evolutionary analyses of morphological and physiological plasticity in thermally variable...

AMER. ZOOL., 38:545-560 (1998)

Evolutionary Analyses of Morphological and Physiological Plasticity inThermally Variable Environments1

JOEL G. KINGSOLVER2 AND RAYMOND B. HUEY

Department of Zoology, Box 351800, University of Washington, Seattle, Washington 98195-1800

SYNOPSIS. Morphological and physiological plasticity is often thought to representan adaptive response to variable environments. However, determining whether agiven pattern of plasticity is in fact adaptive is analytically challenging, as is eval-uating the degree of and limits to adaptive plasticity. Here we describe a generalmethodological framework for studying the evolution of plastic responses. Thisframework synthesizes recent analytical advances from both evolutionary ecologyand functional biology, and it does so by integrating field experiments, functionaland physiological analyses, environmental data, and genetic studies of plasticity.We argue that studies of plasticity in response to the thermal environment may beparticularly valuable in understanding the role of environmental variation in theevolution of plasticity: not only can thermally-relevant traits often be mechanisti-cally and physiologically linked to the thermal environment, but also the variabilityand predictability of the thermal environment itself can be quantified on ecologi-cally relevant time scales. We illustrate this approach by reviewing a case studyof seasonal plasticity in the extent of wing melanization in Western White Butter-flies (Pontia occidentalis). This review demonstrates that 1) wing melanin plasticityis heritable, 2) plasticity does increase fitness in nature, but the effect varies be-tween seasons and between years, 3) selection on existing variation in the magni-tude of plasticity favors increased plasticity in one melanin trait that affects ther-moregulation, but 4) the marked unpredictability of short-term (within-season)weather patterns substantially limits the capacity of plasticity to match optimalwing phenotypes to the weather conditions actually experienced. We complementthe above case study with a casual review of selected aspects of thermal acclimationresponses. The magnitude of thermal acclimation ("flexibility") is demonstrablymodest rather than fully compensatory. The magnitude of genetic variation (cru-cial to evolutionary responses to selection) in thermal acclimation responses hasbeen investigated in only a few species to date. In conclusion, we suggest that anunderstanding of selection and evolution of thermal acclimation will be enhancedby experimental examinations of mechanistic links between traits and environ-ments, of the physiological bases and functional consequences of acclimation, ofpatterns of environmental variability and predictability, of the fitness consequencesof acclimation in nature, and of potential genetic constraints.

INTRODUCTION is by altering their phenotypes. Tradition-ally this response has been termed "plastic-

" . . . a frog or a toad is by no means the ity" if it involves morphological traits butsame thing in summer as in winter." "acclimation" if it involves physiologicalClaude Bernard, 1865 (1949 edition) traits. The basic phenomenon is, however,~ , . ,. . , , . the same in either case: an individual's phe-One way that individual organisms may c h i n t Q ( o r i n ^

respond to variable environmental vanation {pJ?n o f ) lnvimna£ntsi c o n d i t i o n s i n a

way that may alter that individual's fitness.1 From the Symposium Responses of Terrestrial Ar- Acclimation to temperature in eCtOtherms

thropods to Variation in the Thermal and Hydric En- has long been a central topic of physiolog-vironment: Molecular, Organismal, and Evolutionary j c a l r e s e a r c h (Bernard QUOte above; PrOSSer,

S^?or,ntee an^o^ivTSg^30 December 1996, at Albuquerque, New Mexico. mense (PrOSSer, 1986) and has focused pri-

2 E-mail: [email protected] marily on two issues: (i) the physiological

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546 J. G. KlNGSOLVER AND R. B . HUEY

mechanisms underlying acclimation and (ii)the consequences of acclimation for organ-ismal function or performance. Thermal ac-climation in ectotherms affects diversephysiological traits, including shifts in en-zyme kinetics, membrane fluidity, lethaland optimal temperatures, metabolism, etc.(Prosser, 1986; Somero, 1978; Hochachkaand Somero, 1984; Cossins and Bowler,1987).

The adaptive significance of thermal ac-climation has, however, received relativelylimited attention: typically, any observedeffect of acclimation on organismal func-tion has been interpreted uncritically (i.e.,without a formal test) as the adaptive resultof evolution by natural selection in re-sponse to variable environmental conditions(cf. Feder, 1987; Leroi et al, 1994; Hueyand Berrigan 1996; Bennett and Lenski,1997). Consequently, several crucial ques-tions have received limited empirical ortheoretical attention. For example, does agiven pattern of acclimation actually en-hance fitness in nature? Is genetic variationin acclimation response sufficient to permitrapid evolutionary responses to selection onthe direction and magnitude of the re-sponse? Are environmental cues (e.g., de-velopmental temperature, photoperiod) re-liable predictors of environmental shifts(Levins, 1968)? If not, might this unrelia-bility limit the degree of adaptation of plas-ticity (Moran, 1992)? Answering these andrelated questions is a significance challengeto evolutionary physiologists (Leroi et al.,1994; Travis, 1994; Huey and Berrigan,1996; Bennett and Lenski, 1997).

The analytical challenges of studying theevolution of plasticity can be reduced bymerging recent developments made in evo-lutionary ecology with those in evolution-ary physiology. For example, the necessarytheoretical framework for conceptualizingand analyzing selection and evolution ofplasticity in quantitative traits has recentlybeen developed in detail by evolutionaryecologists (e.g., Via and Lande, 1985;Stearns, 1989; Gomulkiewicz and Kirkpa-trick, 1992; Moran, 1992; Scheiner, 1993).Similarly, the important mechanistic linksbetween specific trait values and environ-mental conditions are often accessible via

the tools of functional biologists. In addi-tion, thermal and hydric aspects of the en-vironment are often amenable to quantita-tive analyses of patterns of environmentalvariability and predictability. Thus, prog-ress towards an understanding of the evo-lution of plasticity can be accelerated bycombining strengths of evolutionary and offunctional ecology.

