R E V I E W : E C O L O G Y

Phenotypic Plasticity in the Interactionsand Evolution of Species

Anurag A. Agrawal

When individuals of two species interact, they can adjust their phenotypes in responseto their respective partner, be they antagonists or mutualists. The reciprocal pheno-typic change between individuals of interacting species can reflect an evolutionaryresponse to spatial and temporal variation in species interactions and ecologicallyresult in the structuring of food chains. The evolution of adaptive phenotypicplasticity has led to the success of organisms in novel habitats, and potentiallycontributes to genetic differentiation and speciation. Taken together, phenotypicresponses in species interactions represent modifications that can lead to reciprocalchange in ecological time, altered community patterns, and expanded evolutionarypotential of species.

Phenotypic plasticity is the ability of anorganism to express different pheno-types depending on the biotic or abiotic

environment (Fig. 1). Single genotypes canchange their chemistry, physiology, develop-ment, morphology, or behavior or in responseto environmental cues. R. A. Fisher and other20th century evolutionary biologists lackedexplanations for phenotypic plasticity (1).Evolutionary biologists have been interestedin studying the genetic basis of phenotypes,and early work was focused on traits pre-sumed to be unaffected by the environment.Environmentally affected phenotypes wereconsidered of lesser importance because oftheir apparent lack of a genetic basis. Themodern view of phenotypic plasticity rejectsthis notion because phenotypic plasticity of-ten has a genetic basis. Now, many ecologistsand evolutionary biologists have embracedthe idea that under many circumstances suchphenotypic plasticity can be adaptive (2).This hypothesis parallels Lamarck’s FirstLaw proposed in Philosophie zoologique in1809 (3), which stated that organisms accli-mate to their environment to improve perfor-mance. Of course, Lamarck is largely dis-credited by his Second Law, which suggestedthat these adjustments to the environmentwere heritable. The modern view of plasticitycan be generalized to the statement that phe-notypic plasticity evolves to maximize fitnessin variable environments (the adaptive plas-ticity hypothesis) (2). Here, I take the adap-tive plasticity hypothesis as a starting pointfor evaluating ongoing and future researchdirections in the ecology and evolution ofspecies interactions.

Reciprocal phenotypic change in spe-cies interactions. The intersection betweenspecies interactions and phenotypic plasticityhas generated considerable interest amongevolutionary ecologists (Table 1). The studyof phenotypic responses of one organism toanother is by definition an investigation of aspecies interaction. Yet, biologists have al-most entirely focused on plasticity in speciesinteractions as one-sided events: What is theeffect of variation in species X on the pheno-type of species Y? In nature, however, it isquite likely that interacting individuals arecontinually responding to their interactionpartners in a reciprocal fashion over ecolog-ical time (Fig. 2). Reciprocal interaction sim-ply implies a back-and-forth response interms of phenotypic change between individ-uals, and does not imply symmetry in thestrength of responses or effects of one partneron the other. Many antagonistic or mutualis-tic interactions, including those that are notbehavioral, may involve reciprocal phenotyp-ic changes in ecological time. As an analog,studies of coevolution have long attempted tostudy the reciprocal evolutionary change ininteracting species.

Thompson (4) proposed a similar exami-nation of phenotypic plasticity in species in-teractions termed an interaction norm. Aninteraction norm is expressed as a genotype-by-genotype-by-environment interaction. Inother words, the phenotype of an individualor the sign and strength of an interactionbetween species is determined by the geno-types of interacting individuals and the envi-ronmental conditions in which they occur. Ipropose a refinement of the interaction normconcept that distinguishes environmental ef-fects that are generated by spatial versus tem-poral variation. Reciprocal phenotypicchange between individuals of interacting

species represents an interaction norm wherethe response of one species to the other cre-ates the environment to which the other spe-cies may then respond (Fig. 3). The currentsign, strength, and variability in the speciesinteraction then depends on the past recipro-cal responses between the individuals. In thissimplified view, spatial aspects of the bioticand abiotic environment are assumed to beconstant. The decomposition of the environ-mental component of the interaction norminto temporal (Fig. 3) and spatial aspectsallows for a more detailed analysis of varia-tion in species interactions.

