Evolution of Plant Defenses in Nonindigenous Environments

ANRV397-EN55-23 ARI 2 November 2009 12:23

Evolution of Plant Defenses inNonindigenous EnvironmentsColin M. Orians1,2 and David Ward3

1Department of Biology, Tufts University, Medford, Massachusetts 02155;email: [email protected] of Ecology, Swedish University of Agricultural Sciences, Uppsala S-750 07,Sweden3School of Biological & Conservation Sciences, University of KwaZulu-Natal, Scottsville3209, South Africa; email: [email protected]

Annu. Rev. Entomol. 2010. 55:439–59

First published online as a Review in Advance onSeptember 8, 2009

The Annual Review of Entomology is online atento.annualreviews.org

This article’s doi:10.1146/annurev-ento-112408-085333

Copyright c© 2010 by Annual Reviews.All rights reserved

0066-4170/10/0107-0439$20.00

Key Words

exotic plants, invasions, enemy release, evolution of increasedcompetitive ability, generalist and specialist herbivores, resourceavailability

AbstractExotic plants provide a unique opportunity to explore the evolutionof defense allocation in plants. Many studies have focused on whetherenemy release leads to a change in defense allocation. Little researchhas focused on induced defenses and on how resource availability in thenonindigenous range might cause evolutionary shifts in defense trait al-location. We examine (a) the major evolutionary hypotheses predictingdefense expression in plants, (b) the hypotheses explaining defense evo-lution of exotic species, and (c) the importance of geographic variationin ecological interactions to defense evolution (geographic mosaics). Inaddition, we review the strengths and weaknesses of experimental ap-proaches, present case studies, and suggest areas that deserve furtherattention.

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Exotic plant: a plantthat has been broughtto a new area

Nonindigenousrange: areas whereexotics are outsidetheir native range

Tolerance: traits thatreduce the fitness costsof damage

EXOTIC PLANTS INNONINDIGENOUSENVIRONMENTS

The abundance of exotic plant species is steadilyincreasing, and in some nonindigenous areasthey represent nearly 50% of the total numberof plant species (66). Because many exotic plantsare invasive and cause economic and/or ecolog-ical damage in the nonindigenous range (69),there is tremendous interest in understandingthe factors that determine the abundance anddistribution of exotic species (82).

Exotic species also provide invaluable op-portunities to test ecological and evolutionaryhypotheses (19, 88) (Supplemental Table 1,follow the Supplemental Material link fromthe Annual Reviews home page at http://www.annualreviews.org). Of these, the most widelytested hypotheses are Enemy Release, Evo-lution of Increased Competitive Ability, andNovel Weapons. Although tests of ecologicalhypotheses dominated early studies, the num-ber of studies testing evolutionary hypotheseshas increased and such studies are facilitated bythe fact that we often know when these specieswere introduced and where they came from (36,52, 55, 70, 71, 126, 128).

In this review, we examine the evidencefor defense evolution in exotic plant species,noninvasive or invasive, after introduction intononindigenous habitats that often, but not al-ways, have lower herbivore pressures. Becausemost of the research to date has been on theevolution of resistance traits, as opposed to tol-erance traits (130), our review focuses on resis-tance. Although our primary goal is to examinehow changes in herbivore pressures (specialistsor generalists) might have caused shifts in de-fense expression, too often researchers ignorethe fact that the abiotic environment can leadto evolutionary shifts as well. Plant-pathogeninteractions are also important (77) but are notreviewed here. Many of the same principles,however, might also apply to these interactions.

Our review is structured as follows. First,we briefly describe current hypotheses for theevolution of resistance traits in plants. We

emphasize that the biotic and abiotic envi-ronment can select for changes in defense.Second, we briefly review the major hypothesesconcerning the success of exotic plants andfocus on those that are most relevant todefense evolution. Third, we discuss howenemy pressures and resource availability differamong populations. We take a biogeographicalapproach because selective pressures differwithin and among regions (5, 103). Finally, wereview the emerging patterns and focus on afew well-studied systems to illustrate that theoutcomes of defense evolution in exotic plantsdepend on the ecological context.

EVOLUTION OF DEFENSE

Studying the evolution of defense traits in ex-otic plants requires an understanding of currenthypotheses and potential constraints (geneticconstraints or trade-offs). In this section, wehighlight key features of each.

Defense Evolution Hypotheses

The most commonly invoked defense hypothe-ses are those that focus on differences in herbi-vore pressures, such as Optimal Defense, andthose that incorporate or focus on differencesin the resource environment, such as ResourceAvailability and Growth-Differentiation Bal-ance. Today, Optimal Defense and ResourceAvailability are the most widely cited evolu-tionary hypotheses (43, 97). Below, we brieflyreview key predictions of these hypotheses andemphasize that both enemy pressures and theresource environment are critical to studyingthe evolution of chemical or morphological de-fenses in exotic plants.

Herbivore pressures. Optimal Defense (OD)posits that defenses are costly to produce, andtherefore allocation to defense should be pro-portional to the risk of attack, the value of a par-ticular tissue, and the availability of resourcesto produce the defenses (97). Measuring costsis not simple and early reviews suggested thatcosts were relatively rare (6), but more recentreviews suggest that costs, direct or indirect, of

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Supplemental Material

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http://arjournals.annualreviews.org/article/suppl/10.1146/annurev-ento-112408-085333?file=en-55-orians.pdf


mechanical defenses and chemical defenses arecommon (25, 99). The fact that valuable tis-sues are often more defended (127) and thatpopulations with lower herbivore pressures areless defended (65, 78, 118) further indicate thatcosts may be common. Most studies of defenseevolution in exotic plants have focused on ODbecause herbivore pressures were expected tobe lower.

Escape from native herbivores, however,does not always lead to lower defense alloca-tion in exotic plants. Lower defense allocationdepends upon the fitness value of the tissue,the cost of the defense trait, the degree of mis-match between plant defenses and the counter-defenses of resident herbivores (i.e., chemicalnovelty; 109), the abundance of generalist ver-sus specialist herbivores, the resource environ-ment, and the level of defense exhibited by thenative plant species in the nonindigenous envi-ronment. Change should be less in tissues thatcontribute less to fitness, and it is only in thepresence of mismatches (behavioral or physi-ological) that lower defenses are expected toevolve. In the absence of mismatches, an ex-otic species would be expected to maintain itsdefense levels, or even increase them if the resi-dent species in the nonindigenous environmenthave higher defense levels.

Specialist and generalist herbivores often re-act in different ways to specific plant defenses(81). Toxins (often referred to as qualitativedefenses) such as glucosinolates and alkaloidsare effective against generalist insect herbivores(81). Some toxins deter specialist herbivores,but others are easily detoxified and used by spe-cialists as feeding or oviposition cues (23, 67,81). Quantitative digestibility-reducing com-pounds such as polyphenols and lignins deterboth specialist and generalist herbivores. Manymammalian herbivores are negatively affectedby polyphenols, even though they can reducethe impact of polyphenols by secretion of pro-line from their salivary glands (73).

