Research article

Reaction norms for age and size at maturity in response to

temperature: a test of the compound interest hypothesis

KLAUS FISCHER1,* and KONRAD FIEDLER2

1Institute of Evolutionary and Ecological Sciences, Section Evolutionary Biology, Leiden University,

P.O. Box 9516, NL-2300 RA Leiden, The Netherlands; 2Department of Animal Ecology I, Bayreuth

University, D-95440 Bayreuth, Germany

(*author for correspondence, tel: +31-71-5274877; fax: +31-71-5274900; e-mail: fischer@

rulsfb.leidenuniv.nl)

Received 10 September 2001; accepted 18 March 2002

Co-ordinating editor: O. Leimar

Abstract. In ectotherms, temperature induces similar developmental and evolutionary responses in

body size, with larger individuals occurring or evolving in low temperature environments. Based on

the occasional occurrence of opposite size clines, showing a decline in body size with increasing

latitude, an interaction between generation time and growing season length was suggested to

account for the patterns found. Accordingly, multivoltine species with short generation times

should gain high compound interest benefits from reproducing early at high temperatures, indi-

cating potential for extra generations, even at the expense of being smaller. This should not apply

for obligatorily monovoltine populations. We explicitly test the prediction that monovoltine

populations (no compound interest) should be selected for large body size to maximise adult fitness,

and therefore size at maturity should respond only weakly to temperature. In two monovoltine

populations (an Alpine and a Western German one) of the butterfly Lycaena hippothoe, increasing

temperatures had no significant effect on pupal weight and caused a slight decrease in adult weight

only. In contrast, two closely related, yet potentially multivoltine Lycaena populations showed a

greater weight loss at increasing temperature (in protandrous males, but not in females) and smaller

adult sizes throughout. Thus, the results do support our predictions indicating that the compound

interest hypothesis may yield causal explanations for the relationship between temperature and

insect size at maturity. At all temperatures, the alpine population had higher growth rates and

concomitantly shorter development times (not accompanied by a reduction in size) than the other,

presumably indicating local adaptations to different climates.

Key words: age and size at maturity, body size, butterfly, compound interest, development, growth,

reaction norm, temperature-size-rule

Introduction

For animals, the considerable and wide-ranging ecological importance of body

size is clearly demonstrated by its effect on e.g. fecundity, metabolic rates,

dispersal, competitive, predatory and defensive abilities, capability to with-

stand starvation and desiccation (Peters, 1983; Calder, 1984; Schmidt-Nielsen,

Evolutionary Ecology 16: 333–349, 2002.� 2002 Kluwer Academic Publishers. Printed in the Netherlands.

1984; Partridge and Fowler, 1993; Blanckenhorn, 2000). Hence, understanding

how natural selection acts in the evolution of this key life-history trait is of

special concern in evolutionary ecology (Partridge and French, 1996). A par-

ticularly important and widespread correlate of size-differences in ectotherms is

temperature. The thermal environment experienced by an individual during

development has a direct effect on final size, with body size decreasing as

temperature increases and vice versa (Ray, 1960; Atkinson, 1994, 1996; Sibly

and Atkinson, 1994; Partridge and French, 1996). At least under controlled

laboratory conditions, this relationship holds almost universally (Atkinson,

1994).

Apart from this environmentally induced phenotypic plasticity, temperature

can have evolutionary effects on body size. Latitudinal and altitudinal clines in

body size with an established genetic basis have been reported for several

animals (e.g. Bryant, 1977; Berven, 1982; Imasheva et al., 1994; James et al.,

1995, 1997; Partridge and French, 1996; Chown and Gaston, 1999; Billerbeck

et al., 2000), with smaller individuals being found in populations at lower

latitudes or altitudes. The frequent recurrence of this pattern suggests that size

clines result from natural selection (McCabe and Partridge, 1997). Although

many ecological variables might be involved as selective agents, direct evidence

for the particular importance of temperature was gained from laboratory ex-

periments. Replicated Drosophila populations kept in long-term culture at

different temperatures evolved to be larger at lower temperatures (Partridge

et al., 1994, 1995), and recent studies suggest that body size itself can be a

target of thermal selection (McCabe and Partridge, 1997; Reeve et al., 2000).

In recent years, there has been considerable theoretical interest in the

physiological and evolutionary mechanisms underlying the temperature-size-

rule (e.g. Atkinson, 1994, 1996; Berrigan and Charnov, 1994; Sibly and

Atkinson, 1994; Partridge and French, 1996; Van der Have and De Jong, 1996;

Van Voorhies, 1996; Chown and Gaston, 1999). However, a satisfactory

general explanation is still lacking (Partridge and French, 1996; Chown and

Gaston, 1999) and hypotheses remain contested (cf. Van Voorhies, 1996;

Mousseau, 1997; Partridge and Coyne, 1997; Arnett and Gotelli, 1999). It

remains even unclear whether the similarity of developmental (phenotypic

plasticity) and evolutionary responses of body size to temperature arises from

the same selective pressures or mechanistic constraints (Atkinson, 1996).