Reciprocal phenotypic change in ecologi-cal time may be (i) a primary determinant ofan organism’s phenotype in nature; (ii) theresult of long-term evolution where the envi-ronment (i.e., the species interaction) hasbeen variable; and (iii) a stabilizing factor inmutualistic interactions. A signature of recip-rocal phenotypic change is the escalation ofphenotypes between individuals of two spe-cies over an extended bout of interactions.This can be a directional change in the phe-notype of partners, where exposure to certaincues activates genes in a dose-dependentmanner (Fig. 3). For example, in a mutualis-tic interaction, individuals may increase re-wards in response to increased services froma partner, and this back-and-forth changing ofphenotypes can be a continuous or iterativeprocess. However, reciprocal phenotypicchange does not have to be directional (5–7).Here again, there is an analogy to coevolu-tionary dynamics, where two possible out-comes are escalating (directional) arms racesor polymorphisms that are stable or fluctuat-ing in space or time. The latter case predictshigh levels of genetic and phenotypic varia-tion between populations of the interactingspecies because of variation in the cost-benefit ratio of a particular adaptation tothe partner (8). Nondirectional phenotypicchanges in ecological time may similarlyresult in variable phenotypes between dif-ferent pairs of interacting species. Recentadvances in the understanding of transpos-able elements suggest that stress-inducedretrotransposons may be a mechanism fornondirectional change. Defensive respons-es in plants and animals result in increasedtranspositional activity that may result inimmunity to parasites (6, 7 ).

Although studies have not been conducted

Department of Botany, University of Toronto, 25Willcocks Street, Toronto, ON M5S 3B2, Canada. E-mail: agrawal@botany.utoronto.ca

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to test the specific hypothesis of reciprocalphenotypic change in ecological time, severalexamples suggest that it is common. Interac-tions between probable mutualists such asleguminous plants (Fabaceae) and nitrogen-fixing bacteria (rhizobia) demonstrate recip-rocal phenotypic change (9). Bacteria nearroots start by producing lipo-oligosaccharides(termed Nod factors). Plants then distort roothairs that curl around the bacteria and subse-

quently produce tubules. After additional re-ciprocal signaling, rhizobia differentiate intobacteroids that fix atmospheric nitrogen. Sub-sequent reciprocity dictates the level to whichlegumes and rhizobia cooperate and ex-change resources (10).

Reciprocal phenotypic change has alsobeen indicated in largely antagonistic interac-tions. Smith and Palmer (11) elegantly dem-onstrated plasticity in morphology and claw

strength of predaceous crabs: crabs eatingmussels without shells grew smaller andweaker claws than crabs eating intact musselswith shells. Conversely, mussels respond tocues from predators, including crabs, by in-ducing increased shell thickness, abductormuscle strength, and byssal threads (12, 13).In the relationship between plants and herbi-vores, plants may induce defenses that aredependent on the density of attackers, andherbivores may induce counterdefenses thatare dependent on the concentrations of plantdefenses consumed (14–17) (Fig. 4). Thecontinuous range of phenotypes induced byeach partner exemplifies a hallmark require-ment of the ecological arms race hypothesisbecause it allows for escalating phenotypicchange. If these responses are not continuous,then “arms races” in ecological time are lesslikely. If reciprocal phenotypic change is theresult of adaptive plasticity in both partners,then it is predicted that coevolution may re-sult in phenotypic plasticity, as opposed to, orin addition to fixed adaptations.

Phenotypic changes in species interac-tions typically revert back to the originalphenotypic state after each extended bout ofinteractions (e.g., each year). However, fourpossibilities may delay this resetting of theinteraction: (i) Maternal environment effectsmay persist across generations and years (18,19); (ii) some phenotypic modifications, suchas tree responses to defoliation, occur acrossyears (20); (iii) some phenotypic responses,especially morphological responses, are can-alized and cannot revert to the original stateeven if the interaction is over (21); and (iv)some environments have reduced seasonality,which may prolong the duration of the inter-action. Alternatively, reciprocal phenotypicresponses, especially in behavioral interac-tions, may begin and end in a matter ofseconds. Thus, the time scale of reciprocalphenotypic responses between species variesfrom seconds to years, and it may depend onwhether the responses are chemical, physio-logical, morphological, or behavioral.

Phenotypic plasticity as a determinantof food chain structure. The distributionand abundance of organisms in a multitrophiccommunity context can also be influenced byphenotypic plasticity. For example, there aremanifold plastic responses of prey to preda-tors, some of which may affect other speciesin an ecological community (Table 1). Theconsumption of prey by predators can obvi-ously have strong ramifications for the com-munity; however, nonconsumptive effects ofpredators on the phenotype of prey and lowertrophic levels may be important, but theyhave only recently been examined. One com-mon response of prey to the scent or visualpresence of predators is to hide and/or toreduce feeding (22, 23). These behavioralresponses have the potential to affect not only

Fig. 1. Two individualsof a single clone of theAsian and African wa-ter flea, Daphnia lum-holtzi. The individualon the left was ex-posed to chemicalcues from predaceousfish (induced); the in-dividual on the rightwas not (control). Thesharp helmet and ex-tended tail spine ofthe induced morphprotect D. lumholtzifrom fish predators.The uninduced formwas formerly de-scribed as a differentspecies (D. monachaBrehm 1912). Green(83), in an accurateand prophetic study,related the occurrenceof both morphs to dif-ferences in fish preda-tion. The induction ofthis morphological de-fense has now beenimplicated as a key factor in the success of D. lumholtzi invading North America (84).