Because generalist and specialist insectspecies can exert opposing selective pressures,evolutionary changes in plant chemistry dependupon the relative abundance of each type of

Mechanical defenses:physical defenses suchas trichomes or thornsthat may deterherbivores

Chemical defenses(or secondarymetabolites): organiccompounds that aregenerally not involvedin growth,development orreproduction

Mismatch: acondition in whichtraits of the nativeherbivore preventexploitation of anexotic plant

Specialist herbivore:herbivores that usechemical defenses as acue to locate preferredhost plants or use aschemical defenses intheir own interactionswith predators

Generalist herbivore:polyphagousherbivores that usemultiple plants species

Constitutivedefenses: defensetraits that are alwaysexpressed in a plant

Induced defenses:defense traits that aresynthesized ormobilized in responseto damage

species (Figure 1). Assuming that exotic plantsexperience attack by native generalist herbi-vores but are largely free of attack from spe-cialist herbivores (29), concentrations of planttoxins could increase in the introduced range,rather than decrease as is typically assumed(Figure 1a), and result in greater resistanceto generalist herbivores (51, 59). Lower invest-ment in toxins would be expected only follow-ing escape from both generalist and specialistherbivores. Escape from generalists and spe-cialists is also expected to result in the evo-lution of reduced investment in quantitativedefenses and increased allocation to growth(Figure 1b).

In addition to constitutive defenses, plantscontain many inducible defenses. Surprisingly,few other studies have examined induceddefenses in exotic plants (24, 37). Inducibledefenses are expected to evolve if the cost ofdefense is high and attack frequencies are low(25), just the conditions one might expect inexotic plants. Cipollini et al. (24) compareddefense levels in exotic and native populationsof Alliaria petiolata (Brassicaceae). They pre-dicted that because A. petiolata lacks specialistherbivores and is largely free from attackby generalist herbivores, exotic populationswould have lower constitutive levels but exhibitgreater inducibility. Glucosinolates fit thisprediction, but other defense traits did not.

Resource environment. The Resource Avail-ability Hypothesis is an evolutionary hypothesisthat integrates the effect of the abiotic environ-ment. It is postulated that species that evolve inresource-limiting environments have low max-imal growth rates and invest more in defense(owing to high cost of leaf replacement). Incontrast, species that evolve in high-resourceenvironments have high maximal growth rates,invest less in defense, and are more tolerantof damage (owing to the low cost of leaf re-placement) (26). Many empirical studies havedemonstrated that species in low-resource en-vironments have low intrinsic growth ratesand invest more in defense (38, 74). Recently,Fine et al. (38) performed a phylogenetically

www.annualreviews.org • Evolution of Plant Defenses in Nonindigenous Environments 441

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Toxins used in host selection by specialists

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Figure 1Differential selection on plant resistance traits in the native and introducedrange. Fitness functions of (a) toxins (qualitative defenses) used by specialists tolocate hosts and of (b) quantitative defenses (effective against generalists andspecialists) when herbivores and competitors are absent (solid gray lines). Theassumed higher cost of quantitative defenses, relative to toxins, is indicated bythe steeper fitness function. (a) In the native range, toxins are expected to bemaintained at intermediate levels owing to opposing selection exerted byspecialist and generalist insect herbivores (dashed blue arrows). The absence ofspecialists in the introduced range is expected to lead to an increase in toxins(solid blue arrow). (b) In the native range, quantitative defenses are expected tobe maintained at intermediate levels (dashed blue arrows) owing to opposingselection exerted by herbivores and plant competitors (selection for more rapidgrowth). The reduced enemy pressures in the introduced range are expected toresult in reduced allocation to defense (solid blue arrow) and therefore greaterallocation to growth. Adapted with permission from Reference 81.

controlled reciprocal transplant experiment,using pairs of tropical congeneric species fromeither nutrient-poor white sand or nutrient-rich clay, and found, as expected, that white sandspecies had intrinsically lower growth rates, in-vested more in defenses, and suffered greatermortality following defoliation. Although theabundance of herbivores did not differ betweenthe white sand and clay habitats, white sandspecies were more resistant to herbivory, andherbivore exclusion had little effect on theirgrowth. Similarly, Haugen et al. (44) showedthat stress-adapted populations of Boechera hol-boellii (Brassicaceae) grew more slowly and pro-duced more glucosinolates. We are not aware ofan exotic plant study that attempted to quantifythe effect of the resource environment on theevolution of defense traits.

Thus, we suggest that researchers studyingdefense evolution in exotic plants should go be-yond quantifying differences in herbivore loads,and quantify whether resource availability andthe cost of damage differ between the native andthe nonindigenous range. When resources aremore available in the nonindigenous environ-ment, lower defense allocation could evolve ifthe relative cost of leaf replacement were low(attack rates could be even higher!). Severalfactors may result in higher resource availabil-ity in the nonindigenous environment: morenutrient-rich soils, lack of competitors and thusgreater access to nutrient pools, or species traitsthat allow exotic plants to monopolize access tonutrients.

The abiotic environment (e.g., nutrients,light, water) also influences defense expres-sion and these phenotypic differences mightbe adaptive. Several hypotheses have beenproposed to describe this plasticity in defenseexpression, including the Carbon-NutrientBalance Hypothesis (16) and the Growth Dif-ferentiation Balance Hypothesis (45). Althoughthe two hypotheses lead to different predictions(especially at low resource availability), theywere developed to explain that gradients inresource availability can alter defense expres-sion. Unfortunately, the concentrations ofindividual secondary metabolites often do not

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change in ways predicted by either hypothesis(41, 43), making a priori predictions unreliable.Because environmental effects are ubiquitous,care must be taken when interpreting changesin defense allocation in exotic plants in thefield.

CONSTRAINTS ON DEFENSEEVOLUTION

Genetics of Defense

Although the absence of genetic variation mayconstrain evolution, this does not appear to bemore common in exotic species. Most studieshave documented similar or higher levels ofgenetic variation in the nonindigenous range(36, 52, 71), and this is due in part to re-peated introductions (36, 70, 106). As a result,founder effects and population bottlenecks arerare (83, 106). Nonetheless, exotic populationsmay differ genetically from one another (52).Hybridization is likely to generate even greaterdiversity in growth and resistance traits amongexotic species (11).

In general, plants contain significant geneticvariation in chemical (43) and morphological(7, 79, 104) defense traits (see Reference 79for a counterexample). Therefore, genetic con-straints on the evolution of defenses are likelyto be relatively rare in exotic plants.

Trade-offs

It is assumed that it is costly for a plant topossess more than one type of defense becausethere are likely to be negative correlations (i.e.,trade-offs) between investments in growth andreproduction and secondary metabolism (56,93, 99, 119). Plants may invest in more thanone type of defense (119) and negative correla-tions may exist between different types of de-fense. Indeed, Silvertown & Dodd (93) haveshown, in a phylogenetically controlled studythat there is a significant negative correlationbetween alkaloid and tannin production. Thenature of trade-offs between different types ofdefenses, however, may depend upon resource

availability (119) (Supplemental Appendixand Supplemental Figure 1).

