ECosCIENCE 7 (1) : 18-24 (2000)

Phenotypic plasticity, defined as the ability of the samegenotype to produce different phenotypes, is a taxonomicallywidespread and often very conspicuous phenomenon(Stearns, 1992; Scheiner, 1993). During the last ten years,the study of phenotypic plasticity and its genetic basis hasbecome extremely popular (see Stearns, 1992; Scheiner1993; Schlichting & Pigliucci, 1998 for reviews), although

several controversies have emerged as well (Via et al.,1995; Gotthard & Nylin, 1995). However, both theoreticaland conceptual development have been rapid, and theamount of empirical evidence for adaptive plasticity isaccumulating rapidly. One particularly intensively studiedsystem in the context of adaptive plasticity is the timing ofamphibian metamorphosis in unpredictable environments(Newman, 1992; Gotthard & Nylin, 1995). Several studieshave found that individuals exposed to a short hydroperiodtend to metamorphose earlier than those exposed to a longerhydroperiod. This has been interpreted as evidence foradaptive plasticity, since failure to metamorphose before

Adaptive phenotypic plasticity in timing of meta-morphosis in the common frog Rana temporaria1

Juha MERILÄ2, Anssi LAURILA3, Maarit PAHKALA, Katja RÄSÄNEN & Ane TIMENES LAUGEN,DEpartment of Population Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18d, SE-752 36 Uppsala, Sweden, e-mail: juha.merila@zoologi.uu.se

Abstract: Unpredictable environments are expected to select for adaptive plasticity in traits enabling adjustment of phenotypeto prevailing environmental conditions. Common frogs (Rana temporaria) breed frequently in ponds, which dry up beforethe aquatic larvae have metamorphosed, and consequently, plasticity in timing of metamorphosis in response to pond dryingcould be adaptive. We investigated the responses of half- and full-sib R. temporaria larvae to simulated pond drying in a factorialexperiment to test whether there is adaptive phenotypic plasticity in timing of metamorphosis, and whether this plasticity isgenetically determined. As expected under the adaptive hypothesis, we found that larvae exposed to the decreasing watertreatment metamorphosed significantly faster than their sibs in the constant water treatments. Furthermore, age and size atmetamorphosis were positively correlated in the constant water treatments, but negatively correlated in the decreasing watertreatment. However, larvae from decreasing water treatment metamorphosed, on average, at a smaller size as compared tolarvae from the constant water treatments, even after controlling for variation in developmental time. Since smaller size atmetamorphosis is likely to be related to reduced fitness, this indicates that faster development may trade off with othercomponents of fitness. The results further show that the amount of food received during the four first days of developmentinfluenced age and size at metamorphosis, reinforcing the view that early life nutrition may have a significant impact on laterlife fitness. Although there was a genetic component to developmental rates, we found no evidence for genetic variation inplasticity. In accordance with evidence from other studies, our results suggest existence of adaptive phenotypic plasticity inamphibian development.Keywords: adaptation, body size, genetic variation, metamorphosis, phenotypic plasticity, Rana temporaria.

