Post on 15-Jul-2016
Research article
Physiological costs of growing fast: does accelerated
growth reduce pay-off in adult fitness?
KLAUS FISCHER1,*, ILJA ZEILSTRA1, STEFAN K HETZ2
and KONRAD FIEDLER1
1Department of Animal Ecology I, University of Bayreuth, D-95440 Bayreuth, Germany;2Department of Animal Physiology, Humboldt University, D-10115 Berlin, Germany
(*author for correspondence, tel.: +49-921-553079; fax: +49-921-552784;
e-mail: klaus.fischer@uni-bayreuth.de)
Received 24 March 2004; accepted 9 August 2004
Co-ordinating editor: Leimer
Abstract. Accumulating evidence suggests that, in contrast to earlier assumptions, juvenile growth
rates are optimised by means of natural and sexual selection rather than maximised to be as fast as
possible. Owing to the generally accepted advantage of growing fast to adulthood, such adaptive
variation strongly implies the existence of costs attached to rapid growth. By using four popula-
tions of protandrous copper butterflies with known differences in intrinsic growth rates within and
across populations, we investigate a potential trade-off between rapid growth and the propor-
tionate weight loss at metamorphosis. While controlling for effects of pupal time and mass, we
demonstrate that (1) protandrous males, exhibiting higher growth rates, suffer a higher weight loss
than females throughout, that (2) population differences in weight loss generally follow known
differences in growth rates, and that (3) males have by 6% higher metabolic rates than females
during pupal development. These results support the notion that a higher weight loss during the
development to adulthood may comprise a physiological cost of rapid development, with the pay-
off of accelerated growth being reduced by a disproportionally smaller adult size.
Key words: growth rate, Lepidoptera, life-history trait, metabolic rate, trade-off
Introduction
An increasingly large body of evidence indicates that growth rate is a life-
history trait in its own right that may vary adaptively (Abrams et al., 1996;
Arendt, 1997, 2003; Nylin and Gotthard, 1998; Gotthard, 2000). Empirical
evidence for adaptive variation in growth rates was gained from studies on
insects, spiders, fish, molluscs, amphibians, reptiles, and mammals (see refer-
ences in Gotthard et al., 1994; Arendt, 1997). Traditionally, life-history theory
has explicitly or implicitly assumed that juvenile growth rates generally operate
near their physiological maximum, and that variation is attributable to
environmental variables such as temperature and food availability only
(e.g. Stearns and Koella, 1986; Roff, 1992; Stearns, 1992). However, growth
Evolutionary Ecology 18: 343–353, 2004.� 2004 Kluwer Academic Publishers. Printed in the Netherlands.
rates were frequently found to be optimised by natural selection rather than
maximised (e.g. Gotthard et al., 1994; Nylin et al., 1994, 1996; Abrams et al.,
1996; Lankford et al., 2001; Arendt, 2003). As the benefits of growing fast,
providing a higher chance of surviving to reproduction, is generally accepted
(Roff, 1992; Stearns, 1992), these findings strongly imply the existence of costs
attached to high growth rates.
There are basically two categories of such costs, ecological and physiological
ones. Potential ecological costs include a higher risk of predation due to a
higher foraging activity of fast growing individuals. This interrelation is well
supported by theoretical and empirical evidence (e.g. Lima and Dill, 1990;
Werner and Anholt, 1993; Gotthard, 2000; Lankford et al., 2001). In contrast,
the issue of potential physiological costs related to high growth rates has been
rarely addressed (Gotthard et al., 1994), a prominent exception being the
inverse relationship between growth rate and locomotor ability (e.g. Billerbeck
et al., 2001; Arendt, 2003). Some studies tested the hypothesis that high growth
rates should, based on overall higher metabolic rates, confer lower starvation
endurance, two of which revealed support for the prediction (Stockhoff, 1991;
Gotthard et al., 1994; but not Gotthard, 1998).