Overall, trade-offs between different de-fense types are not common. Koricheva et al.(57) performed a meta-analysis of 31 studiespublished from 1976 to 2002 and showed thatthere was no overall negative correlation be-tween different defensive traits in plants. In fact,correlations between defensive traits rangedfrom positive to negative and depended onthe types of co-occurring defenses used by theplants involved. The only evidence of a trade-off occurred between constitutive and inducibledefenses. Although trade-offs are possible, wecannot assume that exotic plants will be con-strained in their defense evolution.

HYPOTHESES INVOKEDTO EXPLAIN THE SUCCESSOF EXOTIC PLANTS

The focus of this review is on defense evolutionin exotic plants, invasive or noninvasive. Never-theless, it is useful to review the factors that havebeen proposed to explain the success of exoticplants (what makes them invasive). They are(a) enemy release (herbivores or pathogens),(b) biotic resistance, (c) novel phytochemistry(novel weapons is a subcategory), (d ) emptyniche, (e) propagule pressure, and ( f ) evolu-tion of increased competitive ability (EICA)(2, 9, 46). Below we focus on those factors webelieve are most relevant to defense evolution.

Enemy Release

The Enemy Release Hypothesis (ERH) is themost thoroughly studied hypothesis, especiallyin relation to herbivory. ERH is premised on theassumption that (a) herbivores regulate plantpopulations, (b) herbivore pressures, especiallyspecialist herbivores, are lower in the non-indigenous range, and (c) exotic plants bene-fit from reduced herbivore regulation, resultingin greater population growth relative to nativespecies (54).

Lower herbivore pressures, especially byspecialists, are common in the nonindigenous



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range (3, 62, 122, but see 32). The relativeabsence of specialists is a function of threefactors. First, specialist herbivores are rarelyintroduced with the plant. Second, special-ists in the new environment seldom switchhosts. In fact, most herbivores that consumeexotic species are generally externally feedinggeneralists drawn from the resident herbivorecommunity (3, 100). Third, when exotics firstarrive they are invariably rare, and specialistenemies are relatively uncommon on rarespecies compared with widely distributedspecies (100). As exotic species become morecommon and widely distributed (14), nativeherbivore populations are likely to adapt toexotic hosts (92, 94), causing increased enemypressures in the nonindigenous habitat (100).These changes in enemy pressures are likely toselect for new defense genotypes (81).

Herbivore pressures on sugarcane, Saccha-rum officinarum (Poaceae), offer the best evi-dence that enemy pressures change as exoticspecies become more widespread (101). Sugar-cane is native to New Guinea and has been in-troduced into many tropical regions, as early as1000 bc into India/Pakistan (101). Strong et al.compared the number of arthropod herbivoreson sugarcane (for 51 regions) relative to areaunder the crop, time since the crop was first es-tablished, and latitude (proximity to the equa-tor). They found a strong log10 species richnessversus log10 area effect (r = 0.78), establishingarea under cultivation as the most important de-terminant of herbivore richness. Neither time( p = 0.229) nor latitude ( p = 0.896) had a sig-nificant effect. In addition, we used their dataand found that the number of arthropod herbi-vores was higher on mainlands than on islands(49.8 and 33.0, respectively). Lower herbivorepressures on islands can lead to lower alloca-tion to defense (see Biogeography of Defense:General Patterns, below).

We ran an analysis using Scopus as a databaseand found that 31 studies provided evidence insupport of ERH and 12 studies were unable todo so. Some studies documented even higherabundance of generalists in the nonindigenousrange (29). A review by Liu & Stiling (63)

indicates that, on average, herbivore speciesrichness and the number of specialists andendophagous herbivores are generally lowerfor exotic species, a pattern consistent withERH. Their analysis on damage rates, however,was inconclusive. Their meta-analysis, usingHedges’ d as an index of effect size, suggests thatdamage rate fits ERH only when they used a lessconservative confidence interval. [Hedges’ d isthe difference between the amount of damageon exotics in the presence and absence of nativeenemies, measured in units of standard devia-tions (42, 61)]. Levine et al. (61) did a similarreview of biotic resistance, the capacity of thebiotic community to keep out exotic species,and found a significant Hedges’ d for theeffects of herbivory. Moreover, the effect ofherbivores on exotic establishment and perfor-mance was higher and similar, respectively, tothe effects of competitors. This finding indi-cates that herbivores are a strong selective agentfor exotic plants. If ERH is to explain invasionsuccess, it is important to show that invasiveexotic species have a lower herbivore load(or species richness) than noninvasive exoticsdo. To date, the evidence for this is equivocal(21, 50, 64).

There may be biases in the literature on en-emy release. First, many of the early studies ofERH focus on finding suitable biological con-trol agents. Those that did not find a suitable bi-ological control agent may not have been pub-lished (the so-called file-drawer problem, e.g.,42, 89), and thus there may be fewer (negative)results published on the herbivore communitiesof these exotic plants. Second, studies of ERHtend to focus on leaf-feeding herbivores whileignoring those that cause extensive mortality ofseedlings (e.g., slugs and snails). More studiesduring this developmental stage are needed.

Evolution of IncreasedCompetitive Ability

Blossey & Notzold (9) have predicted that if ex-otic species experience lower enemy pressures,they will evolve to allocate fewer resources todefense and more to growth and reproduction

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and thus become more competitive (i.e., EICA)(see also 54). This outcome depends not onlyupon differential herbivore pressures, but alsoon the existence of a trade-off between growthand defense.

Relatively few studies have directly mea-sured changes in defense allocation (24, 80, 86),likely indicating that the defense traits mostworth measuring are not always clear. Multiplestudies suggest that exotic populations are moresusceptible to herbivory than their native coun-terparts (9, 31, 70, 123; but see 59), as would beexpected following reduced defense allocation.Nonetheless, support for this trade-off-basedhypothesis is equivocal. In a 2005 review (11),only 7 of 17 studies supported the full predic-tions of EICA. In our subsequent analysis (on 17additional studies published since 2005), only 5of 17 studies have supported EICA. A numberof these, however, focused on the same species(by the same investigators), and if we eliminateduplicates only 2 of 11 were supportive. Oftenstudies obtained support only for one aspectof the hypothesis. For example, higher com-petitive performance has been shown in exoticpopulations of several species (9, 60, 120, 123,130), but not in others (39, 70, 76, 113, 121).In fact, some exotic populations were less com-petitive than native populations (12, 29, 107).This might be expected if these exotic plantswere adapting to a low-resource environment.In summary, EICA infrequently explains thesuccess of exotic species and suggests that otherfactors contribute to the evolution of growthand defense.