Assuming a common physiological process reducing size at higher temper-

atures, but at the same time acknowledging the evidence for temperature acting

as a selective agent on body size (see above), the study of exceptions and

deviations from the broad rule should prove to be particularly useful to en-

hance our understanding on how selection acts on body size. For example,

some insects show opposite size clines, having a larger body size closer to the

equator (e.g. Mousseau and Roff, 1989; Nylin and Svard, 1990; Mousseau,

334

1997). These seemingly contradictory cases can be explained as follows. In

seasonal breeders, there should be selection to allocate as much of the fa-

vourable season as possible to reproduction (Partridge and French, 1996). As

the length of growing season increases, selection should favour increased size at

maturity to maximise adult fitness. With season length further increasing,

however, selection for increased size should be relaxed in favour of the com-

pletion of an extra generation, leading to a ‘saw-tooth’ latitudinal size cline

(Roff, 1980, 1992; Mousseau and Roff, 1989). Thus, an interaction between

generation time and growing season length may account for the occurrence of

opposite size clines (Chown and Gaston, 1999).

In insects with relatively short generation times as compared to season

length, the law of ‘compound interest’ should apply (Cole, 1954; Lewontin,

1965). To maximise Darwinian fitness, there should be a premium on early

reproduction to increase the number of generations per year, even at the ex-

pense of being smaller. This is particularly likely to be important in multi-

voltine organisms in seasonal environments (Partridge and French, 1996). On

the other hand, if generation time comprises a major part of the total growing

season, as is generally the case in the species where larger individuals have been

found at lower latitudes (i.e. butterflies, moths, crickets; see Masaki, 1978;

Mousseau and Roff, 1989; Nylin and Svard, 1990; Gomi and Takeda, 1996),

selection for large body size is likely to be more intense. Finally, populations

with fixed generation time lack the demographic pressure to mature especially

early, since no individual is capable of fitting in additional generations (Meats,

1971). Consequently, selection for large size at maturity to maximise adult

fitness should be strong.

In this context, temperature can have a major influence through its effect on

development time (Honek and Kocourek, 1990) and hence on the number of

generations possible within a season. At high temperatures, indicating fa-

vourable growth conditions and potential for extra generations, multivoltine

populations (or species) with relatively short development times should gain

compound interest benefits from reproducing earlier at a smaller size. The

expected pattern of a reduction in final size as temperature increases agrees well

with the available empirical evidence (see above). For obligatorily monovoltine

populations, in contrast, early reproduction offers no compound interest

benefits regardless of temperature, whereas all advantages of large body size

should remain. Hence, one would predict no or only minor reductions in size to

occur with increasing temperatures.

The potential explanatory power of the compound interest hypothesis may

have been underestimated in recent reviews on relationships between temper-

ature and adult size (e.g. Berrigan and Charnov, 1994; Atkinson, 1996). Thus,

we set out here to test the particularly critical prediction of a low or absent

response to experimental temperatures in two obligatorily monovoltine

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populations of the butterfly Lycaena hippothoe. This may be the first explicit

test of predictions derived from the compound interest hypothesis (as recently

elaborated by Partridge and French, 1996; Chown and Gaston, 1999). The

resulting reaction norms will be compared to those previously described for

two potentially multivoltine Lycaena populations (L. hippothoe sumadiensis, L.

tityrus; Fischer and Fiedler, 2000, 2001), all of which are taxonomically closely

related and ecologically very similar with regard to habitat requirements and

larval host-plant. In these populations the more time-limited (earlier emerging)

males suffered substantial weight losses at increasing temperatures. Females

also responded to temperature, but much more weakly. Furthermore, we point

out differences between both monovoltine populations (originating from the

central Alps and western Germany) which may represent local adaptations.

Material and methods

Study organism

Lycaena hippothoe (Linnaeus 1761) is a widespread temperate-zone butterfly,

ranging from northern Spain in the west throughout much of the northern

Palaearctic region eastwards to the easternmost parts of Siberia and China

(Ebert and Rennwald, 1991; Tuzov, 2000). Throughout its vast range adults fly

in one generation, except for the western Hungarian lowland population,

which is bivoltine (Fazekas and Balasz, 1979; Tolman and Lewington, 1998;

Tuzov, 2000). Larvae (of the last brood) enter diapause overwintering half-

grown, usually in the third instar (Fischer and Fiedler, 2002). The principal

larval host-plant is Rumex acetosa L. (Polygonaceae), a common and wide-

spread perennial herb occurring in various types of grassland. The two pop-

ulations considered in the experiments reported here include the nominate form

L. hippothoe hippothoe from western Germany (Westerwald, 580 m a.s.l.) and

the alpine subspecies L. hippothoe eurydame (Hoffmansegg 1806) from the

central Alps (Senales valley, 1800 m a.s.l.).

Experimental arrangement

Eight and ten freshly emerged females were caught in 1998 in the western

German and alpine population, respectively. For oviposition females were

transferred to Bayreuth University and maintained in an environmental cabi-

net at a constant temperature (25 �C) and long-day conditions (24-h L/D cycle,

L18:D6 throughout). They were placed individually in glass jars (1 l, approx-

imately 10 cm in diameter and 13 cm in height) lined with moistened filter

paper and the jars covered with gauze. Each jar contained a bunch of the larval

336

food-plant R. acetosa (in H2O) as oviposition substrate as well as highly

concentrated sucrose solution for adult feeding. Eggs were removed each day,

pooled (within populations), and maintained in lots of about 100 in glass vials

at a temperature of 20 �C (L18:D6).