In this paper we examine several aspectsof selection on and the evolution of mor-phological and physiological plasticity. Wefocus on plastic responses to variation inthe thermal environment as a model systembecause of the demonstrable importance oftemperature to the physiology and ecologyof animals, because variation and predict-ability in the thermal environment can bereadily quantified, and because the mecha-nistic links between performance and thethermal environment can often be specified.

We begin by outlining an experimentalfield and laboratory approach that can helpevaluate the nature and extent of adaptiveplasticity and the intrinsic and extrinsic lim-its to such adaptation. Then we illustratethis approach by reviewing a case study ofmorphological plasticity of wing melaninpattern in pierid butterflies in seasonallyfluctuating thermal environments. Our dis-cussion emphasizes the importance of en-vironmental unpredictability in limitingadaptive plasticity, an issue relatively unex-plored in most empirical studies of plastic-ity. Finally, we highlight some understudiedaspects of thermal acclimation of ecto-therms. Specifically, we sample publishedstudies of ectotherms to explore the mag-nitude ("flexibility") of thermal acclima-tion responses, and also review what littleis known about genetic variation in thermalacclimation. Our discussion emphasizesthat an understanding of the evolution ofthermal acclimation—and of plasticity ingeneral—will be furthered via studies thatcombine the mechanistic strengths of evo-lutionary physiology with genetical andfield approaches of evolutionary ecology(see also Travis, 1994; Huey and Berrigan,1996).

ANALYZING ADAPTIVE PLASTICITYA reasonably complete understanding of

microevolutionary issues of adaptive plas-



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ANALYZING ADAPTIVE PLASTICITY 547

ticity requires explicit consideration of sixmain issues (Travis, 1994; Huey and Ber-rigan, 1996). The first two issues explorebasic functional aspects of acclimation(e.g., the physiological bases and the func-tional consequences of a plastic response)and represent the "how" of acclimation(Mayr, 1961). These two issues have longbeen the focus and strength of physiologicalstudies (Prosser, 1986), and so we will dis-cuss them only in passing. The remainingfour issues explore the "evolutionary" as-pects of adaptation, selection, and responseto selection. These issues, which representthe "why" of acclimation (Mayr, 1961), areonly beginning to be explored by evolu-tionary physiologists and hence requiremore attention.

Functional issues1) Describe the induction, direction,

magnitude, and functional consequences ofphenotypic plasticity.—This involves ex-ploring the environmental conditions (orcues such as temperature or photoperiod)that induce the plastic response as well aselucidating the functional consequences ofexpressing different phenotypes in differentenvironments. (Note: information on func-tional consequences is crucial to under-standing both the ecological context and theadaptive significance of plasticity.)

2) Explore the physiological mechanismsunderlying the observed plastic response.—For example, determine whether the ob-served changes are a consequence of lower-level changes in membrane structure, en-zyme activities, expression of stress pro-teins, etc. (Note: This information providesinsights not only into "how" plasticity isachieved mechanistically, but sometimes asto "why" plasticity might be functionallysignificant.)

Evolutionary issues3) Evaluate whether plasticity is in fact

adaptive in nature.—In other words, do al-ternative phenotypes actually increase fit-ness in their appropriate environmental con-ditions in the field? Effective protocols fortesting various aspects of the adaptive sig-nificance of acclimation in the laboratorycurrently exist (Krebs and Loeschcke,

1994; Leroi et al, 1994; Huey et al., 1995;Zamudio et al., 1995; Huey and Berrigan,1996; Krebs and Feder, 1997), but the ul-timate tests of adaptation must be done inthe field. For example, the adaptiveness ofplasticity (e.g., seasonal change in a phe-notype) can be tested by experimentallygenerating these alternative phenotypes, re-leasing them into the field, and then deter-mining their relative fitnesses in each sea-son (see Karban and Carey, 1984; Harvell,1986; Schmitt et al, 1995; Dudley andSchmitt, 1996).

4) Determine whether selection in natureon the observed degree of plasticity is sta-bilizing or directional.—For a quantitativetrait, even if plasticity generates phenotypictrait values that increase fitness in each en-vironment (e.g., if increased heat tolerancein summer phenotypes increases survival),the degree of plasticity may not yield traitvalues that are in fact "optimal" for the en-vironmental conditions. Moreover, by esti-mating how selection on existing variationin a plastic trait varies with time (or withhabitat), we can determine whether selec-tion is acting on the actual magnitude ofplasticity (Weiss and Gorman, 1990; King-solver, 1995a). Looked at in a differentway, evidence for directional selection onplasticity provides a quantitative measure ofmaladaptation—i.e., of the degree to whichplasticity fails to generate the optimal phe-notype in each environment.

5) Determine whether unpredictability inenvironmental conditions may limit the de-gree to which plasticity can adapt organ-isms to variable environments. (Hoffman,1978; Moran, 1992).—Consider a plastictrait that is determined by developmentaltemperature, presumably as an adaptive cueof temperatures to be experienced by adults.However, developmental temperature maybe an unreliable predictor of adult temper-ature, because of the inherent time lag be-tween larval and adult stages. As a result,environmental unpredictability may cause amismatch between the trait value expressedand the environmental conditions duringwhich selection actually operates. Environ-mental unpredictability—if marked—maypotentially limit the degree to which adap-tive plasticity may evolve.