Résumé : Il est attendu que les environnements imprévisibles sélectionnent pour une plasticité adaptative des traits permettantun ajustement du phénotype aux conditions environnementales qui prévalent. Les grenouilles communes (Rana temporaria)se reproduisent fréquemment dans les mares, lesquelles s’assèchent avant que les larves aquatiques ne se soient métamorphosées;en conséquence, une plasticité dans le moment de la métamorphose en réponse à l’assèchement de la mare pourrait êtreadaptative. Par une expérience factorielle, nous avons étudié les réponses de larves de R. temporaria soeurs et demi-soeurs àun assèchement de mare simulé afin de tester s’il existe une plasticité phénotypique adaptative dans le moment de lamétamorphose et si cette plasticité est génétiquement déterminée. Tel que prévu sous l’hypothèse adaptative, les larvesexposées au traitement d’assèchement se sont métamorphosées significativement plus rapidement que leurs soeurs ayant reçuun apport hydrique constant. De plus, l’âge et la taille à la métamorphose étaient positivement corrélés dans le cas d’unapport hydrique constant, mais négativement corrélés dans le cas du traitement d’assèchement. Cependant, les larvesexposées au traitement d’assèchement se sont métamorphosées, en moyenne, à une taille inférieure à celle des larves ayantreçu un apport hydrique constant, ceci même après avoir contrôlé pour la variation dans le temps de développement. Commeune plus petite taille à la métamorphose risque d’être associée à une réduction de la valeur adaptative, ce résultat indiquequ’un développement plus rapide pourrait entrer en conflit avec d’autres composantes de la valeur adaptative. Les résultatsmontrent également que la quantité de nourriture reçue durant les quatre premiers jours de développement influence l’âge etla taille à la métamorphose, ce qui appuie l’idée que la nutrition lors des premiers stades de vie peut avoir un impactsignificatif sur la valeur adaptative des stades de vie ultérieurs. Bien qu’il y ait une composante génétique dans les taux dedéveloppement, nous n’avons trouvé aucune preuve de variabilité génétique dans la plasticité. En accord avec d’autres études,nos résultats suggèrent l’existence d’une plasticité phénotypique adaptative dans le développement des amphibiens.Mots-clés : adaptation, taille corporelle, variabilité génétique, métamorphose, plasticité phénotypique, Rana temporaria.

Introduction

1Rec. 1999-03-09; acc. 1999-10-19.2Author for correspondence. 3Additional address: Integrative Ecology Unit, Division of Population Biology, Departmentof Ecology and Systematics, Box 17, FIN-00014 University of Helsinki, Finland.

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pond drying would lead to zero life time reproductive success.However, the proximate mechanisms inducing accelerateddevelopment in short term ponds are not clear (Newman,1992; Gotthard & Nylin, 1995). In natural situations, theshort duration ponds are on average warmer than the longduration ponds, and the earlier metamorphosis in shortduration ponds could represent a response to highertemperature (Newman, 1989; 1992; Gotthard & Nylin,1995). Likewise, in short duration ponds, the decreasingwater level is accompanied by increased density which inturn may diminish the per capita foraging returns andinitiate earlier metamorphosis (Wilbur & Collins, 1973;Alford & Harris, 1988; Newman, 1992; Laurila & Kujasalo,1999). However, the attempts to explore the possible geneticbasis of plastic responses in absence of food competition arestill rare (Newman 1988a; Semlitsch & Reyer, 1992;Reques & Tejedo, 1997).

The aim of this study was to investigate phenotypicplasticity in timing of metamorphosis in response tohydroperiod in the common frog Rana temporaria (L.).In particular, we tested whether there is any evidence foraccelerated development in response to decreasing watervolume when confounding effects of temperature and densitywere controlled for, and whether the relationship betweensize and age at metamorphosis differed in response to waterlevel treatments. This relationship is usually positive(Wilbur & Collins, 1973; Woodward, Travis & Mitchel,1988; Newman, 1989), but Alford & Harris (1988; see alsoKaplan, 1985) showed that a declining resource access canproduce a negative relationship. Furthermore, we used ahalf-sib design to study whether there was any evidence forgenetic variation for accelerated development, i.e., geneticvariation in phenotypic plasticity.

