et al. 368 THE QUARTERLY REVIEW OF BIOLOGY Volume 81

2003; Bukovinszky et al. 2005), and the pos- versity on insect diversity that are somewhat sibility for positive feedback systems (Turchin more complicated than effects on productiv- 1989; Hamba¨ck and Englund 2005) may pro- ity and involve iterative resampling from a vide other predictive axes. First, reduced at- subset of the data to create expected datasets, tack rates in diverse habitats are always pre- which can be compared to the observed data. dicted when the higher diversity does not The examination of underlying mecha- provide additional food sources. This effect nisms in these examples suggests that all con- may be particularly strong for species, such as sequences of plant diversity may not be equal. many generalist herbivores, that do not use Some mechanisms, such as olfactory interfer- long-distance cues for identifying host plants. ence, are likely to be connected to quite spe- Second, increasing plant diversity is predicted cific plant species, while other mechanisms, to affect visually searching herbivores more such as visual interference, may depend on than species using odor cues because odor general plant characteristics (Hamba¨ck and cues are less distorted in complex habitats. Beckermann 2003). Correct identification of Third, positive feedback systems, such as underlying mechanisms is therefore pivotal attraction to already damaged plants, may for understanding the role of vegetation amplify small differences in attack rate be- heterogeneity in modifying plant-herbivore tween plants in simple and diverse habitats evolution. (Hamba¨ck et al. 2003) that have arisen for scale dependent consequences of other reasons. One reason for this is that if plant diversity the first herbivores that arrive on plants have a slightly higher probability of landing on Effects of vegetation heterogeneity likely plants in simple habitats, these plants would vary greatly depending on spatial scale. A re- then function as magnets for later arriving cent meta-analysis illustrates this phenome- herbivores (Turchin 1989). non; Riccardo Bommarco and John Banks Several examples also exist where focal plant (2003) found that experiments investigating species receive more herbivory in high com- the relationship between plant diversity and pared to low diversity plots (Prieur-Richard herbivore abundance were more likely to detect a negative correlation when treatment et al. 2002). In these cases, the mechanisms plots were small (less than 16 m2) compared linking plant diversity and insect diversity may to when plots were larger. The underlying also explain the patterns between plant diver- mechanism is likely that selection behavior by sity and herbivore attack; the focal plant spe- herbivores is most strongly expressed at small cies may receive more herbivory simply be- spatial scales. For instance, fine-scale varia- cause an important herbivore is more likely tion in vegetation heterogeneity may have to occur in diverse plant communities (Figure large impacts on herbivore host use because 1). This may result because of plant diversity herbivores can move across patches allowing (i.e., more resources), but could also result for greater opportunity to choose appropriate from other mechanisms. For example, an al- host plants and communities (Bommarco and ternate host plant species that causes associ- Banks 2003). In contrast, at larger spatial ational susceptibility for the focal plant may scales, insect herbivores may be unable to se- be more likely to occur in a high diversity en- lect among host plants because of limited vironment (Prieur-Richard et al. 2002; Aquil- knowledge or low dispersal ability. In large ino et al. 2005). While the effects of plant di- patches, this has the consequence that differ- versity are difficult to separate from those of ences among monospecific and mixed plots plant community composition, several exper- is strongest at the border between these areas. imental designs have been proposed to dif- For instance, studies on turnip root flies (De- ferentiate between these confounding effects lia floralis) indicate that the egg-laying rate on (Loreau and Hector 2001; Mulder et al. border plants in monocultures is nearly 200% 2001). Johnson et al. (2006) have modified higher than neighboring plants in polycultu- these methods to allow for tests of plant di- res; egg-laying rates on plants at the center of December 2006PLANT AND INSECT HERBIVORE INTERACTIONS 369 the same monoculture plots is only 70% neity occurs should be an important consid- higher than on center plants in the polycul- eration for studies investigating relationships tures (Bjo¨rkman, Ra¨mert, and Hamba¨ck un- between plant community dynamics and her- published data). This scale-dependent pattern bivore communities. occurs because of the movement behavior expressed by females when encountering unsuit- vegetation heterogeneity and able host plants. genetic variability In addition to the scale-dependencies in- Recent studies have illustrated that plant volved in herbivore selection behavior, differ- community diversity tends to be positively ences between small and large plots may also correlated with intraspecific