Enemy Release andHabitat Productivity

The resource hypothesis proposes that colo-nization by plants is facilitated by high resourceavailability (33). Resources are considered im-portant for invasion because correlations havebeen shown between invasion and disturbance,which can increase resource availability eitherdirectly by altering nutrient availability or in-directly by limiting resource uptake by com-petitors (10, 33, 47). Experimental increases in

resource availability have provided direct sup-port for the resource hypothesis (R) (48).

Blumenthal (10) has modified ERH as R-ERH to indicate a causal relationship betweenresource availability and the Enemy ReleaseHypothesis. The R-ERH draws heavily onthe Resource Availability Hypothesis of Coleyet al. (26) because it assumes that fast-growingspecies from high-resource environments willbe less well-defended whereas slowly growingspecies from low-resource environments willbe well defended because replacement costsare high. Indeed, a meta-analysis strongly in-dicates that species adapted to high-resourceenvironments (high-resource species) are pref-erentially consumed (22). If there is strongerherbivore regulation of high- rather than low-resource species, exotic species will have a muchgreater advantage over native species when re-source availability is high. In a meta-analysisof 79 studies that measured performance inresource-rich and resource-poor environments,Daehler (30) showed that exotic species outper-formed native species in resource-rich but notin resource-poor environments. Blumenthal(10) further argues that poorly defended high-resource species may benefit immediately fromenemy release, but that they may be unlikelyto evolve even lower defenses and that supportfor EICA is most likely in resource-poor en-vironments, but this has not been tested. Howthis might affect the evolution of tolerance wasnot discussed. Zhang & Jiang (129) modeled theinteraction between herbivore release and re-source availability and similarly concluded thatthe absolute level of defense depends on the ra-tio of herbivory to habitat productivity and noton productivity or herbivory per se.

These results underscore the complexity ofplant defense evolution. It is not sufficient todemonstrate lower damage levels and assumeplants will evolve to allocate fewer resourcesto defense and more to growth. Predictingchanges in defense evolution requires knowl-edge of herbivore pressures, the effects of differ-ent herbivores on plant performance (fitness),the response of these herbivores to known plantdefenses, the tolerance and the intrinsic growth


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rates of the exotic plant, and the relative re-source availability in the native and nonindige-nous environments.

Novel Phytochemistry

Darwin may have been the first to suggest thatdiffering from the native species may confer in-vasiveness, which might be called the unlike in-vader hypothesis (2). A proxy for phytochemicaluniqueness is taxonomic isolation (21). Taxo-nomic isolation influences the size of the her-bivorous insect fauna of introduced trees; treeswith fewer native relatives accumulate fewerherbivores than trees with many close relativesin their introduced range (28, 32).

Novel phytochemicals may act as novelweapons, in which exotic species bring new bio-chemicals to communities rendered vulnerableby their naıvete (17). These novel weapons canprotect plants from pathogens and herbivoresas well as alter soil microbial communities andincrease competition via allelopathy (18). Al-lelopathy had been viewed as an experimentallyintractable process, but recent exotic plant stud-ies have brought it back into focus. Allelopathyis suggested to occur in diverse species in-cluding Alliaria petiolata (Brassicaceae), Centau-rea maculosa (Asteraceae), and Lantana camara(Verbenaceae) (4, 18, 49). Allelopathy wassuspected as a mechanism because activated car-bon reduces the concentration of allelochemi-cals and therefore the impact of Centaurea onNorth American bunchgrasses (17). We note,however, that activated carbon may also affectthe concentration of nontoxic exudates (e.g.,sugar) that could have belowground effects. Infact, even in some of the best-studied systems,identifying the active allelopathic agent remainschallenging (35). Regardless of the mechanism,there is growing evidence that exotic species canmonopolize resources through direct or indi-rect (via mutualists) inhibition of native species.

If an exotic species possesses novel weaponsthat inhibit its competitors or its own soilpathogens, it may result in greater capture of re-sources and therefore faster growth in the non-indigenous range than in the native range. If the

novel weapon is not also required for resistanceagainst herbivores, we might expect the evolu-tion of faster growth and lower defenses againstherbivores, even without a change in herbivorepressures. If the novel weapon also acts againstroot-feeding herbivores, then selection mightfavor maintenance (or even an increase) in de-fense in the exotic population.

Empty Niche

Ecological studies indicate the existence of avast number of empty niches and that speciesseldom reach global adaptive optima even in na-tive systems. For example, Compton et al. (27)showed that the number of insect herbivores ofbracken fern Pteridium aquilinum (Dennstaedti-aceae) varied tremendously among sites in spiteof the relatively small variation in the statureand architecture of the plant. The abundanceof empty niches is expected for plants as well.

The occupation of an empty niche by ex-otic plant species implies that they have accessto resources that were not accessed by nativespecies (46, 69). Although it is difficult to iden-tify what exactly constitutes an empty niche(also see Supplemental Appendix), it is mostoften associated with the ability to occupy (orcreate) an unusual disturbance regime (33, 68,91) or the ability to access new resource pools(46).

When an exotic species enters an empty,competition-free niche within the nonindige-nous range, it may result in greater resourcecapture and therefore faster growth in that areathan in the native range. If so, we might expectthe evolution of faster growth and lower de-fenses sensu the Resource Availability Hypoth-esis. This prediction has not been tested.

BIOGEOGRAPHY OF DEFENSE:GENERAL PATTERNS

The distribution and abundance of exoticplants vary among regions and are determinedby biotic and abiotic conditions and propagulepressure (2, 66) (Supplemental Appendix).Given the diversity of ecological contexts in

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which exotics exist, a diversity of evolutionaryshifts should be expected. Studies with plantsin their native ranges provide evidence thatsuch shifts do occur. Within the natural range,populations often exhibit striking differences inchemical and morphological defense expressionthat correlate with herbivore pressures. North-ern latitude salt marsh plants, for example,are constitutively less defended than southernlatitude plants (95), a result consistent withpatterns of herbivore pressures. Swihart et al.(102) found the opposite pattern in a terrestrialsystem: Juvenile twigs from southern popu-lations of birch Betula (Betulaceae) and aspenPopulus (Salicaceae) were less defended againstbrowsing hares than were twigs from northernpopulations. This pattern also correlates withherbivore (browsing) pressures. Even within aregion, differences can be marked. Populationsof Brassica oleracea (Brassicaceae) that experi-ence high browsing pressures produce higherconcentrations of glucosinolates (78). Arabidop-sis (Brassicaceae) populations that experiencegreater herbivore pressures have a higherfrequency of trichomes (65). Similarly, popu-lations of Japanese nettle, Urtica thunbergiana(Urticaceae), that have endured heavy browsingby sika deer, Cervus nippon, have smaller leavesand higher stinging hair density than do pop-ulations without deer (53). Finally, the desertlily, Pancratium sickenbergeri (Amaryllidaceae),contains high levels of calcium oxalate (in theterminal 1 cm of leaf ) in habitats where gazellesare common but not in populations withoutgazelles (due to leopard predation) (118).Although similar patterns have been observedfor silica levels in a number of grass species(75), a recent review indicates that vertebrateherbivores have little or no effect on silicadefense evolution and that silica may have amore negative effect on invertebrate herbivores(grinding down their mandibles) (72, 112).