Fig. 2. In the mutualismbetween many herbivo-rous insects and ants, her-bivores produce a sugar-and amino acid–rich nec-tar as food for ants, andants protect the herbi-vores from predators andparasitoids. Here an ant isdrinking from the nectargland of a scale insect onan aspen tree. Becausethe herbivores can alterthe level of food rewardsoffered depending on thebiotic and abiotic envi-ronment and the ants cansimilarly alter their pro-tective services, reciprocalphenotypic change deter-mines the ecologicaloutcome of the speciesinteraction. [Photographby A. A. Agrawal]

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the predator and prey but also the prey’s food.Indeed, in both aquatic and terrestrial sys-tems, it has now been shown that noncon-sumptive effects of predators on prey behav-ior can cascade through the trophic web tohave effects on standing plant biomass (22,23). In other words, the mere threat ofpredation can result in decreased feedingto the point where plant biomass increases.For example, predator-induced morphologi-cal structures in an intertidal barnacle (Chtha-malus anisopoma) resulted in complex inter-actions whereby the abundance of musselswas reduced and algal cover was increased(24). Because mussels and algae compete forsettlement space, and the plastic response ofthe barnacles reduced settlement space formussels, algae indirectly benefited fromhigher trophic interactions.

Phenotypic plasticity in plants can affectthe abundance and distribution of herbivoresand the predators and parasitoids of herbi-vores. In 1975, Haukioja (25) proposed thatthe well-documented dramatic multiyear cy-cles of herbivores could, in part, be mediatedby plant responses that depended on the den-sity of herbivores. In his model, herbivorepopulations rise until inducing a plant de-fense strong enough to precipitate a crash inthe herbivore population. Although density-dependent induction of defenses has beendocumented in some systems (Fig. 4) andtheoretical arguments suggest that plasticityin plant defense could cause cycles, its true

regulatory role is still unknown (15).Plants may also affect herbivores through

phenotypic plasticity in indirect defense. Her-bivore-damaged plants emit volatile com-pounds that attract natural enemies of herbi-vores (26, 27). The production of plant vola-tiles elicits responses from natural enemies ofherbivores in two ways. Predators and para-sitoids are innately attracted to some plantvolatiles and learn to associate other volatileswith the presence of prey (28, 29). Hence, thereciprocal plastic responses (i.e., volatile pro-duction and associative learning) can be im-portant for the ultimate benefit to the plants.Inappropriate volatile signals or repeated ex-posure to volatiles without prey can backfirefor the plant resulting in natural enemies ofherbivores that learn to avoid plants (29).Thus, reciprocal phenotypic responses maymediate the abundance and distribution oftrophic levels in food chains.

In species interactions, especially mutual-isms, there is often extensive signaling be-tween partners that may cause reciprocal phe-notypic change (Fig. 2). This reciprocalchange may ameliorate the conflict of interestthat often ensues between the partners inmutualism: The increase in fitness of onespecies that comes at the expense of the other(30). For example, the interaction betweenlycaenid caterpillars and ants has been wellstudied: Caterpillars use vibrations and chem-ical signals to attract ants and then feed themsweet nectar; consequently, tending ants de-

fend caterpillars against predators and para-sitoids. Various environmental factors in-cluding caterpillar group size and threat ofpredation influence the cost-benefit ratio ofproviding rewards to ants and, thus, dictate acaterpillar’s signaling and subsequent re-wards (31, 32). The level of the caterpillars’signaling and rewards reciprocally influencesthe number and attentiveness of mutualisticants. Here, the multilevel responses of bothpartners are essential for maintaining stabilityin the interaction. The presence of rewardsaffects the abundance and distribution ofants; however, ineffective defense by antsmay result in reduction in the rewards offeredby caterpillars. Plants display similar flexibil-ity in interactions with pollinating mutualists,with the ability to decrease (30) or increase(33) rewards based on previous pollinationsuccess. Thus, reciprocal phenotypic changemay be an answer to the often-discussed evo-lutionary instability of mutualisms. Recipro-cal phenotypic change may promote fidelityamong mutualists, because it allows for part-ner choice, retaliation, or a general adjust-ment of rewards or services (34, 35). Geno-types that cheat may be cut off by theirpartner and thus disfavored by natural selec-tion (10, 30).