In many temperate-zone insects males typically exhibit shorter development
times and concomitantly increased growth rates than females due to selection
for protandry (e.g. Fagerstrom and Wiklund, 1982; Wiklund et al., 1991;
Zonneveld and Metz, 1991; Fischer and Fiedler, 2000a). Therefore, protan-
drous insects should provide useful modells to investigate potential costs
related to accelerated growth. Here, we address this issue by using four prot-
androus copper butterfly populations, one of Lycaena tityrus from Southern
Germany and three geographically isolated populations of Lycaena hippothoe
from Western Germany, the Central Alps, and Western Hungary. The latter
three show, in addition to sex-specific growth rates, variation across popula-
tions (Fischer and Fiedler 2001, 2002a, 2002b). When reared in a common
environment, the Hungarian population, being the only bivoltine one within
this principally monovoltine species (Tolman and Lewington, 1998), exhibits
considerably higher growth rates than the other two (by 8.7–59.1%, depending
on temperature; Fischer and Fiedler, 2002a). During post-diapause develop-
ment, the monovoltine alpine animals show about 7% higher growth rates than
their (also monovoltine) Western German con-specifics, presumably as an
adaptation to the short growing season in high altitude habitats (Fischer and
Fiedler, 2002b).
Those differences within and across populations enable us to investigate
potential physiological costs associated with increased growth rates. Propor-
tionate weight loss during metamorphosis may represent such a cost (Gotthard
et al., 1994; Fischer and Fiedler, 2000a), as animals need to spend time and
energy in achieving a high pupal mass. If, for fast growing individuals, this
344
investment is not proportionally reflected in adult size (generally believed to be
closely related to fitness; e.g. Peters, 1983; Honek, 1993), this is equivalent to a
relative reduction in the pay-off of accelerated growth.
Assuming that a faster development is less efficient than a slower one
(Gotthard et al., 1994; Arendt, 1997; Fischer and Fiedler, 2000a), we predict
differences in weight loss following the known differences in growth rates: (1)
As all populations exhibit protandry (Fischer and Fiedler, 2000a, 2001, 2002b),
males should suffer a higher proportionate weight loss than females through-
out. (2) Across the three L. hippothoe populations, the Hungarian one should
suffer the highest weight loss, followed by the alpine and finally the Western
German population. Finally, we explore a potential mechanistic source for
differences in proportionate weight loss. Based on the assumption of generally
elevated metabolic rates in fast growing individuals, we predict (3) a higher
mass-specific CO2 production in the pupal phase in fast growing males as
compared to females, potentially accounting for differences in weight loss.
Material and methods
Study organisms
L. tityrus (Poda, 1761) is a temperate-zone butterfly, ranging from Western
Europe to Central Asia. The species is bivoltine with two discrete generations
per year in most parts of its range (Tolman and Lewington, 1998). Larvae of
the last brood enter diapause, overwintering half-grown in the third instar. Ten
freshly emerged females were caught in July 2003 near Bayreuth (Northern
Bavaria, Germany; 400 m a.s.l.).
Lycaena hippothoe (Linnaeus, 1761) is also a temperate-zone butterfly, with a
range from Northern Spain in the west throughout much of the Northern
Palaearctic region to the easternmost parts of Siberia and China (Tuzov, 2000).
Adults fly in one generation throughout its vast range, except for the bivoltine
Western Hungarian population (Tolman and Lewington, 1998; Tuzov, 2000).
Larvae (of the last brood) enter diapause, overwintering half-grown (usually)
in the third instar (Fischer and Fiedler, 2002a). The three populations con-
sidered here include the nominate form L. hippothoe hippothoe from Western
Germany (Westerwald, 580 m a.s.l.), the alpine subspecies L. hippothoe eury-
dame (Hoffmannsegg, 1806) from the central Alps (Senales valley, 1800 m
a.s.l.), and the bivoltine subspecies L. hippothoe sumadiensis Szabo, 1956 from
Western Hungary (orseg, 200 m a.s.l.). Freshly emerged females (8, 10, and 9 of
L. h. hippothoe, eurydame, and sumadiensis, respectively) were caught in 1998
and 1999 in each of these populations.