Some of the most striking differences in de-fense expression exist between mainland and is-land populations. Island plant species are oftenhighly susceptible to exotic enemies (13, 85).Many island species, however, are endemics,so this could be due to mismatches and not

to evolutionary shifts in defense. There are afew cases in which the same plant species isfound in both areas. Vourc’h et al. (114) foundthat island populations of Western red cedar,Thuja plicata (Cupressaceae), which evolved forthousands of years without browsers, had lowerterpene concentrations and were more accept-able to deer than were mainland populations.Since the reintroduction of black-tailed deer inthe twentieth century, there has been selectionfor greater defense (115). Bowen & Van Vuren(13) examined the differences in mechanical andchemical defenses of six shrubs on the islandof Santa Cruz (Channel Islands, California)and compared them to the same species on theneighboring mainland (Santa Ynez Mountains).Despite high grazing pressures by sheep on theislands (108), the island plants had fewer andshorter spines, often lower levels of phenolics intheir leaves, larger leaves, and exhibited gigan-tism (13). Importantly, many phenotypic differ-ences were maintained in common garden ex-periments, indicating local adaptation (85). Weinfer from these results that these island speciesgenerally invest less in defenses and may investmore in growth, as indicated by the greater leafsizes of all species.

In summary, variation in herbivore pressuresamong populations has had a profound effecton the defense of native species. By integrat-ing patterns of enemy pressures with differ-ences in resource availability, we suggest thatexotic species provide an invaluable opportu-nity to test hypotheses concerning the evolu-tion of plant defenses.

COMPARATIVE ANDEXPERIMENTAL APPROACHESTO STUDYING DEFENSEEVOLUTION IN EXOTICS

Comparative In Situ Approach

This approach is strongest when multiple pop-ulations from the native and nonindigenousranges are compared and provide estimates ofherbivore pressures, growth, and defense in thetwo regions. It is more difficult, however, to


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infer evolutionary changes with this approach.First, it is challenging to control for environ-mental differences between the two regions thatmay result in phenotypic, but not evolutionary,shifts in growth and defense. Second, geneticdifferences such as founder effects or hybridiza-tion may give the appearance of changes dueto natural selection. Molecular genetic markers(106) can be used to assess whether there havebeen genetic changes in the invasive speciessince separation from the native range. Today,most studies complement this approach withmanipulative experiments.

Manipulative Approach

The manipulative approach involves studyingplants from multiple populations from the non-indigenous and native range in a common gar-den (greenhouse or field) (31, 123). The benefitof studying the exotic species in the field withinthe native range is that the native range is likelyto have all of the insect species that would ordi-narily affect the plant (see Case Study 1, below).Reciprocal transplants are even better (34).

Traditionally, this approach has discountedvariation among populations (each populationis used as a replicate). As a result, evolutionaryinsights that can be gained by comparing pop-ulations (128) are missed. Although founder ef-fects may be difficult to separate from evolvedchanges, exotic populations are usually geneti-cally diverse, thus minimizing the potential forconfounding founder effects.

Spatial and Temporal Sampling

Studies that compare exotic populations with acommon evolutionary background or that trackchanges within a population provide robusttests of defense evolution (see Case Study 2,below). How frequently should one sample? Al-though changes can be rapid when there is ahigh fitness cost of herbivory (128), the strengthof selection is often unknown. If the strength ofselection is low, decades of repeated samplingmay be required. In these cases, use of herbar-ium samples may be instructive (126).

Phylogenetic Approach

The most common means of the phylogeneticapproach is to use congeneric or confamilialpairs (1, 38, 50). This powerful approach (40)controls for relatedness, but it has limitations.First, pairing can be difficult because ploidydifferences often exist between closely relatedplants (11). Second, a phylogenetic approachmay limit one’s ability to quantify evolutionarychanges in novel biochemistry, because closelyrelated species are likely to be biochemicallymore similar (21). In these cases, it may be bet-ter to examine unrelated species with uniquebiochemistry. Overall, it is a favored approachand especially effective when combined withmanipulative studies.

BIOGEOGRAPHY OF DEFENSEEVOLUTION IN EXOTICPLANTS: PREDICTIONS

Although we expect exotic species to show sim-ilar patterns as native species in defense expres-sion when they escape herbivore pressures, weemphasize that the outcome may be a decreaseor an increase in defense expression (Table 1).Specifically, we predict that the best exam-ples of evolutionary decreases in defense shouldoccur

� Where exotic plants escape specialist andgeneralist herbivores (see Case Studies 1and 2, below);

� When attack rates are low, constitutivedefenses will decline but induced defensesmay be maintained or even be higher;

� In small isolated habitats (islands or main-lands) that are relatively free of herbi-vores; and

� In resource-rich environments (relativeto native range) or under conditions thatincrease resource acquisition (e.g., novelweapons belowground or a competition-free niche).

We predict that the best examples of increaseddefense should occur

� Where only specialists are missing (seeCase Study 3);

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Table 1 Summary of testable defense outcomes

Condition in the nonindigenousenvironment Ecological consequence

Specific evolutionary prediction innonindigenous range

Enemy releaseSee Case Study 1

Increased growth and reproduction Selection for reduced allocation to defenseand increased allocation to growth(Evolution of Increased Competitive Ability)

Variable enemy pressures across exoticpopulations

See Case Study 2

Selective pressures are population specific Evolution of decreased or increased defenseinvestment as predicted by the GeographicMosaic Theory

Escape from specialist herbivores butattacked by generalist herbivores

See Case Study 3

Defense matching with local generalistherbivores

Maintenance or evolution of increasedinvestment in defenses targeted againstgeneralist herbivores

Herbivores present but relatively rare Lower frequency of attack Evolution of increased greater reliance oninduced traits and less reliance onconstitutive traits

Small isolated populations (a) Enemies lacking or (b) enemies fewerin number (low densities results ingreater risk of extinction)

Evolution of decreased defense investment

Novel weapons (against mutualisticmicrobes of competitor or against soilpathogens)

Increased resource uptake and thereforefaster growth

Evolution of fast growth and low defenseinvestment

ororEmpty niche

Ecological shifts in expression (phenotypicplasticity)

Defense matching Herbivore pressures are higher in thenonindigenous range

Evolution of increased defense investment

High-resource environments Greater access to nutrients results inincreased growth and reproduction

Evolution of fast growth and low defenseinvestment or ecological shifts in expression(phenotypic plasticity)

Low-resource environments Fewer nutrients result in reduced growthand reproduction

Evolution of slow growth and high defenseinvestment or ecological shifts in expression(phenotypic plasticity)

� If exotics are introduced into areas withhigher generalist enemy pressures thanin their native range (this would occurwhen mainland plant species move to ahabitat with greater herbivore pressuresor when island plant species move to themainland);

� Where there could also be ontogeneticshifts in resistance as well. Juvenile plants,such as acacias, can be more heavily de-fended (119). Therefore, we would pre-dict that if an Australian Acacia (Fabaceae)is introduced into the African savannawhere taller herbivores, elephants, andgiraffes occur, investment in resistance

traits would occur for a longer period oftime;

� Following reassociation with a special-ist herbivore that is deterred by the spe-cific defense trait (see Case Study 2,below);

� In resource-poor environments (relativeto native range); and

� Where novel weapons appear to con-tribute to the success of invasions by someplant species. As native species adapt,however, there could be selection forincreased production of novel weapons.This could even allow noninvasive exoticsto become invasive exotics.