Material and methods

The animals used in this study originated from a popu-lation breeding in Tvedöra-pond situated ca 10 km west ofLund, southern Sweden (55° 40’ N, 13° 30’ E). This pondfrequently dries up, and hence catastrophic losses ofcomplete cohorts have probably occurred in the past(J. Loman, pers. com.). In early April 1998, adult commonfrogs were collected, transferred to the laboratory inUppsala, and mated artificially to produce 16 half- and full-sibfamilies as depicted in Table I. The fertilizations wereperformed following Berger, Rybacki & Hotz (1994; withslight modifications) giving us full control over the identityof the parents. The eggs developed at a constant 22°C untilgill absorption was complete (stage 25; Gosner, 1960).From this stage onwards, the larvae were raised individuallyat constant 22°C (± 1°C) in 0.8-L containers under eitherhigh (half of the larvae) or low food ratio (half of the larvae)for four days, after which they were divided into threedifferent water level treatments. The treatments were:(i) constant low water level (ca 0.2 L; corresponding to awater column height of ca 2 cm), (ii) constant high waterlevel (0.8 L; corresponding to a water column height ofca 8 cm), and (iii) decreasing water level treatment, in whichthe initial water level (and volume) was the same as for thehigh water level treatment, but this level was successivelyreduced every seventh day by ca 0.2 L (i.e., ca 2 cm) until

the level corresponding to constant low water level wasreached. Since we had no a priori prediction about thelength of the larval period in the two constant water leveltreatments, they together formed a contrast group againstwhich the treatment effects were evaluated (see below).

The tadpoles were fed during water exchanges everyseventh day with a finely ground 1:3 mixture of TetraMin(Ulrich Baensch GmbH, Germany) fish flakes and rodentpellets. (AB Joh. Hansson, Uppsala). The initial food level(after the two-day period on either low [15 mg] or high[30 mg] food level) was 60 mg for the first week, afterwhich it was increased to 120 mg and maintained at thislevel until metamorphosis. The timing of metamorphosis,defined here as the stage when one of the forelimbs hademerged (stage 42; Gosner, 1960), was determined by dailychecks. To obtain a measure of size at metamorphosis, allmetamorphs were weighed with an electronic balance tothe nearest 0.0001 g.

The breeding design adopted in this study consisted offour females each of which were mated to four differentmales, yielding a total of 16 half-and full-sib families(i. e. = crosses; Table I). Within each cross, the experimentsutilized 12 randomly selected larvae which were dividedinto two food level treatments (6 + 6), and further into threewater level treatments (4 + 4 + 4). Hence, there were twolarvae per cross in each combination of water and food leveltreatments, each located in one of the two blocks eachconsisting of three shelves (Table I). These data were ana-lyzed in a factorial design using a mixed-model ANOVA asimplemented in PROC MIXED in SAS (Littell et al., 1996).The factors in our design were: block (random), dam (random),sire nested within dams (random), water level treatment(fixed), and food treatment (fixed). Since the block effectsdid not explain any variation in size and timing of metamor-phosis, they were pooled with the error term. All possibleinteractions between independent variables were initiallyincluded in the models, but excluded if non-significant, with

TABLE I. Schematic presentation of the breeding design utilized inthe experiment. In this design, each of the four females (dams)were crossed with four different males (sires). Each cross included12 larvae which were divided under two food and three waterlevel treatments. Hence, there were two larvae per cross undereach possible combination of water and food levels

Male # Female #

1 2 3 4

1 ¥2 ¥3 ¥4 ¥5 ¥6 ¥7 ¥8 ¥9 ¥10 ¥11 ¥12 ¥13 ¥14 ¥15 ¥16 ¥

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the constraint that the water ¥ sire and water ¥ food interac-tions were always retained since they tested hypotheses ofcentral interest. As we were also interested in investigatingwhether larvae from different water level treatments woulddiffer in size after accounting for differences in the lengthof the larval period (larval period and size at metamorphosisare usually highly correlated), we also performed an analysisin which time to metamorphosis was included in the modelas a covariate. The test among decreasing and constant leveltreatments was performed with a planned contrast using the‘Contrast’ option in PROC MIXED (Littell et al., 1996).This contrast was performed by pooling the two constantwater treatments when comparing them against decreasingwater treatment. Since there was no a priori predictionabout the direction of difference between the two constantwater treatments, the difference between them was tested aposteriori on adjusted means using the Tukey-Kramercorrection in PROC MIXED (Littel et al., 1996). Becausein some crosses all larvae died before metamorphosing, theoriginal sample size of 192 was reduced to 133, and thedesign was unbalanced.