After hatching, young larvae were randomly divided among four groups and

exposed to constant temperatures of 15, 20, 25, and 30 �C (photoperiod

L18:D6 throughout). Hatchlings were reared singly in transparent plastic boxes

(125 ml) containing moistened filter paper and fresh cuttings of R. acetosa in

ample supply. The boxes were checked daily and supplied with new food when

needed. In order to even out minor temperature differences within cabinets, the

boxes were shifted around daily. Following the onset of diapause, dormant

larvae were transferred to another cabinet (T 4 �C, photoperiod L8:D16) for

hibernation. After a diapause of about 5–6 months, larvae were again assigned

to the four different rearing temperatures, and reared in the way outlined above

until adult eclosion. For each individual we measured weight (to the nearest

0.1 mg) at the end of diapause (subsample only), larval (post-diapause) de-

velopment time, pupal time, pupal and adult weight, growth rate. Pupae were

weighed on the day following pupation, adults on the day of eclosion after

having excreted meconium. Relative growth rate was calculated according to

Gotthard et al. (1994) as mean weight gain per day: Growth rate = {[ln(pupal

weight) � ln(diapause weight)]/larval time} · 100.

Statistical methods

Within each population, standard two-way ANOVAs were applied to analyse

the effects of temperature and sex on life-history traits. For a subsequent

comparison between both populations we used three-way ANOVAs (factors:

population, temperature, sex). Differences between groups of larvae, pupae or

butterflies were localised using Tukey’s post-hoc comparison (Spjøtvoll–Stoline

variant; significance threshold p < 0.05 throughout). All statistical analyses

were performed using StatSoft (1999). Throughout the text all means are given

±1 SD.

Results

Developmental pathways

As was expected for these monovoltine populations, the vast majority of larvae

entered diapause even under favourable laboratory (and long-day) conditions.

At lower temperatures of 15 and 20 �C this applied to all larvae in both

populations (sample sizes for western German population 96 and 90, for alpine

337

90 and 219 larvae, respectively). At higher temperatures, however, some indi-

viduals chose a direct development. The percentages of direct developers

reached 3.1 at 25 �C (n ¼ 355) and 31.5% at 30 �C (n ¼ 111) in the western

German population, and 5.0 (n ¼ 298) and 17.4% (n ¼ 98) in the alpine one.

Thus, a notable fraction of subitaneous development did occur under a high

temperature of 30 �C only. Directly developing individuals were excluded from

all subsequent analyses.

Reaction norms for age and size at maturity in western German L. h. hippothoe

Post-diapause development time strongly depended on temperature (Table 1;

for statistics see Table 2) and increased more than fourfold from 16 days

(30 �C) to about 66 days (15 �C). This was due to a longer duration of both the

larval and pupal stage at lower temperatures corresponding to lower devel-

opmental rates. Increasing temperature did not affect pupal weight, but caused

a significant reduction in adult weight (by 13.0% in males and by 13.6% in

females over the temperature gradient). The latter was due to higher weights at

15 �C in both sexes, whereas Tukey’s post-hoc test failed to reveal significant

differences in the range from 20 to 30 �C (Figure 1).

All traits differed significantly between sexes (Table 2). Males exhibited

shorter larval and concomitantly total development times than females. Thus,

protandry (earlier emergence of males; cf. Wiklund and Fagerstrom, 1977;

Fagerstrom and Wiklund, 1982; Zonneveld and Metz, 1991) persisted at all

temperatures. This was at least partially caused by invariably higher larval

growth rates of males. Throughout, females gained considerably higher pupal

and adult weights than males. Overall, however, both sexes responded in the

same manner to increasing temperatures. Consequently, the male–female ratio

of adult weight, ranging between 83.8 and 87.3%, remained similar throughout,

leading to parallel reaction norms for age and size at maturity in both sexes.

Reaction norms for age and size at maturity in alpine L. h. eurydame

The data on post-diapause development in the alpine population revealed

patterns very similar to those reported for the western German one. Again

growth rate, larval, pupal and concomitantly total development time depended

strongly on temperature (Table 1; for statistics see Table 3), with lower tem-

peratures causing lower growth rates and longer development times. As in the

former population, temperature did not significantly affect pupal weight, but

caused a slight reduction in adult weight (by 10.6% in males and by 9.3% in

females between 15 and 30 �C). However, in the post-hoc comparison no

significant differences among temperatures in either of both sexes occurred

(Figure 2).

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As in western German animals, protandry persisted at all temperatures and

was achieved by invariably higher growth rates and shorter development times

in males as compared to females. In contrast to the western German popula-

tion, sex-specific differences in pupal weight did not occur in the alpine pop-

ulation. Females reached, nevertheless, higher adult weights than males

(Fig. 2b; obviously due to a higher weight loss at metamorphosis in males), and

sexual size dimorphism was confined to this stage. However, with regard to

body weight sexes did not respond differently to increasing temperatures.

Table 1. Life-history data (mean ± 1 SD) for post-diapause development of L. h. hippothoe and

L. h. eurydame at different temperatures

T (�C) Trait L. h. hippothoe L. h. eurydame

Males Females Males Females

15 (n = 35) (n = 25) (n = 31) (n = 32)

Larval time (d) 37.9 ± 7.0 42.5 ± 3.8 35.2 ± 4.8 38.3 ± 4.3

Pupal time (d) 26.1 ± 2.3 26.9 ± 3.0 24.1 ± 2.3 23.5 ± 2.8

Larval + pupal time (d) 64.0 ± 8.1 69.4 ± 4.4 59.3 ± 4.7 61.8 ± 5.5

Pupal weight (mg) 168.0 ± 20.8 194.8 ± 21.6 180.8 ± 21.6 183.4 ± 17.9

Adult weight (mg) 74.7 ± 11.8 88.7 ± 11.3 73.7 ± 6.9 82.2 ± 10.7

Growth rate (%/d) 8.8 ± 0.9 (21) 8.1 ± 0.8 (20) 9.3 ± 1.2 (17) 8.8 ± 0.9 (27)

20 (n = 32) (n = 34) (n = 28) (n = 43)