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BIOGEOGRAPHY OF DEFENSEEVOLUTION IN EXOTICPLANTS: CASE STUDIES

We begin our case studies with a study testingEICA because EICA has been such a focus ofinvestigation. The results of this study highlightthe complexities of outcomes. We then presenttwo other case studies that test a subset of pre-dictions described above and in Table 1. Thesestudy systems are three of the most thoroughlystudied and were chosen because they test spe-cific evolutionary predictions using contrastingapproaches.

Case Study 1: Experimental Test of ERand EICA Hypotheses (Silene latifolia)

Prediction: escape from enemies will resultin lower allocation to defense, increased al-location to growth and reproduction, andtherefore greater competitive ability in thenonindigenous range. Wolfe and colleagues(8, 122, 123) have examined native and exoticpopulations of Silene latifolia (Caryophyllaceae),a common roadside and agricultural peren-nial weed native to Europe. This species wasaccidentally introduced into northeast NorthAmerica following the spread of agriculturein the early 1800s. Field studies of 86 pop-ulations in the United States and in Europedemonstrated that North American popula-tions have escaped both generalist and special-ist herbivores (122). Overall, plants were 17times more likely to be damaged in Europethan in North America. Generalist herbivores,which included floral herbivores, snails, andaphids, were far more common in Europe thanin North America. Two specialist herbivores,the fruit predator Hadena bicruris (Lepidoptera:Noctuidae) and the specialist aphid Brachy-caudus populi (Hemiptera: Aphididae), that in-fest flower stalks of bolting and flowering plantsare absent in North America. The anther smutfungus Microbotryum violaceum (formerly Usti-lago violacea) has strong negative effects onplant fitness in Europe and is geographicallyrestricted to populations in Virginia.

Subsequent common garden experiments inNorth America (in the greenhouse and in thefield) with 40 populations (20 populations fromboth Europe and North America) demon-strated that North American plants evolveda weedy phenotype—they germinated earlier,grew faster, produced more flowers, and sur-vived better (8). Importantly, North Americanplants invested less in defensive traits, specif-ically in fewer trichomes and in thinner fruitcapsules, than their European conspecifics.This result is consistent with EICA, except thatthe plants were not more competitive. Wolfeet al. (123) point out that conclusions drawnfrom a common-garden experiment in NorthAmerica must be interpreted with cautionbecause plants experience fewer attacks frompathogens and herbivores in the nonindigenousrange. If investment in defense is costly andthere is reduced defense in their introducedrange, then introduced North American plantsshould be more susceptible to their herbivoresthan European plants. As expected, given theweedy phenotype and lower investment indefense, the North American plants had a two-to threefold higher reproductive success andwere more susceptible to aphid infestation(>twofold), fungal infection (>threefold),and fruit predation (21% higher) than Euro-pean plants (123). About 90% of the NorthAmerican populations were infected, whereasonly about half of the European populationswere infected. Nonetheless, North Americanplants outperformed European plants despitebeing more susceptible to herbivores andpathogens.

In summary, Wolfe et al. have shown thatthese differences are genetically based and con-sistent with the EICA Hypothesis. Other fac-tors, such as genetic drift and resource avail-ability, might also help explain these geneticchanges. We suggest that the evolution of aweedy phenotype with lower defense could alsobe a function of increased resource availabilityin the nonindigenous range, selecting for fastergrowth and lower defense investment in NorthAmerica. Future experiments that take a bio-geographic approach by quantifying resource

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availability, enemy pressures, and the cost ofdamage (i.e., leaf replacement cost) (sensuReference 38) across sites could help determinethe relative importance of enemy release andresource availability on defense evolution.

Case Study 2: Defense EvolutionVaries among Exotic Populations:A Test of the Geographic MosaicTheory (Pastinaca sativa)

Prediction: escape from specialist her-bivores will reduce investment in traitsthat deterthose herbivores. Pastinaca sativa(Apiaceae) produces toxic but costly fura-nocoumarins (124). P. sativa is a biennial herbnative to Europe but was introduced into NorthAmerica and New Zealand 150 and 300 yearsago, respectively (126, 128). These exotic pop-ulations of P. sativa existed for generationsfree from attack by their specialist herbivore,the parsnip webworm, Depressaria pastinacella(Lepidoptera: Oecophoridae). Webworms feedon reproductive structures of P. sativa and canreduce seed production by more than 75%(128). Many, but not all, exotic populations arenow attacked by the webworm and resistanceto the webworms depends largely on the pro-duction of several furanocoumarins: impera-torin, bergapten, isopimpinellin, xanthotoxin,and sphondin. Thus, this is an excellent systemto determine how escape from specialist her-bivores (and subsequent reassociation) causesevolutionary shifts in defense expression.

At a broad scale, Zangerl, Berenbaumand colleagues (126, 128) have shown thatnative European populations and those inNorth America that are commonly attackedby webworms produce high concentrations offuranocoumarins, whereas populations in NewZealand that escaped the webworms producelow concentrations of furanocoumarins (alsosee Supplemental Figure 2). The low levels ofxanthotoxin in European populations appear tobe due to the negative effect of xanthotoxin onthe third trophic level, the specialist parasitoidCopidosoma sosares (Hymenoptera: Encyrtidae)(58, 84).

Further evidence of a selective shift inplant chemistry comes from a recent analysisof herbarium samples (126). Zangerl andBerenbaum found that exotic populations inNorth America from the mid-1800s producedlower amounts of furanocoumarins than nativepopulations in Europe did. During that period,webworms did not occur in North America.Collections subsequent to reassociation withthe specialist herbivore D. pastinacella (firstreported in 1869) have higher concentrationsof furanocoumarins. These results indicate thatenemy release resulted in lower investment insecondary metabolites.