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6) Determine the extent of genetic vari-ation in plasticity.—Even if selection onplasticity is strong, evolutionary changes inthe degree of plasticity cannot occur with-out appropriate genetic variation (Via andLande, 1985; Scheiner and Lyman, 1991).Genetic variation in plasticity may be lim-ited by mechanistic limitations on plasticityand by physiological costs of maintainingor employing plastic responses. Many stud-ies have documented substantial geneticvariation in plasticity of morphological andlife history traits (see Scheiner, 1993), butstudies of the genetic basis of physiologicalacclimation are still rare (see below).

These six issues provide a comprehen-sive—if ambitious—agenda for studyingadaptive plasticity from a microevolution-ary perspective. Nearly all of the empiricalliterature on evolution of plasticity has fo-cused on Issues 1-3 (environmental deter-minants and functional and fitness conse-quences of plasticity) and Issue 6 (geneticvariation for plasticity). In contrast, we areaware of only two published studies thathave estimated natural selection on themagnitude of plasticity within populationsin the field (Issue 4: Weiss and Gorman,1990; Kingsolver, 1995a). Further, weknow of no study that explores quantita-tively how environmental unpredictabilitymay limit the degree of adaptive plasticityin field populations (Issue 6: but see Hoff-man, 1978, and also next section); as weshall show, studies of the thermal and hy-dric environment may be particularly ame-nable to such analyses of environmental un-predictability.

SEASONAL WING MELANIZATION IN PIERIDBUTTERFLIES

We will illustrate the above issues by de-scribing a case study of seasonal shifts inthe degree of wing melanization in pieridbutterflies. Wing melanization is of physi-ological and evolutionary interest becauseof its influence on the thermal biology ofthese butterflies (see below). We concen-trate on the Western White Butterfly, Pontiaoccidentalis, which is widely distributed athigh latitudes and elevations throughout thewestern U.S. and Canada. Many popula-tions have multiple generations each year,

and the different generations develop andlive under quite different thermal regimes.These butterflies are thus suitable for study-ing plasticity across seasonal thermal envi-ronments.

Issue 1: Environmental determinants andfunctional consequences of plasticity

In P. occidentalis as well as in many oth-er butterfly species (Watt, 1969; Brakefield,1987), the amount of melanin pigment indifferent areas of the wings of adults is aplastic trait. Developmentally, the degree ofmelanization is set by photoperiodic (and toa lesser extent, temperature) cues experi-enced late in larval development (Watt,1969; Shapiro, 1976). In P. occidentalis,the greatest shift in wing melanin occurs inthe ventral hindwings and in the bases ofthe dorsal hindwings (Shapiro, 1976; King-solver and Wiernasz, 1991). In both theseregions, melanization is significantly darkerand more extensive in spring than in sum-mer (or following development in shortrather than long photoperiods in the labo-ratory).

Shifts in wing melanization can have di-verse functional consequences (Kingsolverand Wiernasz, 1991), but one obvious con-sequence is for heat exchange and thermo-regulation. Thermoregulation is importantto fitness because pierid butterflies requireelevated body temperatures (28-40°C inmany species) for vigorous and sustainedflight. In cool conditions, Pontia butterfliescan achieve elevated temperatures by bask-ing with their dorsal wing surfaces orientedto solar radiation; conversely in hot condi-tions, many butterflies stop flying, closetheir wings, and orient wings and body tominimize their radiative heat load (heat-avoidance). The degree of wing melanin incertain wing regions can affect the amountof solar radiation absorbed and thus thebody temperatures achieved. For example,classic studies by Watt (1968, 1969)showed that the intensity of melanin on theventral hindwings (VHW) of Colias eury-theme butterflies positively affected bodytemperature during basking. Consequently,even under identical environmental condi-tions, seasonal phenotypes that differed inVHW melanin had different equilibrium



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basking temperatures. Analogous studieswith P. occidentalis show that the intensityof melanin on the basal dorsal hindwings(bDHW) directly affects body temperaturesachieved during basking (unlike Colias, P.occidentalis butterflies bask with theirwings open), whereas melanin on the VHWaffects body temperatures during heat-avoidance (Kingsolver, 1987). These func-tional analyses suggest a simple adaptivehypothesis: seasonal plasticity in wing mel-anin is an adaptation enhancing thermoreg-ulation in seasonally varying thermal envi-ronments (Watt, 1968, 1969; Hoffman,1978).

Issue 2: Mechanistic bases of plasticityThe biochemistry of melanin wing pig-

ments is well described for butterflies, butrelatively little is known about the mecha-nisms underlying plasticity in melanism(Nijhout, 1991). Although pigment deposi-tion occurs during the pupal stage, the ac-tual determination of melanin plasticity isset largely by photoperiod and occurs ear-lier during the larval stage. Photoperiodiccues alter titers of juvenile hormone (JH)during larval development, and JH in turnlater affects the amount of pigment depo-sition in the pupal stage (Nijhout andWheeler, 1982); however, quantitative re-lations between JH titers in larvae and mel-anin pattern in adults are still poorlyknown. A recent study suggests that geneexpression at the distalless locus controlsplasticity in wing melanin in Byclicus but-terflies (Brakefield et al., 1996).

Issue 3: Is plasticity adaptive?The "adaptive plasticity" hypothesis pre-

dicts that "summer" phenotypes, whichhave relatively less wing melanin, shouldhave higher fitness during summer condi-tions than should "spring" phenotypes,which are darker. The reverse should betrue during spring conditions.