Larval time (d) 19.1 ± 1.3 21.0 ± 1.9 16.4 ± 3.3 20.5 ± 3.5

Pupal time (d) 12.7 ± 0.8 13.1 ± 0.8 10.9 ± 0.9 11.7 ± 1.2

Larval + pupal time (d) 31.8 ± 1.7 34.1 ± 1.9 27.3 ± 3.6 32.1 ± 3.9

Pupal weight (mg) 174.0 ± 13.8 184.0 ± 14.9 179.1 ± 19.1 178.1 ± 20.2

Adult weight (mg) 70.2 ± 7.7 80.4 ± 10.0 68.4 ± 11.3 77.5 ± 9.9

Growth rate (%/d) 18.0 ± 1.6 (31) 16.6 ± 1.2 (33) 19.2 ± 2.0 (19) 16.3 ± 2.5 (36)

25 (n = 30) (n = 48) (n = 26) (n = 40)

Larval time (d) 13.5 ± 1.3 14.9 ± 1.5 12.2 ± 0.8 13.1 ± 1.5

Pupal time (d) 8.0 ± 0.4 8.0 ± 0.6 7.3 ± 0.5 7.6 ± 0.5

Larval + pupal time (d) 21.5 ± 1.4 22.8 ± 1.4 19.5 ± 0.9 20.7 ± 1.6

Pupal weight (mg) 171.9 ± 20.7 183.3 ± 20.0 178.6 ± 12.6 187.1 ± 18.9

Adult weight (mg) 66.6 ± 8.1 79.5 ± 8.8 70.4 ± 9.3 81.2 ± 12.7

Growth rate (%/d) 24.8 ± 2.3 (21) 23.0 ± 2.4 (43) 27.8 ± 2.6 (9) 25.9 ± 2.1 (17)

30 (n = 38) (n = 29) (n = 32) (n = 44)

Larval time (d) 9.5 ± 0.9 10.6 ± 1.1 8.8 ± 1.1 9.6 ± 1.0

Pupal time (d) 6.2 ± 0.4 6.4 ± 0.5 6.0 ± 0.3 6.1 ± 0.4

Larval + pupal time (d) 15.7 ± 0.9 17.0 ± 1.3 14.8 ± 0.9 15.7 ± 1.0

Pupal weight (mg) 169.0 ± 17.1 180.2 ± 17.1 175.0 ± 24.9 177.6 ± 22.1

Adult weight (mg) 65.0 ± 9.8 76.6 ± 9.1 65.9 ± 15.1 74.6 ± 10.3

Growth rate (%/d) 33.8 ± 3.4 (24) 32.1 ± 4.0 (23) 36.5 ± 4.4 (10) 34.2 ± 3.7 (24)

Sample sizes differing from those given in headings are reported in parentheses.

339

Hence, male–female ratio of adult weight remained similar regardless of tem-

perature (ranging between 86.7 and 89.7%), again resulting in parallel reaction

norms for males and females.

Population-specific differences in life-history traits

Apart from the effects of temperature and sex analysed above, alpine animals

exhibited shorter larval (three-way ANOVAs for population effects: F1,531 ¼51.8, p < 0.0001), pupal (F1,531 ¼ 116.2, p < 0.0001) and concomitantly total

post-diapause development times (F1,531 ¼ 116.0, p < 0.0001) throughout

than mid-elevation western German ones (Table 1). The shorter development

times correspond with higher larval growth rates in the alpine population

(except for females at 20 �C; F1,359 ¼ 38.3, p < 0.0001). In spite of the shorter

development times, neither pupal (F1,529 ¼ 1.2, p ¼ 0.28) nor adult weight

(F1,524 ¼ 1.2, p ¼ 0.30) differed significantly between both populations. Thus,

the faster development of alpine animals was not achieved at the cost of a

reduction in final weight. Likewise, weight at the end of diapause did not vary

considerably between populations (and sexes), the values being 6.0 ± 1.1 mg

(n ¼ 98) and 6.1 ± 1.0 mg (n ¼ 119) for western German males and females,

and 6.3 ± 0.9 mg (n ¼ 55) and 6.2 ± 0.9 mg (n ¼ 105) for alpine males and

females (two-way ANOVA for effects of population and sex on diapause

Table 2. Two-way ANOVAs for effects of temperature and sex on life-history traits in

L. h. hippothoe

Trait Source n df F p

Larval time (d) Temperature 271 3 263 1205.8 <0.0001

Sex 271 1 263 36.9 <0.0001

Temperature · sex 271 3 263 4.3 0.0059

Pupal time (d) Temperature 271 3 263 2824.6 <0.0001

Sex 271 1 263 4.5 0.0346

Temperature · sex 271 3 263 1.1 0.37

Larval + pupal time (d) Temperature 271 3 263 2606.2 <0.0001

Sex 271 1 263 37.5 <0.0001

Temperature · sex 271 3 263 4.7 0.0032

Pupal weight (mg) Temperature 270 3 262 1.5 0.23

Sex 270 1 262 42.5 <0.0001

Temperature · sex 270 3 262 2.8 0.0386

Adult weight (mg) Temperature 269 3 261 14.8 <0.0001

Sex 269 1 261 104.3 <0.0001

Temperature · sex 269 3 261 0.5 0.71

Growth rate (%/d) Temperature 216 3 208 905.8 <0.0001

Sex 216 1 208 18.8 <0.0001

Temperature · sex 216 3 208 0.7 0.58

Significant p-values are printed in bold.