In addition, as predicted by the geographicmosaic theory of evolution (103), the outcomeof reassociation varies among populationsand depends on the ecological context.Specifically, furanocoumarin production byP. sativa depends on the presence of an al-ternative host plant [cow parsnip Heracleumlanatum (Apiaceae) (125)] and on the abun-dance of webworms in both North Americanand European populations (5). Populations inwhich the webworm also uses cow parsnip, aspecies that produces lower concentrations offuranocoumarins, have lower furanocoumarinconcentrations of P. sativa compared withareas without cow parsnip (125). This find-ing indicates that selection for increasedfuranocoumarin production is relaxed in thepresence of an alternative host, although thisshould presumably depend on the alternativehost species. In contrast, xanthotoxin levelswere 161% higher in wild parsnip populationsthat experience high webworm attack (5).

Recently, the webworm was reported in se-lect populations of P. sativa (that had beenin New Zealand for approximately 150 years)(128). Zangerl et al. compared the fura-nocoumarin profiles from seeds of 33 popula-tions of P. sativa (10 from New Zealand) andfound that New Zealand populations that re-main free from webworm attack are chemicallydistinct from populations (in North Americaand Europe) with long associations with thewebworms. Four of five furanocoumarins havelower concentrations in New Zealand. In



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contrast, the one New Zealand population thatis heavily attacked by webworm is chemicallysimilar to two populations from North Americaand one from Europe, and since reassociation,sphondin concentrations appear to be underpositive selection. New Zealand populationsthat are free from attack also produce high con-centrations of octyl acetate, a volatile that mayattract pollinators (and webworms if present).If so, this might indicate that escape from spe-cialist herbivores results in evolutionary shiftsin secondary chemistry that change both resis-tance and plant-pollinator interactions.

Case Study 3: Contingency in DefenseEvolution: Specialist versus GeneralistHerbivores (Senecio spp.)

Prediction: qualitative defenses that attractspecialists may increase in exotic plantsfollowing escape from specialists. Senecio ja-cobaea (Asteraceae) is a biennial or short-livedperennial native to Eurasia. Populations havebeen in North America, New Zealand, and Aus-tralia since the late 1900s, where it is now con-sidered a noxious weed (98). The plant pro-duces pyrrolizidine alkaloids (PAs), some ofwhich are toxic to generalist herbivores but at-tractive to specialists (67, 105). Even thoughthere is no direct cost of production (116), thereappears to be an ecological cost (lower con-centrations of PAs increase plant susceptibil-ity to generalists, whereas higher concentra-tions increase plant susceptibility to specialists).We therefore would expect defense expressionin exotic populations to depend upon the rel-ative abundance of specialists and generalistherbivores.

Joshi & Vrieling (51) compared the re-sistance of a native S. jacobaea population tothat of three exotic populations of this species(North America, New Zealand, and Australia).They tested the hypothesis that escape fromspecialists would increase resistance to gen-eralists but decrease resistance to specialists(see Figure 1). They found that all the exoticplants were of a single chemotype (jacobine).As expected, the performance of two generalist

herbivore species was much lower on exoticplants and the performance of one species,Mamestra brassicae (Lepidoptera: Noctuidae),was negatively correlated with PA concentra-tion. (Although PAs played a role, and werehigher in exotic plants, other unidentifieddefense traits were also acting.) As would be ex-pected following release from the specialist her-bivore that is attracted by PAs, this and anotherstudy found that PAs were higher in the exoticpopulations (98), and as predicted (Figure 1),two specialist herbivores, Platyptilia isodactylus(Lepidoptera: Pterophoridae) and Longitarsusjacobaeae (Coleoptera: Chrysomelidae), pre-ferred and performed better on plants from theexotic regions (51, 98). Joshi & Vrieling alsopoint out that PA concentrations appear to bedecreasing since the introduction of specialistherbivores (for biological control).

Senecio inaequidens and S. pterophorus are na-tive in South Africa and have been introducedinto Europe. Similar to the study by Joshi &Vrieling, Cano et al. (20) found that exotic pop-ulations of these two species were more resis-tant to a generalist snail and produced higherconcentrations of PAs. For both exotic species,the levels of PAs in the exotic range were lessthan or similar to levels found in two nativeSenecio species. (Although not tested, this find-ing could mean that they would not be moresusceptible to specialist herbivores.) That bothspecies showed the same pattern is consistentwith an evolved increase in PAs since introduc-tion. It is also possible that this difference is aresult of high PAs in the founder population. Insummary, these studies with Senecio highlightthat defense traits can be higher or lower in theexotic range and the difference likely reflectsdisparities in the relative abundance of gener-alists and specialists.

DEFENSE EVOLUTIONIN EXOTIC PLANTS:FUTURE ISSUES

There is increasing evidence that the selectivepressures on plant defenses differ geograph-ically among populations (103). Therefore,

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rather than treating exotic plant populations asreplicates in an analysis, future studies shouldexamine differences among populations (seeCase Studies 2 and 3, above) in terms of bothvariation in specialist and generalist herbivoresand differential resource availability. Exoticspecies may provide a unique opportunity totest for resource-driven changes in defense evo-lution while holding pest pressures relativelyconstant. We also suggest that comparisonsamong exotic populations, some of whichmight be exposed to a reduced set of enemies,should provide researchers the opportunityto identify traits that are especially effectiveagainst specific enemies.

Other interactions also deserve furtherstudy. Escape from root feeders may lead to sig-nificant changes in defense expression. In Bras-sica nigra (Brassicaceae) root herbivory by the flyDelia radicum (Diptera: Anthomyiidae) inducesthe concentrations of the glucosinolate sini-grin, which reduce the performance of the rootfeeder and its parasitoids (96). In cotton Gossyp-ium herbaceum (Malvaceae), root-feeding wire-worms Agriotes lineatus (Coleoptera: Elataridae)induce extrafloral nectar production, whichleads to greater parasitoid recruitment (117).Thus, escape from belowground herbivoresalso has the potential to result in evolutionaryshifts in the inducibility of an indirect defense.

There is considerable interest in the effectof volatiles on tritrophic interactions (15, 90,96, 110, 117). Plants produce volatiles that at-tract natural enemies (parasitoids and even hy-perparasitoids) (111). For example, feeding bycotton bollworm, Helicoverpa zea (Lepidoptera:Noctuidae), on cotton flower (Gossypium hir-sutum: Malvaceae) buds induced the plant to

release odors, acyclic terpenes, that attract par-asitoid enemies of the bollworm (87). Shaltiel& Ayal (90) have noted that parasitoids may beattracted only at the scale of individual plantsand need more specific cues, such as honeydew,to detect the herbivores within a plant. Thisvolatile production may lead to the evolution ofcheating, whereby neighboring plants evolve toreduce volatile production (15). Exotic plantsprovide a unique opportunity to test whetherescape from herbivorous enemies leads to theevolution of reduced production of these long-range attractive volatiles.

Exotic plants also provide an opportunity toexamine the evolution of plant-pollinator inter-actions. As highlighted in Case Study 2, pop-ulations of P. sativa that are free from attackby their specialist webworm may become moreattractive to pollinators (128). The greater at-tractiveness to pollinators indicates that escapefrom specialist herbivores results in evolution-ary shifts that result in the selection for greaterfloral attraction.