Following the pioneering field studies byShapiro (1976), Kingsolver (1995fe) con-ducted field experiments to test these pre-dictions in a population of P. occidentalisin southeastern Washington state. This pop-ulation has four to five adult flight seasons(generations) between April and August.

The degree of melanization in many wingregions is distinctly different (but somewhatoverlapping) in adults from summer andspring generations. Kingsolver collectedeggs from females and reared the eggs(split-family design) in the laboratory in ei-ther Long-day (16 hr light, 8 dark) "Sum-mer" or Short-day (10L:14D) "Spring"treatments. The resulting adult butterfliesdiffered significantly in wing melanin traits(degree of melanin was measured as grey-level intensity using a video analysis sys-tem: see Kingsolver, 1995a, b). For exam-ple, Long-day individuals had significantlyless melanin on the bDHW and VHW thandid Short-day individuals. Shortly afteremergence, each butterfly was marked in-dividually and released at the field site. Dai-ly recapture-release sampling and mark-re-capture statistical methods were used to de-termine whether the rearing treatment af-fected survival (as distinct from recapture)probabilities (Kingsolver, 1995a, b).

The adaptive plasticity hypothesis wassupported by release experiments conduct-ed during two summers (July 1991 and1992): in both years, Long-day (summerphenotype) individuals had significantlygreater survival than did Short-day (springphenotype) individuals. Interestingly, theeffect of developmental treatment on sur-vival was stronger in 1992 than in 1991,perhaps indicating an enhanced advantagefor the summer phenotype during the rela-tively hot summer of 1992.

The adaptive plasticity hypothesis was,however, not supported by a release exper-iment conducted in one spring (1991):Long-day and Short-day individuals hadsimilar survival rates during this season(Kingsolver, \995b). In combination, thesefield studies provided only partial supportfor the hypothesis of adaptive plasticity:Plasticity appeared adaptive during summerconditions, but not during spring. More-over, even in the summer studies, thestrength of selection varied between years.

These results show that rearing treatmentcan affect both wing melanin phenotypeand survival in the field. However, the rear-ing environment will influence many im-portant aspects of the adult phenotype, notjust wing melanin pattern. Consequently,



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the above field tests do not necessarily im-ply a causal link between wing phenotypeand survival. To determine whether plastic-ity in wing pattern and survival are in factcausally linked, Kingsolver (1996) con-ducted companion experiments that directlymanipulated melanin on the posterior VHW(the wing region showing the greatest de-gree of melanin plasticity in P. occidental-is) into one of three treatment groups:"Blackened" individuals in which blackpigment was added along each vein on theposterior half of the VHW; "Yellowed" in-dividuals served as a control group inwhich yellow pigment was added alongeach vein on the posterior half of the VHW;and an "Unpainted" group. If seasonalplasticity is adaptive, then Blackened indi-viduals should show reduced survival insummer relative to Yellowed or Unpaintedbutterflies.

Mark-release-recapture experiments wereconducted in the summers of 1991 and1993. Blackened males indeed had signifi-cantly reduced survival probabilities rela-tive to Yellowed and Unpainted males, con-sistent with the adaptive plasticity hypoth-esis. However, paint treatment had no effecton females, contrary to the hypothesis. Fe-males may be insensitive here because theyare less active than males, and so may beless exposed to stressful summer tempera-tures. (Because VHW melanin does not af-fect mate choice in this species [Wiernasz,1989], the different effects of the manipu-lations on males and females are unlikelyto be related to effects of mating on surviv-al.) Taken as a whole, the above studiessupport the hypothesis that plasticity inwing melanin pattern is sometimes—butnot always—adaptive for seasonally vary-ing thermal conditions. Obviously, plastic-ity isn't always adaptive and its importancevaries between seasons, years, and sexes.

Issue 4: Selection on the magnitude ofplasticity

Even if plasticity in wing melanin isadaptive in this system, selection may stillfavor changes in the degree of plasticity.For example, selection could potentially fa-vor greater (or lesser) plasticity than is ac-tually observed.

SELECTION ON PLASTICITYU./4"

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FIG. 1. Selection on plasticity of wing melanin inPontia occidentalis butterflies. For the bases of thedorsal hindwings (bDHW melanin), long photoperiodsresult in less melanin in the summer generations, yetthere is evidence of selection favoring further decreas-es in melanin in summer conditions. Conversely, short-er photoperiods result in more melanin during springgenerations, yet there is evidence of selection favoringfurther increases in melanin in spring conditions.

To explore selection on the magnitude ofplasticity, Kingsolver (1995a) conductedmark-release-recapture studies (two MRRin spring and two in summer) with wild-caught individuals, and measured direction-al selection coefficients for several wingtraits (including bDHW and VHW melanin)during both spring and summer generations.For most of the wing traits, directional se-lection was generally weak or absent. How-ever for melanin at the bases of the dorsalhindwings (bDHW melanin), which influ-ences thermoregulation during basking(Kingsolver, 1987), significant directionalselection was detected in all four studies.Most importantly, the direction of selectionalternated between seasons: selection waspositive for enhanced bDHW melanin inspring but negative in summer. These re-sults are strongly consistent with expecta-tions based on thermoregulatory consider-ations.

Recall, however, that bDHW melanin isphenotypically plastic, so the mean degreeof bDHW melanin differs significantly be-tween spring and summer generations (Fig.1). As a result, the observed pattern of sea-sonally alternating directional selection im-



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plies that selection favors increased plastic-ity in this trait—that is, selection currentlyfavors an increase in the slope of the "normof reaction" relating bDHW melanin to en-vironmental rearing conditions (in this case,photoperiod). Thus, even though plasticityis generally adaptive, even more plasticityin this trait would further increase survival.