340

weight; population-effect F1,373 ¼ 5.6, p ¼ 0.02, all p-values in post-hoc com-

parison >0.25; sex-effect F1,373 < 0.01, p ¼ 0.95).

Discussion

Reaction norms for age and size at maturity

Even under favourable laboratory conditions, the alpine and western German

L. hippothoe populations followed an essentially monovoltine lifecycle. Only at

Figure 1. Pupal (a) and adult weight (b) of L. h. hippothoe in relation to temperature. Boxes within

sexes marked by the same letter do not differ significantly (Tukey’s post-hoc comparison after two-

way ANOVA).

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unrealistically high temperatures combined with long photoperiods a sub-

stantial fraction of subitaneous developers occurred. Our results revealed that

developmental temperature had in neither of these monovoltine populations a

significant effect on pupal weight. Adult weight, however, decreased with in-

creasing temperature, but the response was rather weak in both populations

(weight loss of about 13% in western German and 10% in alpine animals

between 15 and 30 �C). A post-hoc comparison (Tukey’s) failed to reveal

statistically significant weight differences between rearing temperatures, except

for the western German population, where males and females reared at 15 �Cwere heavier than those reared at all other temperatures. Although using a

fairly conservative test, these results nevertheless indicate that weight differ-

ences between individual temperature treatments were small, even though there

was a significant trend towards smaller adult weights with increasing temper-

ature over the whole range.

Note, however, that in some other studies exclusively pupal weight (or even

earlier stages) have been used, still showing in the vast majority of cases a

significant reduction in size (cf. Atkinson, 1994). In contrast to these, our results

give only weak support for the temperature-size-rule, and they clearly differ

from those previously reported for taxonomically and ecologically closely re-

lated Lycaena populations, i.e. a western Hungarian lowland population of L.

hippothoe (L. h. sumadiensis; Fischer and Fiedler, 2001) and alpine L. tityrus

Table 3. Two-way ANOVAs for effects of temperature and sex on life-history traits in

L. h. eurydame

Trait Source n df F p

Larval time (d) Temperature 276 3 268 1183.2 <0.0001

Sex 276 1 268 39.9 <0.0001

Temperature · sex 276 3 268 5.3 0.0014

Pupal time (d) Temperature 276 3 268 2215.9 <0.0001

Sex 276 1 268 0.6 0.44

Temperature · sex 276 3 268 2.8 0.0428

Larval + pupal time (d) Temperature 276 3 268 2600.8 <0.0001

Sex 276 1 268 35.8 <0.0001

Temperature · sex 276 3 268 5.1 0.0020

Pupal weight (mg) Temperature 275 3 267 1.7 0.18

Sex 275 1 267 1.7 0.19

Temperature · sex 275 3 267 0.6 0.59

Adult weight (mg) Temperature 271 3 263 6.6 0.0003

Sex 271 1 263 48.6 <0.0001

Temperature · sex 271 3 263 0.2 0.93

Growth rate (%/d) Temperature 159 3 151 798.7 <0.0001

Sex 159 1 151 21.8 <0.0001

Temperature · sex 159 3 151 2.1 0.11

Significant p-values are printed in bold.

342

(Fischer and Fiedler, 2000; see below). The latter two populations were found to

be potentially multivoltine under favourable laboratory conditions. In nature,

L. h. sumadiensis appears to be bivoltine (Fazekas and Balasz, 1979; Tolman

and Lewington, 1998). The alpine L. tityrus population is monovoltine due to

the short vegetation period in the higher altitudes of the Alps, but L. tityrus

populations next (only a few km) to the one considered here are known to be

bivoltine (Scheuringer, 1972) and gene flow is likely to occur (cf. Descimon,

1980). Both populations are hereafter referred to as oligovoltine ones.

In contrast to the monovoltine populations, an increase in temperature

caused significant reductions already in pupal as well as adult weight in directly

Figure 2. Pupal (a) and adult weight (b) of L. h. eurydame in relation to temperature. Boxes within

sexes marked by the same letter do not differ significantly (Tukey’s post-hoc comparison after two-

way ANOVA).

343

developing individuals of both oligovoltine populations (Fischer and Fiedler,

2000, 2001). In the latter, loss in adult weight between the highest and lowest

value amounted to 38.4 and 16.7% for male and female L. tityrus, and to 23.0

and 11.8% in male and female L. h. sumadiensis, respectively. The, overall,

weaker response of the monovoltine populations to increasing temperature

supports our predictions derived from the compound interest hypothesis (cf.

Meats, 1971; Partridge and French, 1996; Chown and Gaston, 1999). Mono-

voltine populations, not able to gain compound interest benefits from maturing

earlier at higher temperatures (indicating potential for extra generations), fa-

voured large size to maximise adult fitness throughout, and achieved, overall,

considerably higher weights than the oligovoltine ones (Fischer and Fiedler,

2002).

Another intriguing difference between oligo- and mono-voltine populations

is that in the former sexes showed divergent reaction norms for age and size at

maturity in response to temperature, whereas in the latter sexes responded in

the same manner to increasing temperatures. At low temperatures, males and

females of the oligovoltine populations achieved similar weights despite the

males’ shorter development time. At high temperatures, however, protandrous

males were forced into a trade-off in which they favoured early emergence over

large size, leading to a distinct weight loss. Female weight, however, was less

affected. Thus, with a rise of temperature males fell increasingly behind females

(Fischer and Fiedler, 2000, 2001). Such sex-related reaction norms were pre-

dicted from sexual selection theory, assuming a selective premium on rapid

development (protandry) for males, and on large body size (fecundity advan-

tage) in females (e.g. Fagerstrom and Wiklund, 1982; Bulmer, 1983; Roff, 1992;

Honek, 1993; Garcıa-Barros, 2000).