Finally, evolution of defenses in exotic plantsshould factor in escape from pathogens as well.In one of the best reciprocal transplant stud-ies to date, DeWalt et al. (34) showed thatescape from herbivores, and especially fungalpathogens, has increased growth rates and fa-cilitated range expansion in the invasive shrubClidemia hirta (Melastomataceae) in Hawaii. Inits native range C. hirta is found in open habitatsonly but, owing to enemy release, is common inlow-light understory forested habitats in its ex-otic range. Whether range expansion into low-resource environments has led to lower defenseinvestment deserves further study in this andother systems.

SUMMARY POINTS

1. We emphasize that defense evolution in exotic plants may be a function of differentialenemy pressures, as well as changes in resource availability, and therefore encouragegreater focus on alternative explanations.

2. Defense evolution in exotic plants is common, but the outcome can be either an increaseor a decrease in defense investment. Greater focus needs to be given to induced defenses.


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Specific predictions require a priori knowledge of how resistance traits affect specialistand generalist herbivores.

3. Selection pressures can differ among populations (geographic mosaics) and often resultin important among-population differences in defense evolution.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

Colin Orians is grateful for the support of Tufts University (for providing him a research semesterleave), the Swedish Agricultural University in Uppsala (for hosting him as a guest professor),and the National Science Foundation (DEB 9981568). David Ward is grateful for the support ofthe University of KwaZulu-Natal (for providing him a sabbatical semester leave), the NationalResearch Foundation for funding, and Vanessa Stuart for assistance in many ways. We thankYoram Ayal, Carla D’Antonio, Christer Bjorkman, Don Cipollini, Peter Dalin, Megan Griffiths,Terry Olckers, Adam Steinbrenner, Kees Verhoeven, Louise Vet, Klaas Vrieling, Lorne Wolfe,and Arthur Zangerl for their insights and contributions.

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AR397-FM ARI 12 November 2009 9:17

Annual Review ofEntomology

Volume 55, 2010Contents

FrontispieceMike W. Service � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � xiv

The Making of a Medical EntomologistMike W. Service � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Ecology of Herbivorous Arthropods in Urban LandscapesMichael J. Raupp, Paula M. Shrewsbury, and Daniel A. Herms � � � � � � � � � � � � � � � � � � � � � � � � � �19

Causes and Consequences of Cannibalism in Noncarnivorous InsectsMatthew L. Richardson, Robert F. Mitchell, Peter F. Reagel,and Lawrence M. Hanks � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �39

Insect Biodiversity and Conservation in AustralasiaPeter S. Cranston � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �55

Ekbom Syndrome: The Challenge of “Invisible Bug” InfestationsNancy C. Hinkle � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �77

Update on Powassan Virus: Emergence of a North AmericanTick-Borne FlavivirusGregory D. Ebel � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �95

Beyond Drosophila: RNAi In Vivo and Functional Genomics in InsectsXavier Belles � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 111

DicistrovirusesBryony C. Bonning and W. Allen Miller � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 129

Olive Fruit Fly: Managing an Ancient Pest in Modern TimesKent M. Daane and Marshall W. Johnson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 151

Insect Silk: One Name, Many MaterialsTara D. Sutherland, James H. Young, Sarah Weisman, Cheryl Y. Hayashi,and David J. Merritt � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 171

Bayesian Phylogenetics and Its Influence on Insect SystematicsFredrik Ronquist and Andrew R. Deans � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 189

Insect Fat Body: Energy, Metabolism, and RegulationEstela L. Arrese and Jose L. Soulages � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 207

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Sex Differences in Phenotypic Plasticity Affect Variation in Sexual SizeDimorphism in Insects: From Physiology to EvolutionR. Craig Stillwell, Wolf U. Blanckenhorn, Tiit Teder, Goggy Davidowitz,Charles W. Fox � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 227

Facultative Symbionts in Aphids and the Horizontal Transfer ofEcologically Important TraitsKerry M. Oliver, Patrick H. Degnan, Gaelen R. Burke, and Nancy A. Moran � � � � � � � � � 247

Honey Bees as a Model for Vision, Perception, and CognitionMandyam V. Srinivasan � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 267

Invasion Biology, Ecology, and Management of the Light Brown AppleMoth (Tortricidae)D.M. Suckling and E.G. Brockerhoff � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 285

Feeding Mechanisms of Adult Lepidoptera: Structure, Function, andEvolution of the MouthpartsHarald W. Krenn � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 307

Integrated Management of Sugarcane Whitegrubs in Australia:An Evolving SuccessPeter G. Allsopp � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 329

The Developmental, Molecular, and Transport Biology of MalpighianTubulesKlaus W. Beyenbach, Helen Skaer, and Julian A.T. Dow � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 351

Biorational Approaches to Managing Stored-Product InsectsThomas W. Phillips and James E. Throne � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 375

Parallel Olfactory Systems in Insects: Anatomy and FunctionC. Giovanni Galizia and Wolfgang Rossler � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 399

Integrative Taxonomy: A Multisource Approach to ExploringBiodiversityBirgit C. Schlick-Steiner, Florian M. Steiner, Bernhard Seifert,Christian Stauffer, Erhard Christian, and Ross H. Crozier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 421

Evolution of Plant Defenses in Nonindigenous EnvironmentsColin M. Orians and David Ward � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 439

Landscape Epidemiology of Vector-Borne DiseasesWilliam K. Reisen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 461

Role of Adhesion in Arthropod Immune RecognitionOtto Schmidt, Kenneth Soderhall, Ulrich Theopold, and Ingrid Faye � � � � � � � � � � � � � � � � � � � � 485

Physical Ecology of Fluid Flow Sensing in ArthropodsJerome Casas and Olivier Dangles � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 505

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Managing Invasive Populations of Asian Longhorned Beetle and CitrusLonghorned Beetle: A Worldwide PerspectiveRobert A. Haack, Franck Herard, Jianghua Sun, and Jean J. Turgeon � � � � � � � � � � � � � � � � � 521

Threats Posed to Rare or Endangered Insects by Invasions ofNonnative SpeciesDavid L. Wagner and Roy G. Van Driesche � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 547

Malaria Management: Past, Present, and FutureA. Enayati and J. Hemingway � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 569

Regulation of Midgut Growth, Development, and MetamorphosisRaziel S. Hakim, Kate Baldwin, and Guy Smagghe � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 593

Cellulolytic Systems in InsectsHirofumi Watanabe and Gaku Tokuda � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 609

Indexes

Cumulative Index of Contributing Authors, Volumes 46–55 � � � � � � � � � � � � � � � � � � � � � � � � � � � 633

Cumulative Index of Chapter Titles, Volumes 46–55 � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 638

Errata

An online log of corrections to Annual Review of Entomology articles may be found athttp://ento.annualreviews.org/errata.shtml

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Documents

Evolution of Plant Defenses in Nonindigenous Environments