345
Experimental arrangement
For oviposition captured females were transferred to Bayreuth University and
maintained in an environmental cabinet at a constant temperature (25–27 �C)and under long-day conditions (L18:D6). Females were placed individually in
glass jars (1 l) covered with gauze. Each jar contained leaves of the larval food-
plant Rumex acetosa as oviposition substrate as well as highly concentrated
sucrose solution for adult feeding. Eggs were removed daily, pooled (within
populations), and maintained in lots of about 100 in glass vials at a temper-
ature of 20 �C (L18:D6 throughout). After hatching, young L. hippothoe larvae
were randomly divided among four groups and exposed to constant temper-
atures of 15, 20, 25, and 30 �C, whereas all L. tityrus larvae were reared at
20 �C. 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 (L. h. hippothoe and eurydame)
larvae were transferred to another cabinet (T 4 �C, photoperiod L8:D16) for
hibernation. Note that under the given experimental arrangement, L. tityrus
and L. h. sumadiensis larvae generally developed directly into adults without
diapause, whereas the vast majority of L. h. hippothoe and eurydame larvae
entered diapause development (Fischer and Fiedler, 2002a). After a diapause of
about 5–6 months, these larvae were again assigned to the four different
rearing temperatures, and reared in the way outlined above until adult eclo-
sion. For all individuals, we measured development time, pupal and adult
mass. Pupae were weighed on the day following pupation, adults on the day of
eclosion after having excreted meconium. From these data, growth rates (mean
weight gain per day; Fischer and Fiedler, 2002a; 2002b) and proportionate
weight loss during metamorphosis ([1 ) (adult weight/pupal weight)] · 100;
Gotthard et al., 1994) were calculated.
Respirometry
L. tityrus pupae were used to test for sex-specific differences in CO2 release rate
(as a proxy for metabolic rate) at the Humboldt University, Berlin. CO2 release
was measured for single pupae using a two channel DIRGA (URAS 4, 0 . . .
100 ppm, Hartmann and Braun, Germany) with two flow-through respirom-
eters optimised for fast response. Data were logged to a computer via the serial
interface of the URAS 4 at an accuracy of ± 0.1 nmol g)1 min)1 and a
sampling rate of 1 s)1. A flow rate of 50 ml min)1 of CO2-free air was main-
tained by two independent mass flow controllers (MKS 1259, range
346
100 ml min)1; MKS instruments, Methuen, Massachusetts, USA). Calibration
was checked by the internal calibration function of the URAS 4. Air temper-
ature during experiments was kept at 20 ± 0.1 �C by a computer controlled
peltier cooling device, relative humidity at 80 ± 2%. Each experimental run
lasted for at least 150 min. Animals were allowed to habituate to the experi-
mental conditions for 30 min. After that time, mean mass-specific CO2 output
rate M.CO2 (nmol g)1 min)1) was calculated by averaging the CO2 output rate
over at least 90 min. This relatively short period was considered sufficient as
animals showed continuous CO2 release over longer periods (>12 h) in pilot
experiments. For more details on the experimental set up see Mbata et al.
(2000). Pupae were weighed before and after testing to calculate the water loss
during the experiments. To account for potential changes in metabolic rate
across the pupal stage, all pupae were tested at a similar age (i.e. on days 9–11
following pupation).
Statistical methods
For L. hippothoe, effects of population, temperature and sex on propor-
tionate weight loss were analysed by a three-way analysis of co-variance
(ANCOVA). As pupal mass and pupal time may passively affect weight loss
(due to differences in volume-surface ratios and the exposure times of pupae
to their environment, potentially affecting evaporation rates), both traits
were controlled for as covariates. Analogously, effects of sex on weight loss
were tested with a one-way ANCOVA in L. tityrus. The first three axes
extracted by principal component analyses (results not shown) consistently
depicted a growth, a mass, and a weight loss variable, respectively. Thus,
there should be no autocorrelation problems with adding pupal mass as
covariate in the ANCOVAs. All statistical analyses were performed using
StatSoft (1999). Throughout n gives the number of individuals and means
are given ± 1 sd.