Fig. 3. (A) One possible course of reciprocalphenotypic change between individuals in anantagonistic species interaction. Key: Circles,levels of defense in a host organism; triangles,levels of counterdefense in the parasite. Thedynamic nature of such increase in defensefollowing attack and decrease following remov-al of parasites has been recently demonstratedfor spines on Acacia drepanolobium that areinduced by vertebrate herbivores (75). Ecolog-ical reciprocity may take place in all interac-tions, irrespective of the sign of effect on anindividual species. However, phenotypic changein response to a species interaction need not bedirectional (5). (B) Colorado potato beetle (Lep-tinotarsa decemlineata) with eggs. Althoughdamage to potato leaves by this herbivorecauses an induction of plant defenses (protein-ase inhibitors), following induction beetles cleverly adjust their arsenal of digestive proteases to beinsensitive to plant defense (14). [ Photograph by Jack Kelly Clark, ANR, University of California atDavis, ©The Regents, University of California]

Fig. 4. Potential for an ecological arms racebetween plants and herbivores. (A) Phenotypicescalation in a plant defense (pigmentedglands containing hemigossypolone in cotton)that is dependent on the number of attackingmite herbivores [redrawn from (16) with per-mission from Kluwer Academic Publishers]; and(B) phenotypic escalation in a herbivore’s(Trichoplusia ni) counterdefense (production ofinhibitor insensitive proteases) dependent ofthe concentration of plant defense (proteinaseinhibitors) consumed. [Redrawn from (17) withpermission from Elsevier Science]

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Ecological and evolutionary conse-quences of phenotypic plasticity in novelhabitats. How does phenotypic plasticityaffect ecological success and evolutionarydivergence in new or novel habitats, where“habitat” refers to a biotic or abiotic neigh-borhood? As an example consider host-use inparasitoids, insects with a well-developedability for associative learning. Learning canbe a general form of phenotypic plasticitythat organisms can apply to different environ-mental stimuli. Can the ability to learn, andtherefore associate particular environmentalcues with particular hosts, influence the po-tential to use new hosts and potentially theability for a race of parasitoids to specializeon that new host? Such questions about theecological and evolutionary consequences ofplasticity have been raised in the past, as farback as Baldwin in 1896 (1, 36). Yet, empir-ically these questions remain completely un-answered. For example, are invasive speciesmore phenotypically plastic than unsuccess-

ful invaders? Two studies highlight the factthat organisms rely on plasticity in novelhabitats: (i) Lizards introduced to islandswith different vegetation types and (ii) snailsin habitats invaded by exotic predators werethought to have genetically adapted to thesenew environments (37, 38). However, in bothof these cases, the respective phenotypes inthe new habitats (long hind limbs and in-creased shell thickness) were ultimately ex-plained by phenotypic plasticity, not geneticchange (39, 40). One reason why plasticitywas not strongly considered in the originalstudies is that the respective native habitatswere apparently not particularly variable invegetation structure and predation risk (37,38). In another study, Fox has discoveredthat the host-range of a seed beetle hasexpanded to a new tree species and thatmaternal environmental effects (i.e., phe-notypic plasticity cued in the maternalgeneration and expressed in progeny) onprogeny size and composition are facilitating

this shift (41). By definition, organisms innovel habitats will experience new challengesthat may cause the expression of potentiallybeneficial traits through plasticity.

Two empirical examples demonstrate thepossible role of phenotypic plasticity in evo-lutionary divergence. Phenotypic plasticitymay have facilitated the host-shift of Rhago-letis flies from hawthorn to apple fruits (42,43). Naıve adults emerging from apple hostsshowed a strong preference for hawthorn inboth choice and no-choice tests (42). How-ever, those adults that experience apple intheir ecological neighborhood after emergingfrom pupae overwhelmingly chose apple overhawthorn in subsequent oviposition. The con-tribution of this induction of host-fidelity torestricted gene flow and genetic substructur-ing has been demonstrated in nature for thissystem (43). Thus, phenotypic plasticity mayhave played a role in this sympatric specia-tion. Early abiotic experience in the form oflight conditions of adult Drosophila melano-gaster resulted in assortative mating in labo-ratory trials (44). Although the phenotypeitself was unknown, the environmentallycued change resulted in organisms from sim-ilar environments preferentially mating witheach other, a potential mechanism for facili-tating evolutionary divergence. In both ofthese studies a plastic response led to assor-tative mating among individuals that experi-ence the same environment.