The quantitative genetic interpretation of the effects inour model are as follows. The term dam estimates 1/4 ofadditive genetic variance, but includes also genetic and envi-ronmental maternal effects if present (Lynch & Walsh, 1998).The term sire estimates 1/4 of additive genetic effects, but italso includes 1/4 of dominance variance if such was present.Evidence for adaptive genetic plasticity would be providedby a significant interaction between sire and water leveltreatment effects. Significant interaction between dam andwater level treatment could also provide evidence for adaptivegenetic plasticity, but it could also result from interactionbetween maternal and treatment effects.

To check whether temperatures at different levels ofwater treatment differed, water temperatures were measuredat eight high and 13 low water level vials during the middleof the experiment. There was indeed a slight difference inaverage temperature between high (x = 21.33, SE = 0.03)and low (x = 21.12, SE = 0.04) water level treatments (t-test:t = 3.45, df = 19, p > 0.003), possibly because of the highercooling effect of small water volume. However, thesedifferences are unlikely to influence our conclusions fortwo reasons. First, a faster development of larvae from thedecreasing water level treatment than from the high waterlevel treatment would provide evidence for adaptive plasticity,yet this test would be a conservative one. Second, althoughthere was no difference in water temperatures among theblocks (ANOVA: F1,42 = 0.30, p = 0.83), the differences in watertemperatures among different water level treatments weremuch smaller than the differences in water temperature amongdifferent shelves within the blocks (Shelf 1: 22.4 ± 0.15°C ;Shelf 2: 22.1 ± 0.17°C; Shelf 3: 21.6 ± 0.15°C; ANOVA:F2,45 = 6.51, p < 0.004), yet there were no shelf effects on anyof the response variables (p > 0.10 in all cases).

All statistical analyses were performed with 6.12 versionof the SAS statistical package (SAS, 1996), or withStatView 5.0 (SAS, 1998). Weight and age at metamorphosiswere log-tranformed before statistical analyses to homogenizevariances between treatment groups. Satterthwaite proce-dure was used to obtain corrected degrees of freedom inmixed model analyses (Littell et al., 1996).

Results

DEVELOPMENT TIME

Timing of metamorphosis differed significantlybetween different water treatments, being shortest for thosein decreasing water level, intermediate in constant highwater level, and longest for those in constant low waterlevel treatment (Table II; Figure 1). The ‘decreasing versusconstant water level’ contrast revealed that the larvae indecreasing water level treatment metamorphosed significantlyearlier as compared to their sibs in constant water leveltreatment (Table II). There was no difference in timing ofmetamorphosis between the two constant water treatments(Tukey-Kramer, p > 0.05). Timing of metamorphosis wasalso affected by the initial food level, and larvae exposed toinitially high food level metamorphosed significantly earlierthan those exposed to low food treatment (Table II). Thedam main effect was not significant, whereas the significantsire effect indicated significant male genetic contribution totiming of metamorphosis (Table II). As all the otherinteractions in the model, the sire ¥ water treatmentinteraction did not account for any variation in the timing ofmetamorphosis (Table II), giving little evidence for geneticvariation in plasticity in timing of metamorphosis.

SIZE AT METAMORPHOSIS

Size at metamorphosis was not influenced by foodtreatment, and neither dam nor sire contribution to meta-morphic size were significant (Table IIIa). However, watertreatment had a significant effect on size at metamorphosis(Table IIIa, Figure 1), and since the contrast between constantand decreasing water treatments was significant, thissuggests that the larvae from constant water treatmentattained a significantly larger size at metamorphosis thanthe larvae from decreasing water treatment (Table IIIa,Figure 1). However, these results may not be surprising inlight of the fact that size and age at metamorphosis areusually positively correlated; therefore, we repeated theanalysis by introducing timing of metamorphosis into theanalysis as a covariate. The results of this analysis revealedseveral interesting points. First, as expected, the timing ofmetamorphosis had a nearly significant main effect on sizeat metamorphosis, but there was also a significant interac-tion effect between water level treatment and timing ofmetamorphosis on weight (Table IIIb). A closer lookrevealed that this interaction occurred because in constantwater level treatments, the correlation between size and