Results
Weight loss at metamorphosis across sexes and populations of L: hippothoe
AnANCOVA revealed highly significant effects of population, temperature, and
sex on the proportionate weight loss during metamorphosis (Table 1). Overall,
sex had the strongest effectwithmales loosing about 62%of the initial pupalmass
as compared to about 58% in females (Table 2; Fig. 1). The sex difference was
highly consistent across populations and temperatures. Differences across
populations were less pronounced though highly significant. Hungarian
347
L. h. sumadiensis showed the highest values throughout except formales at 15 �C,where L. h. eurydame experienced a marginally higher weight loss (Table 2).
Moreover, alpine L. h. eurydame exhibited a higher weight loss than western
German L. h. hippothoe except for females at 20 �C and males at 25 �C. Weight
loss averaged at about 61% for L. h. sumadiensis, 59% for L. h. eurydame, and
58% for L. h. hippothoe across sexes and rearing temperatures. Further, weight
loss generally increased with increasing temperature, which was slightly more
pronounced in males than in females, causing a significant temperature by sex
interaction (Table 1, Fig. 1). Additionally, the significant temperature by pop-
ulation interaction suggests some slight differences among populations in the
response to temperature. While pupal development time did have an impact on
proportionate weight loss, pupal mass did not as could be expected from the
results of a principal component analysis (Table 1; see Methods).
We failed, however, to find a direct link between growth rate and weight loss
within (population by sex by temperature) groups. Correlation coefficients ran-
ged between )0.34 and 0.41 and were (after Bonferroni correction)
Table 2. Proportionate weight loss during metamorphosis (mean ± sd) for males and females in
three populations of Lycaena hippothoe at different experimental temperatures
T
(�C)L. h. hippothoe L. h. eurydame L. h. sumadiensis
Males Females Males Females Males Females
(%) n (%) n (%) n (%) n (%) n (%) n
15 55.4 ± 6.7 35 54.3 ± 4.7 25 59.1 ± 4.5 31 55.2 ± 3.3 32 58.8 ± 4.9 46 57.6 ± 4.7 52
20 59.7 ± 3.2 32 56.7 ± 3.2 34 61.9 ± 4.0 28 56.2 ± 3.9 43 62.8 ± 4.3 50 58.7 ± 3.8 56
25 61.1 ± 3.8 30 56.6 ± 2.1 48 60.7 ± 3.5 26 56.9 ± 2.9 40 63.5 ± 3.2 62 58.9 ± 2.9 50
30 61.5 ± 4.5 38 57.5 ± 3.6 29 62.4 ± 5.5 32 58.2 ± 2.8 44 66.9 ± 3.9 53 60.6 ± 3.7 64
Table 1. Three-way analysis of co-variance (ANCOVA) for the effects of population, temperature
and sex on the proportionate weight loss during metamorphosis in Lycaena hippothoe (total
n = 971). Effects of pupal mass and pupal time were controlled for as covariates. Significant
p-values are given in bold
Source df F p
Population 2945 52.2 <0.0001
Temperature 3945 17.1 <0.0001
Sex 1945 217.2 <0.0001
Pupal time 1945 13.9 0.0002
Pupal mass 1945 0.5 0.4801
Population · temp. 6945 3.3 0.0030
Population · sex 2945 1.2 0.3027
Temperature · sex 3945 5.5 0.0010
Pop. · temp. · sex 6945 1.8 0.0987
348
non-significant throughout (p-values ranged between 0.02 and 0.80, group
sample sizes between 25 and 64).
Weight loss at metamorphosis and metabolic rates across sexes in L: tityrus
As expected, males had higher growth rates than females (18.9 ± 0.7 vs.