The idea that plasticity may lead to eco-logical success in a novel habitat is perhapsintuitive, but the idea that plasticity may alsolead to evolutionary divergence in novel hab-itats is less so. The hypothesis posits thatplasticity may itself lead to genetic differen-tiation, a seeming contradiction. Here, thekey is that plasticity allows for the coloniza-tion and success in a novel habitat, and otherforces (e.g., allopatry or induced preferencefor the novel habitat) cause restricted geneflow to organisms in the original habitat. Ifplastic organisms are restricted to or favor thenovel habitat, a new host race may be formed.The eventual loss of plasticity may not berequired in all cases, as it seems that Rhago-letis has retained its diet-induced phenotypicplasticity even in the new host race (42).

The ecological and evolutionary conse-quences of phenotypic plasticity depend, inpart, on whether plasticity evolves in re-sponse to particular environmental variation(i.e., specialized sun versus shade leaves inplants) or evolves as an overall strategy of theorganism (i.e., associative learning). For mostplastic traits, the response is probably inter-mediate, in that the trait may be responsive toat least a few different environmental stimuli.Whether this range of response to stimuli isadaptive or not, I predict that the larger therange of stimuli to which a trait will respond,the more likely this plastic trait will affect the

Table 1. Apparently adaptive phenotypic responses of organisms in species interactions. In few of theseinteractions have reciprocal responses been investigated. Because of the variable nature of phenotypicplasticity, the sign of the interaction may change depending on the respective phenotypes of theinteracting organisms.

Response Reference

Competition

Increased production of defensive caste in social insects (55)Production of defensive structures in aquatic invertebrates (56, 57)Production of dispersal morphs (58)Trophic specialization in tadpoles (59)Stem elongation in plants (54)Adjustment of progeny vigor in plants (60)

Mutualism

Rewards dependent on the presence of mutualists in plants and animals (31, 61, 62)Behavioral avoidance/attraction to partner depending of rewards in

animals(63, 64)

Plants punishing cheaters (10, 30)Adjustment of rewards according to need in plants and animals (31–33, 65)

Predation risk (animals)

Hiding, reduced activity and feeding (22, 23)Diet or habitat induced camouflage (66, 67)Induction of morphological defenses (18, 21, 39, 68)Production of dispersal morphs (69)Behavioral escape (70, 71)Transformation into a parasite of the predator (72)Adjustment of progeny defenses (18, 73)

Parasitism/herbivory

Increased immune function in animals (68)Induced chemical and/or morphological defense in plants (15, 74, 75)Increased heterophylly (in this case, producing leaves under water) (76)Behavioral shifts in the host (adaptive for host) (77)Behavioral shifts in the host (adaptive for parasite) (78)Gall formation on plants (adaptive for galler) (15)

Food quality ( predators and herbivores)

Adjustment of gut enzymes (14, 17, 79)Adjustment of feeding structures (11, 80)Adjustment of progeny size and quality (41, 81)Adjustment of behavioral preferences (82)

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ecology and evolution of interactions in novelhabitats. Learning and other general forms ofphenotypic plasticity with responses to di-verse stimuli have enormous potential asmechanisms to increase the success of organ-isms in novel habitats (45). If phenotypicplasticity is involved in the ecological andevolutionary success of organisms in novelhabitats, then it might be expected that sub-disciplines, from invasion biology to specia-tion, may benefit from considering the con-sequences of plasticity.

A unique form of phenotypic plasticitythat may result in evolutionary change ismutation in response to stress. Transposableelement activity increases in response tostress in both plants (6) and animals (7).Similarly, under stressful conditions organ-isms can produce DNA polymerases (muta-ses) that replicate faulty or mutated DNA,potentially introducing solutions in an envi-ronment where novelty is required (46). Suchenvironmentally induced mutations have par-ticularly potent evolutionary potential inclonal organisms such as microbes andplants. Even in nonclonal plants, stress-in-duced somatic mutations may be transferredto progeny because reproductive tissues maybe differentiated from mutated somatic tis-sues. The adaptive benefits of high mutationrate in a novel interaction between specieshave now been demonstrated (47). Thus, ifinduced transposons and mutases haveevolved by natural selection, then this formof phenotypic plasticity may be a new mech-anism for generating variation subject to nat-ural selection.

Evolution of phenotypic plasticity:Costs? Although phenotypic plasticity ap-pears to be ubiquitous in species interactions,costs of plasticity must constrain its evolu-tion. The following questions arise from thisfundamental assumption: (i) Do costs of plas-ticity prevent the evolution of plasticity forparticular traits; and (ii) given that plasticityhas evolved in a trait, why does it not con-tinue to evolve to the point where the speciescould be successful in all environments (48,49)?