Issue 5: Environmental unpredictabilityWhether plasticity is adaptive will de-

pend in part on the predictability of the en-vironment (Levins, 1968). In other words,do environmental conditions experiencedby butterfly larvae adequately predict con-ditions experienced by adults? The thermalenvironment is particularly suitable for ex-ploring this question, as long-term weatherrecords are often available. To address thisissue, we therefore examined long-termweather records (1941-1992) of daily max-imum air temperatures (Tmax) from a weath-er station near Kingsolver's (MRR) studysite.

Temperature variation at three differentscales is relevant to the short-term evolu-tion of plasticity in this system. First, arebetween-season differences in Tmax predict-able, such that photopenodic cues duringlarval development would be good predic-tors of seasonal temperatures experiencedby adults? Not surprisingly, the answer isyes (Fig. 2): monthly average Tmax in Aprilis on average 13°C lower than in July, andin fact average Tmax is always lower in Aprilthan in July. Interestingly, there is a signif-icant position correlation (r2 = 18%) be-tween mean April and July Tmax: years thatare on average warmer in April are alsousually warmer in July. Second, are within-season differences in Tmax minor, whichwould reinforce the usefulness of photope-riod as an environmental cue? Here the an-swer is no (Fig. 3): the weekly average Tmaxduring (for example) the first week of Julyeach year was surprisingly variable andranged from 23 to 38°C. [Note: becauseadults butterflies usually live for about oneweek, a weekly average reflects the tem-perature conditions experienced during thetime scale of an individual butterfly's lifespan.] Because Tmax in early July is stronglyrelated to solar radiation intensity, a Traax

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FIG. 2. Correlation of mean daily maximum temper-ature (T,,^) for the months of April and July for 1941-1992 at Othello, Washington, based on U.S. WeatherBureau data.

value of 23°C represents cool, cloudy con-ditions in which flight activity may be lim-ited by low body temperatures; whereas aTmax of 38°C represents hot, sunny condi-tions in which flight activity may be limitedby high body temperatures. Thus, even in agiven season (and hence at a given photo-period), adults in different years may seevery different temperature conditions.

Third, can between-year unpredictabilityof photoperiodic cues alone be amelioratedif butterflies were able to integrate bothphotoperiodic and temperature cues (Hoff-mann, 1978; Shapiro, 1976; Kingsolver,1995ft) from their rearing environment? Ifso, the butterflies might adjust their devel-opmental trajectories for wing melanizationin response to immediate weather condi-tions as well as to photoperiod. For P. oc-cidentalis in the field, adult butterfliesemerge about two weeks after melanin pat-tern is determined developmentally in thelarvae. How well do current temperatureconditions predict temperatures two weekslater? Data on weekly average Tmax for thefirst and third weeks of July yield a clear,negative answer (Fig. 3): average Tmax inthe first week of July explains less than 7%of the variation in Tmax two weeks later.Thus, the thermal environment (and pho-toperiod) during the larval stage is a poor



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552 J. G. KlNGSOLVER AND R. B. HUEY

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predictor of the thermal environment adultswill face, at least within seasons.

This explicit consideration of the pre-dictability—or lack thereof—of the thermalenvironment adds some insights to ouranalysis of adaptive plasticity. Between-season patterns in temperature are very pre-dictable, at least on a gross scale (Fig. 2);and the magnitude of the between-seasonshifts in the thermal environment favor theevolution of plasticity. However, if we shiftthe time scale to variation between years orto within the lifetime of an individual, thethermal environment is clearly unpredicta-ble (Fig. 3). This short-term unpredictabil-ity likely prevents plasticity from evolvinga precise match between mean phenotypictrait values and the fluctuating thermal en-vironment.

Issue 6: Genetic variation in plasticityEven if selection currently favors in-

creased plasticity in bDHW melanin (see Is-sue 4, above), genetic variation in plasticityis a prerequisite for an evolutionary re-sponse to this selection. One common wayof identifying genetic variation is to ex-

amine variation in the slopes of reactionnorms for a set of genotypes or familiessampled from the population of interest{e.g., Via and Lande, 1985). By measuringreaction norms of wing melanization for aset of full-sib families of P. occidentalis,Kingsolver and Wiernasz (1991) identifiedsignificant (broad-sense) genetic variationin the plasticity of the extent of melanin inmany wing regions. This suggests that theevolution of plasticity in these traits is notstrongly constrained genetically.

ADAPTIVE PLASTICITY OF WING MELANIN:A SUMMARY

This case study provides some provision-al understanding of the existence, degree,and limits to adaptive plasticity in thermallyvariable environments. First, experimentalanalyses show that plasticity of wing mel-anin increases one component of fitness(adult survival) during summer but notspring conditions. Experimental manipula-tions of wing pattern verify that this effecton survival that can attributed to plasticityof wing pattern per se, rather than someother effect of rearing conditions. Second,



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selection analyses of natural variation de-tect consistent selection favoring increasingplasticity in one wing trait that is known tobe important for thermoregulation. Thus,the observed plasticity was not at an evo-lutionary optimum. Third, short-term un-predictability of the thermal environmentwithin a season is surprisingly large. Thisunpredictability likely limits the capacityfor adaptive plasticity in wing melanintraits, simply because larval conditions donot adequately predict adult ones. In fact,in many temperate regions short-termweather variation is dominated by weathersystems that occur on the time scale of 4—7 days, such that weather variation on ascale of a week or more is typically highlyunpredictable (e.g., Kingsolver 1981)—thisis why weather forecasts beyond a few daysare notoriously unreliable. As a result,short-term unpredictability in weather maybe limiting to adaptive plasticity for manyother temperate-zone species with life cy-cles on this time scale. Fourth, there is suf-ficient genetic variation in plasticity ofwing melanin to permit evolutionary re-sponses to selection on plasticity per se.