The occurrence of such sex-related differences, however, does complicate the

present comparison. Clearly, males of the oligovoltine populations suffered a

higher relative loss in adult weight than those of the monovoltine populations.

For females, however, adult weight loss at increasing temperatures was roughly

the same in both types of populations. We tentatively assume this to be a

consequence of the ambiguous status of these ‘oligovoltine’ populations, where

presumably fecundity selection for large body size in females is still intense,

whereas in males there is a selective premium on protandry (see above). The

potential benefits of larger female size, however, should be much lower in truly

multivoltine populations, where it should pay off to speed up development in

favour of additional generations. Such reaction norms with no or only minor

differences between sexes were generally found in various species and popu-

lations of Drosophila (e.g. David et al., 1994; McCabe and Partridge, 1997) as

well as in other insect species (for review see Atkinson, 1994).

To sum up, mono- and oligo-voltine populations showed different responses

to temperature. The mechanisms underlying these differential responses,

344

however, remain to be uncovered. Reduction in adult size at higher tempera-

tures may either be a consequence of maturing earlier in multi- and oligo-

voltine populations to augment the chance for realisation of an additional

generation (Partridge and French, 1996; Chown and Gaston, 1999). Alterna-

tively, given a common physiological constraint reducing size at higher tem-

peratures (e.g. Atkinson, 1994, 1996; Van der Have and De Jong, 1996;

Ernsting and Isaaks, 1997), there may be selection against weight reduction in

monovoltine populations to maximise adult fitness (cf. Mousseau and Roff,

1989; Roff, 1992). Both explanations would be compatible with the compound

interest hypothesis.

The striking parallelism of reaction norms across species boundaries

(L. tityrus and L. h. sumadiensis) and the pronounced variation between dif-

ferent populations of L. hippothoe clearly speak in favour of an ecological

rather than a phylogenetic explanation. Since we have found sex-specific re-

action norms in directly developing populations facing different environments

(i.e. Alps, lowland western Hungary; see also Leimar, 1996), these should not

be attributed to specific environmental conditions, but may be more wide-

spread in species living under time constraints (and where one sex is more time-

constrained than the other). The complete absence of genotype–environment

interactions between sex and temperature in monovoltine L. hippothoe popu-

lations, which should be less time-constrained than populations trying to

realise a second generation per season, emphasise the notion outlined by Nylin

and Gotthard (1998) that clear trade-offs can be expected in stressful situations

only. Without such time constraints, weight loss should be largely avoided due

to plastic growth, as was found in a number of other temperate-zone butterflies

(e.g. Nylin et al., 1989, 1993; Wiklund et al., 1991; Nylin, 1992; Gotthard

et al., 1994, 1999).

Population-specific differences in life-history traits

At all temperatures, the alpine population exhibited shorter post-diapause

development times than the western German one. Both larval and pupal stage

contributed to this developmental advantage due to higher developmental

rates. As these results are based on experiments under common environment

conditions, they do reflect inherent (i.e. genetic, possibly combined with ma-

ternal) differences between both populations, which may represent local adap-

tations to regional climates (Ayres and Scriber, 1994; Mopper and Strauss,

1998), with selection favouring high growth rates in the alpine environment

with a short growing season.

The shorter development time in the alpine population did not result in a

reduced final size, as is obvious from equal pupal and adult weights in both

populations. Hence, weight loss was avoided due to plastic growth (higher

345

growth rates), and consequently the basic trade-off between development time

and size frequently assumed in life-history theory (e.g. Roff, 1992; Stearns,

1992) did not occur. These results agree with earlier studies on butterflies which

revealed an unexpectedly high degree of plasticity in growth and development

(e.g. Nylin et al., 1989, 1996; Nylin, 1992, 1994; Gotthard et al., 1999), and

stress the importance to consider the triangular nature of relationships between

size, development time and growth rate (see Nylin, 1994; Abrams et al., 1996;

Nylin and Gotthard, 1998).

Acknowledgements

We greatly acknowledge valuable comments by D. Atkinson, W. Blancken-

horn, O. Leimar, and W. Weisser that helped to improve the quality of this

paper. Thanks are due to K. Kaminsky, C. Ruf, and A. Servant for help with

butterfly rearing. This study was supported by grants from the Friedrich-Ebert-

Foundation to K. Fischer.

References

Abrams, P.A., Leimar, O., Nylin, S. and Wiklund, C. (1996) The effect of flexible growth rates on

optimal sizes and development times in a seasonal environment. Am. Nat. 147, 381–395.

Arnett, A.E. and Gotelli, N.J. (1999) Geographic variation in life-history traits of the ant lion,

Myrmeleon immaculatus: evolutionary implications of Bergmann’s rule. Evolution 53, 1180–1188.

Atkinson, D. (1994) Temperature and organism size – a biological law for ectotherms? Adv. Ecol.

Res. 25, 1–58.

Atkinson, D. (1996) Ectotherm life-history responses to developmental temperature. In I.A.

Johnston and A.F. Bennett (eds) Animals and Temperature: Phenotypic and Evolutionary Ad-

aptation, Cambridge University Press Cambridge, pp. 183–204.

Ayres, M.P. and Scriber, J.M. (1994) Local adaptation to regional climates in Papilio canadensis

(Lepidoptera: Papilionidae). Ecol. Monogr. 64, 465–482.