TABLE II. Mixed model nested ANOVA of developmental time.‘Decreasing versus Constant’ = contrast between decreasing andconstant water treatments. Var. = variance component, ddf = deno-minator degrees of freedom, ndf = numerator degrees of freedom

Random effects Var. ± SE z P

Dam 0.0005 ± 0.0014 0.34 0.37Sire (Dam) 0.0059 ± 0.0007 2.02 0.021Water ¥ sire 0.0000 - -Residual 0.0058 ± 0.0008 7.52 < 0.0001

Fixed effects ndf ddf F P

Water 2 114 4.18 0.018Food 1 115 4.73 0.032Food ¥ water 2 114 2.99 0.054Decreasing versus Constant 1 114 4.49 0.036

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timing of metamorphosis was positive, whereas in thedecreasing water level treatment it was negative (Figure 2).Second, the initial food level treatment had a significanteffect on metamorphic size (high: 0.25 ± 0.007 g; low:0.23 ± 0.007 g), suggesting a long lasting carry-over effecton metamorphic size (Table IIIb). Finally, the contrastbetween constant and decreasing water level treatmentssuggests that metamorphic size was significantly higher inconstant than in decreasing water level treatments (Table IIIb).

Discussion

Our results indicate that decreasing water volume willinduce earlier metamorphosis in the common frog, as wellas lead to changes in the relationship between timing andsize at metamorphosis. Since the confounding effects oftemperature and increasing density were controlled for,effects which usually accompany reduction of water level innatural situations, these findings suggest that the environ-mental cue(s) triggering earlier metamorphosis is directlyrelated to changes in water volume. For example, constantlow water level, combined with ample per capita food level,did not speed up development, but a change in watervolume induced the earlier metamorphosis. Hence, theresults are in accordance with those of several other studieswhich have found evidence for extensive plasticity in timingof amphibian metamorphosis (Wilbur & Collins, 1973;Wilbur, 1987; Semlitsch & Wilbur, 1988; Newman, 1988a;Crump, 1989; Morey & James, 1994; Denver, Mirhandi &Phillips, 1998; Laurila & Kujasalo, 1999), and in particular,suggest that this plasticity might have adaptive value inallowing tadpoles to escape the drying pond habitat(Newman, 1992; Gotthard & Nylin, 1995).

We found that the relationship between metamorphicsize and timing of metamorphosis differed between constantand decreasing water treatments. While the size of the larvaefrom both low and high constant water treatments increasedwith increasing age, the opposite was true for the larvaefrom the decreasing water level treatment. The correlationbetween size and developmental time in R. temporaria(J. Merilä & A. Laurila, unpubl. data) and other amphibiansis usually positive (Wilbur & Collins 1973, Newman, 1989;Semlitsch, 1993), but exceptions to this pattern have beennoted (Travis, 1983; 1984; Smith, 1987; Pfenning, Marby &Orange, 1991). Alford & Harris (1988; see also Kaplan,1985) showed that decreasing food availability during devel-opment could select for a negative correlation between ageand size at metamorphosis, and this was provided as anexplanation for the generally negative relationship betweenage and size in metamorphosis in Scaphiopus multiplicatusin which food resources decline rapidly with time (Pfenning,Marby & Orange, 1991). As for our results, we suggest thatthe negative relationship between age and size at metamor-phosis could reflect adaptive phenotypic plasticity: whenfaced with increased risk of pond drying, it would obviouslybe beneficial to lower the size threshold for metamorphosisand metamorphose at a smaller size. This is because even ifmetamorphosis at a smaller size may mean loss of fitness(metamorphic size and fitness are positively correlated:Smith, 1987; Semlitsch, Scott & Pechmann, 1988), a failureto metamorphose before the pond has dried out will give nofitness at all.