Ecological costs of plasticity are definedby a reduction in fitness of plastic organismscompared with less plastic organisms, wherethe fitness difference is only realized in aparticular set of environments (i.e., with par-ticular interaction partners present or duringrapid environmental shifts). An imperfectmatch between a phenotype and the environ-ment that results in relatively low fitnessexemplifies an ecological cost. Because thesuccess of plasticity is dependent on the pre-dictability of a changing environment, lags inthe response to environmental stimuli orchanges in the environment that are not pre-dictable can impose a significant ecologicalcost compared with that experienced by fixed

genotypes (48). These types of costs mayresult in selection disfavoring plasticity. Forexample, when transferred from antibiotic-free to antibiotic-containing media, inducibleresistance to tetracycline in Escherichia coliis associated with a much longer lag phase ingrowth compared with that of bacteria con-stitutively expressing resistance (50).

The genetic costs of plasticity involvetrade offs between the degree or pattern ofplasticity and other traits that increase fitness.These costs include the maintenance of phys-iological machinery to sense or regulate phe-notypic plasticity (i.e., an allocation cost),and are based in pleiotropy, linkage disequi-librium, or epistasis influencing other traits.The signature of genetic costs is lower fitnessof plastic organisms compared with less plas-tic conspecific genotypes in a single environ-ment. In the example of resistance to tetracy-cline in E. coli, possession of an inducibleoperon itself (in the absence of its expressionor expressed and compared with a constitu-tively expressed genotype) has a very lowfitness cost (51).

Both ecological and genetic costs of plas-ticity may impose an evolutionary constrainton responses to natural selection favoringplasticity, although little empirical progresshas been made in this area. The most power-ful approach to study the costs of phenotypicplasticity is to start with heritable variationfor a plastic trait within a species. Tradition-ally, quantitative genetic variation within apopulation, selection experiments, or mutantsthat under- or overexpress a trait of interesthave been employed. Hybridization of close-ly related species (52) and genetic engineer-ing (53) has also been employed to manipu-late the level of phenotypic responses in spe-cies interactions.

Knowing the mechanism of phenotypicplasticity will be of utmost importance indetecting genetic costs. Take for example,two individuals of a plant species, one that isplastic in its response to competitors and onethat is not (54). The unresponsive individualmay lack the receptors necessary to respondto competitors and also may lack all of thenecessary physiological machinery to re-spond to the signal from the receptors; con-versely, the unresponsive individual mayhave all of the receptors and machinery nec-essary to respond, but may simply be defec-tive in some final step of the response path-way. These two extremes of the continuumrepresent potential pitfalls in detecting thegenetic costs because the mechanistic basisfor why some organisms are more plasticthan others is not known. In the former case,genetic costs are likely detectable; in thelatter case, genetic costs may be more diffi-cult to detect. The ecological, rather thangenetic, costs of plasticity may be readilydetermined using genetic (or phenotypic) ma-

nipulations where the mechanisms of plastic-ity are unknown. The ecological costs ofphenotypic plasticity will be evident as longas the ecological arena for the experiment isrepresentative of the typical (variable) habi-tats that organisms experience.

Conclusion. Understanding the interac-tions between species is an important goal ofecology and evolution. In addition to theperhaps obvious consumptive interactions be-tween a consumer and a resource, or twoexploitative competitors, we now have a firmgrip on the sometimes more subtle interac-tions that organisms mediate through alteredphenotypes when exposed to interaction part-ners. Because phenotypically plastic adapta-tions are more likely to evolve in variableenvironments than fixed adaptations, andspecies interactions are intrinsically variablein space and time, the (co)evolution of spe-cies interactions has certainly resulted in phe-notypic plasticity. These phenotypic chang-es can result in the structuring of foodchains, reciprocal ecological changes in an-tagonistic and mutualistic interactions, andthe evolution of species. Although costs arelikely to constrain the evolution of adaptivephenotypic plasticity, the ubiquity of plas-ticity in species interactions suggests thatthe benefits outweigh costs under a widevariety of conditions.

References and Notes1. M. J. West-Eberhard, Annu. Rev. Ecol. Syst. 20, 249

(1989).2. S. A. Dudley, J. Schmitt, Am. Nat. 147, 445 (1996).3. J.-B. Lamarck, Zoological Philosophy: An Exposition

with Regard to the Natural History of Animals (Univ.of Chicago Press, Chicago, 1984).