PHYSIOLOGICAL ACCLIMATION AS ADAPTIVEPLASTICITY

The above section uses research on but-terfly wing melanin to illustrate our pro-posed agenda for studying the evolution ofadaptive plasticity. To apply this agenda tothe study of physiological acclimation,however, we need to broaden the type oftraits we review. For most cases of mor-phological plasticity, including butterflywing melanin, the trait value is determinedduring development and may be fixedthroughout much or all of adult life. In con-trast, many physiological traits have valuesthat vary dynamically with the recent andpresent state of a given individual. Suchtraits are more challenging to study, if onlybecause they can not be characterized by asingle measurement.

The paradigmatic example of a multi-val-ue, labile trait would be thermal perfor-mance curves, which describe the relation-ship between some aspect of physiologicalor organismal performance (or fitness) andtemperature for an individual. An individ-

ual's performance curve can be character-ized by quantifying upper and lower tem-peratures for performance (including sur-vival), thermal performance breadth, andthe optimal temperature (Huey and Steven-son, 1979). [Alternatively, these curves canbe analyzed as "infinite-dimensional traits"(Kirkpatrick and Heckman, 1989).] The im-pact of acclimation of a thermal perfor-mance curve will be manifest as a changein position or shape of the performancecurve, as evidenced for example by a shiftin the optimum temperature.

We will explore two questions dealingwith acclimation and performance curves.First, how much do performance curvesshift with acclimation temperature, and areshifts in position accompanied by shifts inheight (i.e., in maximal performance)? Sec-ond, what is known about the magnitude ofgenetic variation in acclimatory plasticity inthermal performance curves (or in partsthereof)? The first question extends some ofour above comments on Issues 1 and 4,whereas the second question addresses Is-sue 6.

Because of space limitations, we will notreview laboratory tests of the "beneficialacclimation hypothesis," which proposesthat acclimation enhances fitness in the en-vironment that induced it (Leroi et al.,1994; Zamudio et al, 1995; Bennett andLenski, 1997). Several of these tests are el-egant (e.g., Bennett and Lenski, 1997) andcomplement field tests of the "adaptiveplasticity hypothesis." Fortunately, theselaboratory tests have recently been re-viewed (Hoffmann, 1995; Huey and Berri-gan, 1996; Bennett and Lenski, 1997).Those reviews suggest two key points: (1)the laboratory environment offers a su-perb—if arguably artificial—venue for un-ambiguous tests of the adaptive significanceof acclimation, and (2) many of these lab-oratory tests either fail to support BeneficialAcclimation or sometimes actually contra-dict it (Leroi et al, 1994; Zamudio et al,1995; Huey and Berrigan, 1996; Bennettand Lenski, 1997).

Flexibility of acclimationA fundamental issue in acclimation stud-

ies is how much the phenotype shifts in re-



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sponse to acclimation. This issue is relevantnot only to discussions of physiological"compensation" (Precht, 1949), but to gen-eral discussions of physiological adaptationto tropical versus temperate zones (e.g.,Dobzhansky, 1950; Feder, 1977, 1982; Tsu-ji, 1988) or to any constant versus fluctu-ating environment (Levins, 1968; Brownand Feldmeth, 1971).

In a classic study of thermal acclimationin Drosophila, Richard Levins (1969) usedthe term acclimation "flexibility" with ref-erence to the magnitude of an acclimation-induced shift in a phenotypic trait: he quan-tified flexibility as the magnitude of the dif-ference in heat tolerance of individuals ac-climated to two temperatures. Similarly, thedifference in wing melanism could indexthe flexibility of response to a photoperiodtreatment. Note, however, that for the spe-cial case of performance curves or relatedtraits (e.g., optimal, lethal, or preferred tem-peratures), both the trait of interest and theacclimation treatment itself are measured inthe same units (temperature). For suchtraits, acclimation flexibility can be calcu-lated as the slope of the regression of the

trait value on acclimation temperature, suchthat flexibility is a dimensionless number.A flexibility of 1 indicates a positive, 1°Cshift in the trait for each 1°C shift in accli-mation temperature, suggesting completecompensation for acclimation temperature.In contrast, a flexibility of 0 indicates thatthe trait is unaffected by the acclimationtreatments. [Slopes can also be negative, in-dicating an "inverse" response (Forster-Blouin, 1989).]

How flexible, in fact, are thermal perfor-mance curves of ectotherms? Are plastictraits flexible enough to compensate fullyfor temperature shifts? The literature here isimmense (Prosser, 1986), and we have onlymade a cursory search for examples. Brett(1956) tabulated acclimation responses ofupper lethal and for lower lethal tempera-tures for a variety of fish species; and wecalculated flexibilities for both (Fig. 4; seeTable 1). Both traits respond positivelythough weakly (i.e., low slopes) to accli-mation temperature, but the flexibility oflower lethal temperatures is greater thanthat of upper lethal temperatures (paired t-test, P <C 0.001). In general, flexibilities of