Berrigan, D. and Charnov, E.L. (1994) Reaction norms for age and size at maturity in response to

temperature: a puzzle for life historians. Oikos 70, 474–478.

Berven, K.A. (1982) The genetic basis of altitudinal variation in the wood frog Rana sylvatica. I. An

experimental analysis of life history traits. Evolution 36, 962–983.

Billerbeck, J.M., Schultz, E.T. and Conover, D.O. (2000) Adaptive variation in energy acquisition

and allocation among latitudinal populations of the Atlantic silverside. Oecologia 122, 210–219.

Blanckenhorn, W.U. (2000) The evolution of body size: what keeps organisms small? Quart. Rev.

Biol. 75, 385–407.

Bryant, E.H. (1977) Morphological adaptation of the housefly, Musca domesticus L. Evolution 31,

598–610.

Bulmer, M.G. (1983) Models for the evolution of protandry in insects. Theor. Popul. Biol. 23, 314–

322.

Calder, W.A. (1984) Size, Function and Life History. Harvard University Press, Harvard.

Chown, S.L. and Gaston, K.J. (1999) Exploring links between physiology and ecology at macro-

scales: the role of respiratory metabolism in insects. Biol. Rev. Camb. Philos. Soc. 74, 87–120.

346

Cole, L.C. (1954) The population consequences of life history phenomena. Quart. Rev. Biol. 29,

103–137.

David, J.R., Moreteau, B., Gauthier, J.P., Petavy, G., Stockel, A. and Imasheva, A.G. (1994)

Reaction norms of size characters in relation to growth temperature in Drosophila melanogaster –

an isofemale lines analysis. Genet. Sel. Evol. 26, 229–251.

Descimon, H. (1980) Heodes tityrus tityrus Poda et H. tityrus subalpina Speyer (Lycaenidae): un

probleme de speciation en milieu alpin. Nota Lepid. 2,123–125.

Ebert, G. and Rennwald, E. (1991) Die Schmetterlinge Baden-Wurttembergs. Vol. 2. Ulmer,

Stuttgart.

Ernsting, G. and Isaaks, A. (1997) Effects of temperature and season on egg size, hatchling size and

adult size in Notiophilus biguttatus. Ecol. Entomol. 22, 32–40.

Fagerstrom, T. and Wiklund, C. (1982) Why do males emerge before females? Protandry as a

mating strategy in male and female butterflies. Oecologia 52, 164–166.

Fazekas, I. and Balazs, T. (1979) Taxonomische, okologische und faunistische Uberprufung des

Palaeochrysophanus hippothoe sumadiensis Szabo 1956 (Lep.: Lycaenidae). Ent. Zeit. 89, 230–

236.

Fischer, K. and Fiedler, K. (2000) Sex-related differences in reaction norms in the butterfly Lycaena

tityrus (Lepidoptera: Lycaenidae). Oikos 90, 372–380.

Fischer, K. and Fiedler, K. (2001) Dimorphic growth patterns and sex-specific reactions norms in

the butterfly Lycaena hippothoe sumadiensis. J. Evol. Biol. 14, 210–218.

Fischer, K. and Fiedler, K. (2002) Life-history plasticity in the butterfly Lycaena hippothoe: local

adaptations and trade-offs. Biol. J. Linn. Soc. 75, 173–185.

Garcıa-Barros, E. (2000) Body size, egg size, and their interspecific relationships with ecological

and life history traits in butterflies (Lepidoptera: Papilionidea, Hesperioidea). Biol. J. Linn. Soc.

70, 251–284.

Gomi, T. and Takeda, M. (1996) Changes in life-history traits in the Fall Webworm within half a

century of introduction to Japan. Funct. Ecol. 10, 384–389.

Gotthard, K., Nylin, S. and Wiklund, C. (1994) Adaptive variation in growth rate: life history costs

and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99, 281–289.

Gotthard, K., Nylin, S. and Wiklund, C. (1999) Seasonal plasticity in two satyrine butterflies: state-

dependent decision making in relation to daylength. Oikos 84, 453–462.

Honek, A. (1993) Intraspecific variation in body size and fecundity in insects: a general relation-

ship. Oikos 66, 483–492.

Honek, A. and Kocourek, F. (1990) Temperature and development time in insects: a general

relationship between thermal constraints. Zool. Jb. Syst. 117, 401–439.

Imasheva, A.G., Bubli, O.A. and Lazebny, O.E. (1994) Variation in wing length in Eurasian

natural populations of Drosophila melanogaster. Heredity 72, 508–514.

James, A.C., Azevedo, R.B.R. and Partridge, L. (1995) Cellular basis and development timing in a

size cline of Drosophila melanogaster. Genetics 140, 659–666.

James, A.C., Azevedo, R.B.R. and Partridge, L. (1997) Genetic and environmental responses to

temperature of Drosophila melanogaster from a latitudinal cline. Genetics 146, 881–890.

Leimar, O. (1996) Life history plasticity: influence of photoperiod on growth and development in

the common blue butterfly. Oikos 76, 228–234.

Lewontin, R.C. (1965) Selection for colonizing ability. In H.G. Baker and G.L. Stebbins, (eds) The

Genetics of Colonizing Species. Academic Press, London, pp. 77–94.

Masaki, S. (1978) Climatic adaptation and species status in the lawn ground cricket. II. Body size.

Oecologia 35, 343–356.

McCabe, J. and Partridge, L. (1997) An interaction between environmental temperature and ge-

netic variation for body size for the fitness of adult female Drosophila melanogaster. Evolution 51,

1164–1174.