17.5 ± 1.0 %/day; t183 ¼ 10.9, p<0.0001) conferring shorter larval times
(25.2 ± 0.9, n ¼ 107 vs. 27.3 ± 1.2 days, n ¼ 78; t183 ¼ )13.8, p<0.0001). An
ANCOVA confirmed a highly significant sex difference in weight loss (males:
60.6 ± 3.5%, n ¼ 107; females 56.6 ± 5.4%, n ¼ 71; sex: F1174 ¼ 36.6,
p<0.0001; pupal time: F1174 ¼ 1.1, p ¼ 0.30; pupal mass: F1174 ¼ 0.7,
p ¼ 0.40). This difference caused a highly significant sexual size dimorphism in
adult mass (males: 45.8 ± 5.1 mg; females: 51.6 ± 8.7 mg; t176 ¼ )5.7,p<0.0001), while variation among sexes in pupal mass was marginal and non-
significant (males: 116.2 ± 8.9 mg; females: 119.3 ± 13.9 mg; t183 ¼ )1.9,p ¼ 0.066). After removing outliers (defined as >1.5 times the range of the
25th–75th percentiles), mass-specific CO2 production of pupae differed
significantly across sexes (males: 212.0 ± 14.1 nmol g)1 min)1, n ¼ 39;
females; 200.1 ± 14.3 nmol g)1 min)1, n ¼ 37; t74 ¼ 3.7, p ¼ 0.0005). This
difference persisted when using the whole data set and the non-parametric
Kolmogorov-Smirnov test (males: 211.7 ± 20.8 nmol g)1 min)1, n ¼ 43;
females 204.6 ± 21.3 nmol g)1 min)1, n ¼ 40; p<0.025). Water loss during
experiments did not differ among males and females (t77 ¼ )0.1, p ¼ 0.94).
Again, there were no significant correlations between growth rate and weight
loss within both sexes (males: r ¼ 0.01, p ¼ 0.90, n ¼ 107; females: r ¼ 0.13,
p ¼ 0.28, n ¼ 71).
50
55
60
65
70
15 20 25 30
temperature [˚C]
wei
gh
t lo
ss [
%]
Figure 1. Proportionate weight loss at metamorphosis for Lycaena hippothoe males and females
from three populations at different experimental temperatures. Filled symbols: males, open sym-
bols: females. Diamonds: L. h. sumadiensis, triangles: L. h. eurydame, squares: L. h. hippothoe. For
sample sizes and standard deviations see Table 2.
349
Discussion
Accumulating evidence suggests that growth rate is a life-history trait in its
own right and in that a target of natural selection (e.g. Arendt, 1997; Nylin and
Gotthard, 1998). These findings are of wide-ranging importance for funda-
mental issues addressed by life-history theory, such as the relationship between
age and size at maturity (e.g. Abrams et al., 1996; Arendt, 1997; Nylin and
Gotthard, 1998; Gotthard, 2000). As in a number of other species (cf. Gotthard
et al., 1994; Arendt, 1997), growth rates were found to vary across sexes and
populations of copper butterflies. Those differences presumably represent
adaptations driven by sexual selection and the opportunities and constraints
imposed by the given environment (Fischer and Fiedler, 2000a, 2001, 2002a,
2002b). If thus growth rates are at least sometimes not maximised, this can only
be understood if a fast development carries some kind of cost (Arendt, 1997).
Based on the variation found, we predicted differences in proportionate weight
loss at metamorphosis, assuming that higher growth rates confer higher weight
losses.
By analysing weight loss in four populations of copper butterflies we could
show that (1) protandrous, faster developing males suffered a higher weight
loss than females throughout, that (2) population differences in weight loss
generally followed known differences in growth rates, and that (3) males and
females differ in metabolic rates during pupal development. Thus, our results
correspond closely to our a priori predictions, giving support for the notion
that a higher weight loss during the development to adulthood may comprise a
physiological cost of rapid development. To further illustrate the relevance of
such presumed costs the sexual size dimorphism among males and females
comprises a valuable example. The difference between males and females (with
males being generally smaller in spite of their accelerated growth) is much more
pronounced in the adult than in the pupal stage, where it is in some cases even
absent (see above for L. tityrus; see further Fischer and Fiedler, 2000a, 2001,
2002b).