genetic variabil- be caused by differences in the importance of ity (Vellend and Geber 2005). It is currently herbivore selection behavior versus local unclear as to whether this correlation results growth (Hamba¨ck and Beckerman 2003). from a causal process (i.e., community diver- While patterns at small spatial scales may be sity increasing genetic diversity or vice versa) driven by insect preference, patterns at larger or whether similar mechanisms drive diversity spatial scales, where patch choice is not an patterns at both interspecific and intraspe- option, may be driven by insect performance. cific levels (Vellend and Geber 2005). How- Accordingly, experiments performed at small ever, if vegetational heterogeneity does caus- spatial scales may only be able to detect the ally impact intraspecific genetic variation, short-term dynamics that result from emigra- then it may be another mechanism by which tion and immigration and individual choice plant community composition influences the in patch use. In contrast, experiments per- evolution of plant-herbivore interactions. For formed at large spatial scales may be able to example, many studies have demonstrated detect the longer-term dynamics that result that intraspecific variation alone can influ- from differential insect population growth ence herbivory rates (Fritz and Simms 1992). rates, but may be less able to detect short- Furthermore, work by Johnson et al. (2006) term dynamics. In all cases, the relevant scale illustrates that the influence of plant intraspe- of investigation depends on both the level of cific genetic variation on herbivore commu- heterogeneity in the plant community and nity dynamics may even feed back to affect the dispersal ability of the insects. For exam- the plant community. The missing link in this ple, Koricheva et al. (2000) report that only process is determining whether vegetation the most sessile insects responded to small- heterogeneity is a driving force that causally scale plant diversity manipulations. impacts intraspecific diversity. Ultimately, fac- Scale is also relevant to the effects of vege- torial experiments in which both intraspecific tation heterogeneity on insect evolution and diversity and interspecific diversity are manip- diversification. For example, gene flow be- ulated are needed to ascertain the causality tween insect populations on different hosts of these relationships and how the two levels may be much less when the varies over larger of diversity independently, and interactively, spatial scales than when plant community var- influence plant-herbivore dynamics. As an ies over larger spatial scales than when varia- initial step, Boothe and Grime (2003) have tion is fine-scale in nature. Thus, variation demonstrated that plant species diversity is over larger spatial scales may promote the di- more likely to be maintained in genetically vergence between insect populations that is diverse plots compared to genetically uni- the first step toward reproductive isolation form ones. Theory predicts a similar relation- and speciation. In contrast, however, varia- ship (Vellend 2006). The consequences of tion at intermediate scales may increase the this dynamic for relationships with herbivores speed of speciation due to reinforcement, represent an open avenue for research. though this remains controversial (Servedio and Noor 2003). In short, both the underly- plant defense variation in different ing mechanisms and the actual patterns ob- community types served may differ depending on spatial scale. In addition to quantitative genetic studies to Consequently, the scale at which heteroge- investigate microevolutionary patterns, obser- 370 THE QUARTERLY REVIEW OF BIOLOGY Volume 81 vational studies of defense traits in communi- troduced congeners are not only likely to ties of differing composition can potentially share similarities in resource use, but in chem- provide evidence for evolutionary responses. ical and physical defenses as well, they are While caution must be exercised since, with- likely to be attacked by common consumers out manipulative experiments, one cannot be (Connor et al. 1980). We predict that in certain whether vegetation heterogeneity is communities with native congeners, host the mechanism responsible for any observed shifts by native herbivores onto introduced differences, we find work that links geographic plants are more likely than in communities variation in defense levels with variation in without native congeners. Evidence that native plant community composition (e.g., Zangerl herbivores frequently host-shift onto intro- and Berenbaum 2003) highly suggestive and duced plants is accumulating (Connor et al. enticing. Future studies should examine the 1980; Agrawal et al. 2005), although whether defense phenotypes of plants in multiple such host shifts are associated with the pres- community types and consider reciprocal ence of congeneric neighbors remains to be transplant experiments to identify the prob- determined. able selective agents responsible for variation Plant diversity, in general, is also often as- in levels of defense. sociated with invasion resistance. This is typically thought to occur because a more