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These and many other data {e.g., Cossinsand Bowler, 1987) suggest that thermaltraits in fact may show quite limited accli-mation flexibility. Performance shifts, butnot enough to yield perfect compensation.So why don't traits show greater acclima-tion responses? After all, if environmentalor operative temperature shifts from 10°Cto 20°C, it would seem adaptive for an ec-totherm's optimal temperature to shift from10°C to 20°C as well. Beyond the obviousbut largely untested possibility (see below)that acclimation may have limited impacton fitness in natural populations, we can of-fer three classes of explanations that requireexploration. First, thermoregulation may al-ter the relationship between gross environ-mental temperatures and actual body tem-peratures. If a change in environmentaltemperature does not cause an equivalentchange in body temperature, then the de-gree of acclimation flexibility might be lessthan expected. Second, there may be intrin-sic constraints on the degree of acclimationresponse. These constraints could resultfrom a lack of appropriate genetic variation(see below), from the consequences of par-ticular physiological mechanisms of accli-mation (e.g., Somero, 1978; Cossins andBowler, 1987; Leroi et al., 1994), or be-cause the costs of maintaining or deployingacclimation capacity are excessive relativeto the benefits (Dykhuizen and Davies,1980; Scheiner, 1993; Krebs and Loeschke,1994; Hoffmann, 1995; Krebs and Feder,1997). Third, environmental unpredictabil-ity, as noted above, might in fact select forless than full flexibility, as an animal mak-ing a major acclimation response might infact overshoot the optimal phenotypic shift(Fisher, 1958, pp. 44-45). The asymmetricshape of thermal performance curves mayenhance this effect, as the consequences ex-periencing body temperatures above the op-timal temperature are much greater thanthose of experiencing body temperaturesbelow the optimum.

A related issue is whether acclimation in-fluences the height as well as position ofthermal performance curves. Consider, forexample, Fry and Hart's (1948) pioneering



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study of thermal acclimation of swimmingspeed in goldfish. Between acclimationtemperatures of 5 and 35°C, these fish showa major acclimation response in the optimaltemperature for speed (Fig. 5, flexibility =0.65), suggesting substantial though notcomplete compensation. However, the max-imum speed of fishes at their optimal tem-perature was depressed—sometimes severe-ly—if fish were acclimated to temperaturesother than 25°C (Fig. 5). In fact, after ac-climation to 5°C, the maximum speed offishes at their new optimal temperature wasonly 44% that fish acclimated to 25°C. Ob-viously, acclimation of absolute perfor-mance to low temperature changes theheight as well as the position of the perfor-mance curve; and this may have profoundecological significance.

Genetic variation in thermal acclimationHow much genetic variation within pop-

ulations exists for acclimation response?The fact that acclimation responses oftendiffer among populations and species (Lev-ins, 1969; Prosser, 1986; but see Hoffmannand Watson, 1993) strongly implies that ge-netic variation in acclimation capacity doesexist within populations. Nevertheless, di-rect evidence of genetic variation in phys-

iological acclimation within populations isremarkably meager (see Huey and Berri-gan, 1996). As for other aspects of pheno-typic plasticity (see Issue 6 above), geneticvariation in thermal acclimation may be ex-plored using studies involving breeding de-signs or selection experiments in the labo-ratory.

Studies of genetic variation must distin-guish between genetic variation in meantrait value from variation in plasticity per se(cf. Falconer, 1989; Via and Lande, 1985).For example, Gibbs et al. (1991) sampledfamilies of grasshoppers (Melanoplus san-guinipes) from 18 populations, raised themunder several seasonal regimes differing intemperature and photoperiod, and thenmeasured melting temperatures of epicutic-ular lipids, which provide a primary barrierto water loss. Melting temperatures differedsignificantly among populations, amongfamilies within populations, and amongseasonal treatments; but were unaffected byinteractions between treatment and popula-tion or between treatment and family withinpopulations. Thus, despite documentingsignificant genetic variation in melting tem-peratures, Gibbs et al. (1991) found no ev-idence of genetic variation in acclimationability, either among sites or among fami-



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lies within sites. In a subsequent analysis,Gibbs and Mousseau (1994) found no evi-dence of genetic variation in the timecourse of acclimation. Similarly, Loeschckeand Krebs (1994) found no variation in ac-climation to high temperature stress amongisofemale lines of Drosophila buzzatii.However, Krebs and Feder (1997) have re-cently found variation among isofemalelines of D. melanogaster in Hsp70 expres-sion and in inducible thermotolerance oflarvae.

Clonal organisms are particularly ame-nable for studying the genetical architectureunderlying acclimation responses. For ex-ample, Walton et al. (1995) examined vari-ation in acclimation response to tempera-ture in four strains of a clonal protist, Eu-plotes vannus, each from a different localityin Italy and nearby islands. Their data sug-gest inter-strain variation in acclimation re-sponses, though it is not clear whether thevariation is in the magnitude or in the ra-pidity of the acclimation response.

Jon Herron and D. Pepin (Herron, 1996)have done the most complete and elegantstudy to date of the genetic basis of thermalacclimation, using clones of the multicel-lular alga, Volvox aureus, from a singlepopulation. They studied genetic variationin the impact of acclimation temperature onthe thermal dependence of swimmingspeed, using light as a stimulus to induceswimming in these positively phototacticalgae. Herron and Pepin raised clone-matesat three temperatures and then measuredtheir thermal sensitivity of performance(swimming speed at five temperatures). Be-cause they then replicated the entire exper-iment, they were able to determine whetherthe acclimation responses of clones were re-peatable (thus genetic). Acclimation flexi-bility (as denned above) for optimal swim-ming not only differed significantly amongclones, but was also highly repeatable be-tween replicates. Consequently, the sensi-tivity of thermal performance to acclima-tion temperatures appears to vary geneti-cally in V. aureus (i.e., significant "broadsense" heritabilities).

Natural selection in the laboratory hasalso been used to uncover evidence of ge-netic variation in plasticity. Cavicchi et al.