The sex difference in weight loss was highly consistent across species and
populations, regardless of rearing temperature, food quality, and develop-
mental pathway (Fischer and Fiedler, 2000a, 2000b; present results). It was
also found in another butterfly, Pararge aegeria (Gotthard et al., 1994). But
why should weight loss differ across sexes and populations? Because of con-
trolling for pupal mass and time as covariates, which was not the case in earlier
studies (Gotthard et al., 1994; Fischer and Fiedler, 2000a), we can largely rule
out that passive effects such as evaporation rates cause those differences. In
L. h. eurydame sexes differed in weight loss, although pupal mass and devel-
opment time are equal (Fischer and Fiedler, 2002b). Likewise, L. h. eurydame
exhibited a higher weight loss than L. h. hippothoe in spite of equal pupal
350
masses and a generally shorter pupal development time in the alpine popula-
tion (Fischer and Fiedler, 2002b). Thus, different mass to surface ratios or
pupal times cannot explain those differences in weight loss.
Based on our results we suggest that there might be a causal link between
growth rate and weight loss. This is, however, not supported by correlation
analyses. The failure to confirm a direct link within groups is not entirely
surprising, as there is substantial variation in both traits, which may make it
hard to corroborate a consistent pattern within treatment groups (Gotthard
et al., 1994). Apart from genetic and environmental sources of variation,
methodological constraints further hamper analyses. Measuring butterfly fresh
weight is always a balance between being too early (meconium not entirely
excreted) and too late (weight loss due to desiccation). Moreover, allocation
patterns might be largely or entirely fixed due to a lack of genetic variation
today, thus representing a historical trade-off (e.g. Stearns, 1992). This may
also explain conflicting results found in Pararge aegeria, where sex-differences
in weight loss persisted also in the Madeira population not showing higher
male growth rates (Gotthard et al., 1994). One should note here that protan-
dry, being related to seasonal environments, is expected to occur in almost the
entire range of Pararge aegeria (Nylin et al., 1993).
As proximate reason for the differences in weight loss we suggest generally
elevated metabolic rates in fast growing individuals and populations, persisting
in the pupal stage (cf. Stockhoff, 1991; Gotthard et al., 1994; Gotthard, 1998).
Although pupal development times, a possible correlate of higher metabolic
rates, do only marginally differ between sexes (though there is a consistent
trend for males being faster; Fischer and Fiedler, 2000a, 2002a, 2002b), met-
abolic rates during pupal development were indeed found to be significantly
higher in L. tityrus males than in females. Interestingly, the sex difference in
metabolic rate is very similar to the one in weight loss, with males showing by 6
and 7% higher values. The males’ increased metabolism is considered to result
from selection for early male emergence and thus rapid development (Fag-
erstrom and Wiklund, 1982; Wiklund et al., 1991; Zonneveld and Metz, 1991;
Fischer and Fiedler, 2000a).
In conclusion, our results suggest that a higher proportionate weight loss
during pupal development may comprise a physiological cost of a faster
development, which reduces the pay-off of high growth rates, as achieving a
high pupal mass is not proportionally reflected in adult size. However, we do
acknowledge that our study is correlative in nature, and that experimental
approaches using more direct manipulations of growth rates (e.g. artificial
selection) are required to settle the issue. This is especially true as we could not
show a direct link between growth rate and weight loss. Identifying the costs
associated with rapid growth is an important issue in life-history theory, and
will remain a challenge to evolutionary ecologists for some time to come.
351
Acknowledgements
We thank K. Reinhold and K. Gotthard for valuable comments on earlier
drafts of this manuscript. S. Bauerfeind, K. Kaminsky, C. Ruf, and A. Servant
helped with butterfly rearing, and D. P€uschel assisted with CO2 measurements.
We acknowledge financial support from the Friedrich-Ebert-Foundation and
the German Research Council (DFG grant no. Fi 846/1-2) to K. Fischer.
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