Meats, A. (1971) The relative importance to population increase of mortality, fecundity and the

time variables of the reproductive schedule. Oecologia 6, 223–237.

Mopper, S. and Strauss, S.Y. (1998) Genetic Structure and Local Adaptation in Natural Insect

Populations: Effects of Ecology, Life History, and Behavior. Chapman & Hall, London.

347

Mousseau, T.A. (1997) Ectotherms follow the converse to Bergmann’s rule. Evolution 51, 630–632.

Mousseau, T.A. and Roff, D.A. (1989) Adaptation to seasonality in a cricket: patterns of phe-

notypic and genotypic variation in body size and diapause expression along a cline in season

length. Evolution 43, 1483–1496.

Nylin, S. (1992) Seasonal plasticity in life history traits: growth and development in Polygonia c-

album (Lepidoptera: Nymphalidae). Biol. J. Linn. Soc. 47, 301–323.

Nylin, S. (1994) Seasonal plasticity and life-cycle adaptations in butterflies. In: H.V. Danks (ed.)

Insect Life-Cycle Polymorphism. Kluwer, Dordrecht, pp. 41–67.

Nylin, S. and Gotthard, K. (1998) Plasticity in life-history traits. Annu. Rev. Entomol. 43, 63–83.

Nylin, S. and Svard, L. (1990) Latitudinal patterns in the size of European butterflies. Holarct.

Ecol. 14, 192–202.

Nylin, S., Wickman, P.-O. and Wiklund, C. (1989) Seasonal plasticity in growth and development

of the speckled wood butterfly, Pararge aegeria. Biol. J. Linn. Soc. 38, 155–171.

Nylin, S., Wiklund, C., Wickman, P.-O. and Garcia-Barros, E. (1993) Absence of trade-offs be-

tween sexual size dimorphism and early male emergence in a butterfly. Ecology 74, 1414–1427.

Nylin, S., Gotthard, K. and Wiklund, C. (1996) Reaction norms for age and size at maturity in

Lasiommata butterflies: Predictions and tests. Evolution 50, 1351–1358.

Partridge, L. and Coyne, J.A. (1997) Bergmann’s rule in ectotherms: is it adaptive? Evolution 51,

632–635.

Partridge, L. and Fowler, K. (1993) Direct and correlated responses to selection on thorax length in

Drosophila melanogaster. Evolution 47, 213–226.

Partridge, L. and French, V. (1996) Thermal evolution of ectotherm body size: why get big in the

cold? In I.A. Johnston, and A.F. Bennett (eds) Animals and Temperature: Phenotypic and Evo-

lutionary Adaptation. Cambridge University Press, Cambridge, pp. 265–292.

Partridge, L., Barrie, B., Fowler, K. and French, V. (1994) Evolution and development of body size

and cell size in Drosophila melanogaster in response to temperature. Evolution 48, 1269–1276.

Partridge, L., Barrie, B., Barton, N.H., Fowler, K. and French, V. (1995) Rapid laboratory evo-

lution of adult life history traits in Drosophila melanogaster in response to temperature. Evolution

49, 538–544.

Peters, R.H. (1983) The Ecological Implications of Body Size. Cambridge University Press, Cam-

bridge.

Ray, C. (1960) The application of Bergmann’s and Allen’s rules to the poikilotherms. J. Morph.

106, 85–108.

Reeve, M.W., Fowler, K. and Partridge, L. (2000) Increased body size confers greater fitness at

lower experimental temperature in male Drosophila melanogaster. J. Evol. Biol. 13, 836–844.

Roff, D.A. (1980) Optimizing development time in a seasonal environment: the ‘ups and downs’ of

clinal variation. Oecologia 45, 202–208.

Roff, D.A. (1992) The Evolution of Life Histories: Theory and Analysis. Chapman & Hall, London.

Scheuringer, E. (1972) Die Macrolepidopteren-Fauna des Schnalstales. Studi Trentini di Scienze

Naturali 49, 229–448.

Schmidt-Nielsen, K. (1984) Scaling: Why is Animal Size so Important? Cambridge University Press,

Cambridge.

Sibly, R.M. and Atkinson, D. (1994) How rearing temperature affects optimal adult size in ecto-

therms. Funct. Ecol. 8, 486–493.

StatSoft (1999) Statistica 5.5 for Windows. StatSoft, Tulsa.

Stearns, S.C. (1992) The Evolution of Life Histories. Oxford University Press, Oxford.

Tolman, T. and Lewington, R. (1998) Die Tagfalter Europas und Nordwestafrikas. Franckh-Kos-

mos, Stuttgart.

Tuzov, V.K. (2000) Guide to the Butterflies of Russia and Adjacent Territories. Vol. 2. PenSoft

Publishers, Moscow.

Van der Have, T.M. and De Jong, G. (1996) Adult size in ectotherms: temperature effects on

growth and differentiation. J. Theor. Biol. 183, 329–340.

Van Voorhies, W.A. (1996) Bergmann size clines: a simple explanation for their occurrence in

ectotherms. Evolution 50, 1259–1264.

348

Wiklund, C. and Fagerstrom, T. (1977) Why does males emerge before females? A hypothesis to

explain the incidence of protandry in butterflies. Oecologia 31, 153–158.

Wiklund, C., Nylin, S. and Forsberg, J. (1991) Sex-related variation in growth rate as a result of

selection for large size and protandry in a bivoltine butterfly, Pieris napi. Oikos 60, 241–250.

Zonneveld, C. and Metz, J.A.J. (1991) Models on butterfly protandry: Virgin females are at risk to

die. Theor. Popul. Biol. 40, 308–321.

349