4. J. N. Thompson, Annu. Rev. Ecol. Syst. 19, 65 (1988).5. F. R. Adler, R. Karban, Am. Nat. 144, 813 (1994).6. M. A. Grandbastien, Trends Plant Sci. 3, 181 (1998).7. M. G. Kidwell, D. R. Lisch, Evolution 55, 1 (2001).8. J. N. Thompson, in Herbivores: Between Plants and

Predators, H. Olff, V. Brown, R. Drent, Eds. (Blackwell,Oxford, 1999), pp. 7–30.

9. D. J. Gage, W. Margolin, Curr. Opin. Microbiol. 3, 613(2000).

10. R. F. Denison, Am. Nat. 156, 567 (2000).11. L. D. Smith, A. R. Palmer, Science 264, 710 (1994).12. O. Reimer, M. Tedengren, Oikos 75, 383 (1996).13. G. H. Leonard, M. D. Bertness, P. O. Yund, Ecology 80,

1 (1999).14. C. J. Bolter, M. A. Jongsma, J. Insect Physiol. 41, 1071

(1995).15. R. Karban, I. T. Baldwin, Induced Responses to Her-

bivory (Univ. of Chicago Press, Chicago, 1997).16. A. Agrawal, R. Karban, Entomol. Exp. Appl. 96, 39

(2000).17. R. M. Broadway, J. Insect Physiol. 41, 107 (1995).18. A. A. Agrawal, C. Laforsch, R. Tollrian, Nature 401, 60

(1999).19. T. A. Mousseau, C. W. Fox, Eds., Maternal Effects as

Adaptations (Oxford Univ. Press, New York, 1998).20. E. Haukioja, Annu. Rev. Entomol. 36, 25 (1991).21. C. M. Lively, Evolution 40, 232 (1986).22. A. P. Beckerman, M. Uriarte, O. J. Schmitz, Proc. Natl.

Acad. Sci. U.S.A. 94, 10735 (1997).23. J. Van Buskirk, B. R. Schmidt, Ecology 81, 3009

(2000).24. P. Raimondi, S. Forde, L. Delph, C. Lively, Oikos 91,

353 (2000).25. E. Haukioja, T. Hakala, Rep. Kevo Subarctic Res. Stat.

12, 1 (1975).

S C I E N C E ’ S C O M P A S S

www.sciencemag.org SCIENCE VOL 294 12 OCTOBER 2001 325

26. C. M. De Moraes, W. J. Lewis, P. W. Pare, H. T. Alborn,J. H. Tumlinson, Nature 393, 570 (1998).

27. A. Kessler, I. T. Baldwin, Science 291, 2141 (2001).28. L. Vet, W. Lewis, R. Carde, in Chemical Ecology of

Insects 2, R. Carde, W. Bell, Eds. (Chapman & Hall,New York, 1995), pp. 65–101.

29. B. Drukker, J. Bruin, M. W. Sabelis, Physiol. Entomol.25, 260 (2000).

30. O. Pellmyr, C. J. Huth, Nature 372, 257 (1994).31. O. Leimar, A. H. Axen, Anim. Behav. 46, 1177 (1993).32. A. H. Axen, N. E. Pierce, Behav. Ecol. 9, 109 (1998).33. A. H. Ladio, M. A. Aizen, Oecologia 120, 235 (1999).34. O. Leimar, Proc. R. Soc. London Ser. B. 264, 1209

(1997).35. M. Doebeli, N. Knowlton, Proc. Natl. Acad. Sci. U.S.A.

95, 8676 (1998).36. B. W. Robinson, R. Dukas, Oikos 85, 582 (1999).37. R. H. Seeley, Proc. Natl. Acad. Sci. U.S.A. 83, 6897

(1986).38. J. B. Losos, K. I. Warheit, T. W. Schoener, Nature 387,

70 (1997).39. G. C. Trussell, L. D. Smith, Proc. Natl. Acad. Sci. U.S.A.

97, 2123 (2000).40. J. B. Losos et al., Evolution 54, 301 (2000).41. C. W. Fox, U. M. Savalli, Ecology 81, 3 (2000).42. R. J. Prokopy, A. L. Averill, S. S. Cooley, C. A. Roitberg,

Science 218, 76 (1982).43. J. L. Feder et al., Proc. Natl. Acad. Sci. U.S.A. 91, 7990

(1994).44. M. Barth, H. V. B. Hirsch, M. Heisenberg, Anim. Behav.

53, 25 (1997).45. R. Dukas, E. A. Bernays, Proc. Natl. Acad. Sci. U.S.A.