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FIGURE 1. Effects of water level treatment on developmental rate (= ageat metamorphosis in days), size at metamorphosis and age adjusted size(= residual size) at metamorphosis. The values are least square means (± SE)adjusted for other effects in models presented in Tables II and III.

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At a more proximate level, Denver’s (1997) studies onlarval stress responses infer a possible physiological mecha-nism behind the negative correlation between age and sizeat metamorphosis. Denver (1997) found that the amount ofcorticosteroid hormones increased in tadpoles stressed bydrying pond conditions, and because corticosteroids affectappetite, this could lead to a negative correlation betweensize and age at metamorphosis. Hence, this explanationbased on Denver’s (1997) results provides an intrinsicphysiological explanation that parallels the extrinsicallyderived model of Alford & Harris (1988): Both explanationsfor negative size-age relationship evoke reduced resourceutilization/access as a cause for smaller size of latermetamorphosing larvae. These explanations are alsoconsistent with models of metamorphosis (Wilbur &

Collins, 1973; Ludwig & Rowe, 1990), and with empiricaldata (Alford & Harris, 1988; Newman, 1994), the latter ofwhich suggests that decreasing growth rate is sufficient totrigger an earlier metamorphosis. For example, earlier workwith R. temporaria suggests that tadpole growth rate slowsdown as water level declines (Laurila & Kujasalo, 1999).

Because size at metamorphosis in many amphibians iscorrelated with juvenile survival (Smith, 1987), adult bodysize (Berven & Gill, 1983), timing of sexual maturity(Smith, 1987; Semlitsch, Scott & Pechmann, 1988), andreproductive success in both males and females (Salthe &Duellman, 1973; Howard, 1980), large size at metamorphosiscan be expected to be associated with increased fitness. Wefound that while metamorphosing earlier than the indi-viduals from the constant water treatments, the larvaefrom the decreasing water treatment metamorphosed at asmaller size than the larvae from the constant high watertreatment when the timing of metamorphosis was controlledfor. Consequently, this suggests that early metamorphosis,while adaptive in the sense of securing survival, may tradeoff with other components of fitness. The fact that the larvaefrom the constant low water treatment also metamorphosedat a rather small size may indicate that constant low waterlevel, together with high concentration of food relative towater volume, may have had a negative effect on growth.However, as the relationship between size and timing ofmetamorphosis differed between low constant and decreasingwater level treatments, the causes for small metamorphicsize in these two groups are likely to be different.

There was a genetic contribution to the timing of meta-morphosis as indicated by the large sire contribution to thevariation in the length of larval period. This is in accordancewith the results of Plytycz, Dulak & Pecio (1984), whodemonstrated genetic control of larval period in anotherpopulation of R. temporaria, but contrasts with the resultsof some other studies in which non-genetic maternal factorswere found to be the main source of variation in develop-mental time (Travis, 1981). However, the lack of maternalcontribution to timing of developmental rate could be due tothe small number (n = 4) of female parents used in thisstudy. Furthermore, the size of the male contribution was solarge, that it corresponds to a broad sense heritability esti-mate larger than unity, which could be due to the fact that

TABLE III. Mixed model nested ANOVA and ANCOVA of size (= weight) at metamorphosis. ‘Decreasing versus Constant’ = contrastbetween decreasing and constant water treatments. Var. = variance component, ndf = numerator degrees of freedom. ddf = denominatordegrees of freedom.

a) ANOVA b) ANCOVARandom effects Var ± SE z p Var ± SE z p

Dam 0.0001 ± 0.0001 0.85 0.20 0.0003 ± 0.0004 0.72 0.23Sire (Dam) 0.0001 ± 0.0001 0.60 0.27 0.0003 ± 0.0003 0.78 0.22Water ¥ Sire 0.0000 0.0000 Residual 0.0017 ± 0.0002 7.57 < 0.0001 0.0045 ± 0.0005 7.48 < 0.0001