(1995) detected significant divergence inacclimation responses of heat tolerance andof heat hardening in replicated populationsof D. melanogaster that had been evolvingby laboratory natural selection for 15 yearsat either 18, 25, or 29°C differ in their ac-climation responses and in heat hardening(Cavicchi et al., 1995). Similarly, McDanielet al. (1995) found that apparent adaptationof D. tripunctata and D. robusta to labo-ratory conditions resulted in a diminutionof their acclimation response.

Bennett and Lenski (1997) have recentlydemonstrated that the acclimation responseof the bacterium Escherichia coli dependson the "historical" temperature at whichthe bacteria have been evolving. For ex-ample, bacteria that were evolved at 32°C(2,000 generations) and also were accli-mated to 32°C had higher fitness at 37°Cthan those same bacteria if acclimated toand then tested at 37°C. This result clearlycontradicts the "beneficial acclimation hy-pothesis" but is consistent with the "opti-mal acclimation temperature model," re-viewed in Huey and Berrigan (1996).

This brief review demonstrates that ourunderstanding of the magnitude of geneticvariation in thermal acclimation responsesis strikingly limited: clearly this is an openniche for evolutionary physiologists. Stud-ies with clonal organisms (Walton et al.,1995; Herron, 1996), isofemale lines (Loes-chcke and Krebs, 1994; Krebs and Feder,1997), selected lines (Cavicchi et al., 1995;Bennett and Lenski, 1997), or geographi-cally separated populations (Tsuji, 1968;Hoffmann and Watson, 1993) may be par-ticularly valuable, both to document geneticvariation and to isolate strains or lines dif-fering in acclimation (Hoffmann, 1990).Those strains can be exploited not only tobegin to elucidate physiological mecha-nisms underlying variation in acclimationresponses, but also to use in studies of thefunctional consequences of variation in re-sponses (Krebs and Feder, 1997).

FUTURE STUDIES OF EVOLUTION OFPLASTICITY

Physiologists have provided a detailedunderstanding of the mechanisms underly-ing plasticity of many physiological traits



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(e.g., Somero, 1978). In addition, the con-sequences of thermal acclimation for per-formance and even fitness in the lab havebeen well described in a number of studysystems (see Huey and Berrigan, 1996;Bennett and Lenski, 1997). By comparison,the developmental mechanisms underlyingplasticity of morphological traits are morepoorly known in most instances (e.g.,Scheiner, 1993). However, several evolu-tionary aspects of acclimation seem ripe forstudy:

First, laboratory tests are an efficient andeffective way of exploring the adaptive sig-nificance and evolution of acclimation re-sponses (Leroi et ah, 1994; Zamudio et al.,1995; Bennett and Lenski, 1997). However,we believe that laboratory results need tobe validated in nature. Certainly, as was ev-ident in the example of butterfly melaninpatterns (above), the relationship betweenplasticity and fitness in the nature is rarelyas straightforward as functional and labo-ratory studies might predict. Ultimately,field studies will need to score not only howplasticity influences survival, but also howplasticity influences reproduction, for it isentirely possible that a "costly" trait mightincrease survival, but simultaneously lowerreproduction and hence potentially lowerfitness.

Second, additional studies of geneticvariation in acclimation are needed. Inter-estingly, nearly all studies of morphologicaltraits have detected substantial genetic vari-ation in plasticity (Scheiner, 1993), whereasthe few studies to date on thermal accli-mation are mixed (above). Is this discrep-ancy merely an artifact of sample size or ofrelative measurement error, or is it a realdifference between morphological andphysiological plasticity?

Third, the role of environmental unpre-dictability for the evolution of plasticity hasbeen widely discussed in theoretical analy-ses, but remains virtually unexplored in em-pirical studies (Levins, 1968; Moran, 1992).Physiological and morphological traits mayshow different responses in this regard. Forexample, the time lag between environmen-tal determination and expression of physi-ological acclimation is sometimes short(minutes to days), whereas that involving

morphological traits often involves longertime lags. Further, physiological acclima-tion is usually reversible, whereas morpho-logical plasticity is often much less so. Ap-propriate use of long-term weather datamay be particularly valuable for analysingenvironmental unpredictability in relationto plasticity of physiological (and certainmorphological) traits. For example, G. Da-vidowitz has explored the relationship be-tween variability and predictability in pre-cipitation to plasticity in age and size at ma-turity in pallid-wing grasshoppers (Trimer-otropis pallidipennis) in the southwesternU.S. (G. Davidowitz, unpublished results).In addition, the asymmetric shape of ther-mal performance curves can have importantconsequences for the evolution of perfor-mance curves (Gilchrist, 1995); mathemat-ical models exploring how these conse-quences impact the evolution of acclimationmay be instructive.

Finally, we need to address the questionof why physiological traits appear to showlimited flexibility (Table 1). A related issueis why the magnitude of performance canbe affected by acclimation (Fig. 5).

These are fundamental—if complex—is-sues. However, our understanding of theevolution of thermal acclimation, and ofplasticity more generally, requires their ex-ploration. We believe that the field of ther-mal acclimation offers special opportunitiesand challenges.

ACKNOWLEDGMENTS

We thank J. Harrison and J. Phillips forthe opportunity to participate in this sym-posium. We acknowledge thoughtful com-ments on the manuscript from A. F. Ben-nett, K. Miller, J. Schmitt, W. Zamer, andfour anonymous reviewers as well as con-structive discussions with D. Berrigan andG. Gilchrist. We thank G. Davidowitz forallowing us to cite unpublished results fromhis Ph.D. research. The writing of this pa-per was supported by NSF EBN 9419850 toJGK and IBN 9514205 to RBH.

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