97, 2637 (2000).46. M. Radman, Nature 401, 866 (1999).47. A. Giraud et al., Science 291, 2606 (2001).48. T. J. DeWitt, A. Sih, D. S. Wilson, Trends Ecol. Evol. 13,

77 (1998).

49. M. vam Kleunen, M. Fischer, B. Schmid, Evolution 54,1947 (2000).

50. R. E. Lenski et al., Mol. Ecol. 3, 127 (1994).51. T. N. M. Nguyen, Q. G. Phan, L. P. Duong, K. P.

Bertrand, R. E. Lenski, Mol. Biol. Evol. 6, 213 (1989).52. J. M. Scriber, R. L. Lindroth, J. Nitao, Oecologia 81,

186 (1989).53. G. W. Felton et al., Curr. Biol. 9, 317 (1999).54. J. Schmitt, S. A. Dudley, M. Pigliucci, Am. Nat. 154,

S43 (1999).55. J. A. Harvey, L. S. Corley, M. R. Strand, Nature 406,

183 (2000).56. C. D. Harvell, D. K. Padilla, Proc. Natl. Acad. Sci.

U.S.A. 87, 508 (1990).57. E. Chorensky, Biol. Bull. 165, 569 (1983).58. R. F. Denno, G. K. Roderick, Ecology 73, 1323 (1992).59. D. W. Pfennig, P. J. Murphy, Evolution 54, 1738

(2000).60. K. Donohue, J. Schmitt, in Maternal Effects as Adap-

tations, T. A. Mousseau, C. W. Fox, Eds. (Oxford Univ.Press, New York, 1998), pp. 137–158.

61. S. J. Risch, F. R. Rickson, Nature 291, 149 (1981).62. J. Stimson, Marine Biol. 106, 211 (1990).63. R. Irwin, A. K. Brody, Oecologia 116, 519 (1998).64. D. Wagner, L. Kurina, Ecol. Entomol. 22, 352 (1997).65. A. A. Agrawal, M. T. Rutter, Oikos 83, 227 (1998).66. W. N. Hazel, D. A. West, Biol. J. Linn. Soc. 57, 81

(1996).67. E. Greene, Science 243, 643 (1989).68. R. Tollrian, C. D. Harvell, The Ecology and Evolution of

Inducible Defenses (Princeton Univ. Press, Princeton,1999).

69. W. W. Weisser, C. Braendle, N. Minoretti, Proc. R.Soc. London Ser. B. 266, 1175 (1999).

70. K. M. Warkentin, Proc. Natl. Acad. Sci. U.S.A. 92,3507 (1995).

71. J. E. Losey, D. R. F, Ecology 79, 2143 (1999).

72. J. O. Washburn, M. E. Gross, D. R. Mercer, J. R.Anderson, Science 240, 1193 (1988).

73. R. Shine, S. J. Downes, Oecologia 119, 1 (1999).74. A. A. Agrawal, Science 279, 1201 (1998).75. T. P. Young, B. D. Okello, Oecologia 115, 508 (1998).76. J. Kouki, Funct. Ecol. 7, 21 (1993).77. R. Karban, G. English-Loeb, Ecology 78, 603 (1997).78. J. Moore, BioScience 45, 89 (1995).79. M. J. Snyder, J. I. Glendinning, J. Comp. Physiol. A.

179, 255 (1996).80. G. G. Mittelbach, C. W. Osenberg, P. C. Wainwright,

Evol. Ecol. Res. 1, 111 (1999).81. C. W. Fox, M. S. Thakar, T. A. Mousseau, Am. Nat.

149, 149 (1997).82. A. A. Agrawal, C. Kobayashi, J. S. Thaler, Ecology 80,

518 (1999).83. J. Green, E. African J. Zool. 151, 181 (1967).84. R. Tollrian, personal communication. Scanning elec-

tron micrograph courtesy of C. Laforsch and R.Tollrian.

85. This article was inspired by J. Gurevitch and N.Huntley’s challenge to address three questions forthe next century of ecology and evolution ( pre-sented at the Ecological Society of America meet-ing in 2000). I thank L. Adler, anonymous review-ers, T. Bao, S. Barrett, A. Bell, J. Bronstein, M.Dorken, R. Dukas, J. Fordyce, M. Johnson, R. Karban,N. Kurashige, A. Mooers, K. Rotem, J. J. Thaler, J. S.Thaler, P. Van Zandt, L. Vet, D. Viswanathan, M.West-Eberhard, and A. Winn for comments anddiscussion. My laboratory and current work (www.botany.utoronto.ca/researchlabs/agrawallab/index.stm) is being supported by the Botany Departmentat the University of Toronto and the Natural Sci-ences and Engineering Research Council of Canada.

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