Fixed effects ndf ddf F p ndf ddf F p

Water 2 118 5.79 0.004 2 118 6.45 0.002Food 1 119 2.24 0.137 1 117 7.53 0.007Food ¥ Water 2 117 0.70 0.497 2 114 2.10 0.127Age at metamorphosis 1 81.4 3.81 0.054Age ¥ Water 2 119 6.49 0.002

Decreasing versus Constant 1 118 4.80 0.030 1 121 9.77 0.002

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FIGURE 2. Size as a function of age at metamorphosis in days inRana temporaria in three different water level treatments. Heavy continuousline = decreasing water level, thin continuous line = constant high watertreatment; stippled line = constant low water level. The slopes of these least-square regressions are significantly different for constant and decreasingwater level treatments (p < 0.05; for formal statistical test see Table III).

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the male component also captures 1/4 of the non-additivevariance, which has been suggested to be typically large fortraits closely associated with fitness (Crnokrak & Roff, 1995)

We found no evidence for genetic variation in plasticityitself suggesting that regardless of their genetic background,offspring from different parentages responded to the waterlevel treatments in a similar manner. This contrasts with thefindings of Newman (1988b) and Reques & Tejedo (1997),who have found genetic variation in tadpole responses todifferent drying regimes. There are two possible explana-tions for these contrasting results. First, the relatively smallsample sizes in this study, together with the large variancein timing of metamorphosis may make it difficult to detectanything but very large interaction effects between parentageand drying regime. As the breeding design was far fromoptimal for detecting weak interaction effects (Kearsey &Pooni, 1996), the results should not be taken as evidence forlack of genetic variation in plasticity itself. Second, it is alsopossible that there is little or no genetic variation in plasticresponses to pond drying, perhaps because it has been lostfrom the study population, or from the species as a whole.However, further work is required to distinguish betweenthese alternatives.

Finally, an additional finding of this study meritsdiscussion, namely, the fact that the effect of food ratioduring the four initial days of development as free-swimmingand feeding larvae had an effect on both age and size atmetamorphosis. There is increasing evidence from amphibians(Wilbur, 1980; Travis & Trexler, 1986) and other vertebrates(Haywood & Perrins, 1992; Merilä & Svensson, 1996;Desai & Halles, 1997), that conditions experienced duringearly development can influence various fitness-relatedtraits during later life. Hence, although there is great flexi-bility in developmental trajectories, for example in thesense that the influence of initially poor environmentalconditions can be at least sometimes reversed if feedingconditions improve, the conditions experienced in earlydevelopment seem to leave a permanent trace on thedevelopment of the common frog. Such effects, whetherinduced by early environmental or maternal/paternal effects,may have important evolutionary and population levelconsequences (Bernando, 1996; Rossiter, 1996).

In conclusion, the results of this study suggest that com-mon frogs are able to speed up their metamorphosis in theface of pond drying, and that the accelerated metamorphosisis accompanied by smaller size at metamorphosis. Althoughthere is genetic variation in developmental time, we foundno evidence for a genetic basis for the variation in plasticresponse to water level treatment. Although our results donot allow us to identify the precise environmental cue(s)triggering the accelerated metamorphosis in desiccatinghabitat, they suggest that elevated temperature or physicalinteractions between tadpoles are not required as cues toaccelerate development. These findings add to the increasingevidence that amphibians are capable of responding adap-tively to habitat desiccation, but more detailed and extensivestudies of within- and among-population genetic variation inthis plasticity would be helpful to gain a better understandingof how different populations will respond to increased desic-cation stress brought about by global climate warming.

Acknowledgements

We thank N. Kolm, E. Karvonen, F. Söderman and G.Wickström Løe for help during the course of this study. Commentsfrom S. Nylin and two anonymous referees helped to improve anearlier version of this manuscript. Our work was supported by grantsfrom the Swedish Natural Science Research Council (grantB-AA/BU 12029-304), Maj and Thor Nessling Foundation (project#98053), Academy of Finland (A. Laurila) and NorFA (A. Laurila,J. Merilä, M. Pahkala, K. Räsänen).

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