diverse community implies that a greater percentage plant invasions and community of available resources are already being used, heterogeneity leaving little empty niche space for an exotic Situations in which community composi- plant to invade. However, insect herbivores tion is being inadvertently manipulated over could also contribute to this pattern. If insect broad geographic scales, such as by changes diversity is greater in high diversity plant com- in agricultural practices or by biological in- munities, then the probability of a host shift vasion, provide excellent opportunities to onto the colonizing exotic may be more likely, monitor evolutionary changes in insects and thus limiting its invasion success. The first their host plants. For example, Chew (1979) study to address this hypothesis demonstrated speculated that the selective pressures on the that plant diversity increased herbivory on a Brassicaceous host plants she studied would colonizing exotic species, and that this in- likely differ following invasion by the exotic creased herbivory resulted in decreased dem- crucifer Thlaspi. Several other examples of in- ographic vigor of the exotic (Prieur-Richard vasive plants that apparently alter attack on et al. 2002). Furthermore, these results were natives have recently emerged (Zimmerman driven by functional group composition, and 1960; Thomas et al. 1987; Carroll and Boyd the presence of one unrelated family contrib- 1992; Solarz and Newman 1996; Rand and uted most to the increased herbivory ob- Louda 2004; Lau and Strauss 2005; Russell served in high compared to low diversity and Louda 2005; Lau 2006). We believe that plots, rather than the presence of closely re- the study of plant-herbivore interactions in lated confamilials. A broad survey investigat- both invaded versus non-invaded sites and in ing herbivory on noninvasive exotic species introduced versus native habitats are “natural versus highly-invasive exotics could shed light experiments” that provide interesting re- on whether host shifts by native (or intro- search opportunities. For example, Darwin duced) herbivores can influence the invasion and others have suggested that among intro- potential of exotic plants, and whether the duced plants, those lacking native congeners composition of the plant community influ- should be the most likely to flourish because ences this process. The only study to attempt of the lack of very similar competitors (Dar- to link herbivore host shifts with invasiveness win 1859; Rejmańek 1999; Daehler 2001). confirms the first part of this prediction; This hypothesis can be extended to the ef- highly invasive species received less herbivory fects of phylogenetic relatedness on plant- than less invasive exotics (Carpenter and herbivore interactions. Because native and in- Cappuccino 2005). December 2006PLANT AND INSECT HERBIVORE INTERACTIONS 371

Conclusions of these evolutionary effects are mediated by Given the myriad ways in which vegeta- tritrophic interactions, thus implicating an tional heterogeneity can influence the ecol- intertwining of variation in both the plant ogy of plant-herbivore interactions, the evo- community and animal community interac- lutionary effects of such heterogeneity are tions. Finally, we have outlined several open also likely pervasive. Indeed, much of what we hypotheses (Tables 1 and 2), from the impact have reviewed indicates not only strong ef- that vegetation heterogeneity has on the fects of plant community heterogeneity on evolution of the host-alternation life-history herbivores, but also provides feedbacks that strategy (and vice versa) to the importance of reshape the plant community. While studies frequency dependent coevolutionary inter- involving multiple interactors rapidly become actions. The reality of community ecology cumbersome and difficult to manipulate, par- thus represents an important frontier for ticularly when combined with the large sam- understanding the evolution of plant-insect ple sizes necessary for traditional quantitative interactions. genetic studies, observations and experiments at several scales can help to illuminate acknowledgments important patterns. Existing evidence suggests that competing plants alter selection We thank Marc Johnson, Marc Lajeunesse, Kailen Mooney, John Parker, Mike C Singer (University of (via various mechanisms) by herbivores on Texas), Mike S Singer (Wesleyan University), and plant defenses. Likewise, host shifts, host race Christer Wiklund for providing helpful comments and formation, and possibly speciation in herbi- discussion. Our research is supported by NSF DEB- vores are tied to plant community structure. 0447550 (AAA, www.herbivory.com), by NSF IBN- These generalizations are no small victory for 0206601 ( JAL and SY Strauss), and by the Swedish evolutionary ecology; they reject simple pair- Research Council for Environment, Agricultural Sci- wise interactions as being all-important and ences and Spatial Planning (FORMAS to PAH). JAL is have led to predictions for when and why currently supported by NSF IOB 0620318 to P Tiffin, host shifts are likely to occur. At least some R Shaw, and P Reich.

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