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First published online February 27, 2009
Journal of Experimental Biology 212, 808-814 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.025528
Phenotypic flexibility of traits related to energy acquisition in mice divergently selected for basal metabolic rate (BMR)
ek*
Institute of Biology, University of Bia
ystok, 
wierkowa
20b, 15-950 Biaystok, Poland
* Author for correspondence (e-mail: anetak{at}uwb.edu.pl)
Accepted 6 January 2009
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: phenotypic flexibility, immediate spare capacity, organ size, organ mass, metabolic load, citrate synthase, artificial selection
|
INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Piersma and Drent, 2003). In
recent years, the magnitude of this modulation has been extensively quantified
at different levels of biological organization, from enzymes
(Sabat and Bozinovic, 2000;
Weiss et al., 1998) to tissues
(Villarin et al., 2003),
organs and whole animals (Kristan and
Hammond, 2006). Several studies have demonstrated that processes
related to energy acquisition and expenditure are among the most sensitive to
changes in environmental conditions
(Hammond and Kristan, 2000;
Konarzewski and Diamond, 1994;
McWilliams and Karasov, 2002;
Naya et al., 2005;
Toloza et al., 1991;
Tracy and Diamond, 2005). The
digestive system is the `interface' between animal and environment for energy
acquisition and, for this reason, its phenotypic flexibility has attracted
particular attention (Karasov and
McWilliams, 2005). Although such studies have identified several
major physiological processes underlying phenotypic flexibility in digestive
performance, there is little consensus on their relative significance in
accommodating changing energy and nutrient requirements [Secor and Diamond
vs Starck (Secor and Diamond,
1998; Starck,
1999a)].
Theoretical considerations suggest that the phenotypic response to
environmental challenge involves two components, as reviewed by Karasov and
McWilliams (Karasov and McWilliams,
2005). First, an initial increase of energy acquisition is
realized from the immediate spare capacity of the digestive system
(Diamond and Hammond, 1992;
Karasov and McWilliams, 2005),
which is built into the digestive organs but not utilized under routine
physiological loads. The immediate spare capacity handles increased energy
demands prior to the second phase of the response – upregulation of
physiological processes underlying energy acquisition [e.g. increased organ
mass, transporter density, etc. (Karasov
and McWilliams, 2005)].
Although this theoretical framework is physiologically reasonable, it does
not reveal the specific proximate mechanisms determining the magnitude of
phenotypic flexibility. It is also unclear how the benefits of maintaining an
immediate spare capacity for quick response to increased demands trades off
with the metabolic costs of maintaining that capacity in routine conditions.
Nevertheless, if Karasov and McWilliams' model
(Karasov and McWilliams, 2005)
is correct, then one of the main factors determining the magnitude of
immediate spare capacity and phenotypic flexibility should be the size (mass)
of the digestive organs immediately prior to metabolic stress. Here, we
propose two hypotheses relating the initial organ size to their phenotypic
flexibility. First, we hypothesize that phenotypic flexibility of internal
organs has additive rather than multiplicative dynamics. If so, we predict
that animals having relatively larger digestive organs will respond to a
sudden demand by increasing the magnitude of energy intake and upregulation of
the functions of the internal organs, which will be strictly proportional to
the initial organ size. This proportionality should particularly hold in the
first, most-challenging phase of the upregulation of the functions related to
energy acquisition, which is handled by an immediate spare capacity. If,
however, the dynamics of phenotypic flexibility is multiplicative, one can
predict two scenarios: first, the phenotypic response of animals having
initially larger organs should be more than proportional, which will allow
them to achieve a new physiological steady state faster and at higher levels.
Second, animals having smaller organs under routine conditions may respond
with proportionately greater phenotypic flexibility, which will allow them to
match energy acquisition rates of animals with initially larger organs.
The above hypotheses also embrace two possible alternative relationships
between metabolic costs of maintaining internal organs, their immediate spare
capacities and the magnitude of phenotypic flexibility. If basal metabolic
rate (BMR) subsumes these costs under routine conditions, as suggested by some
studies (e.g. Konarzewski and Diamond,
1995), then one can expect that the magnitude of phenotypic
flexibility of internal organs expressed due to sudden demand will be
positively correlated with the level of BMR preceding this demand.
Alternatively, however, the ability of animals having small internal organs
(and low BMR) to match the energy acquisition rates of animals having larger
organs would point to the independence of BMR (measured under routine
conditions) and phenotypic flexibility expressed under metabolic stress.
To test the above hypotheses, we used mice from two lines selected for high
and low BMR (Ksiek et al.,
2004). There are two reasons why mice of these lines are good
models for studying relationships between digestive organ size, immediate
spare capacities and phenotypic flexibility. First, apart from a 30%
difference in BMR, these lines distinctly differ in the relative sizes of the
small intestine, liver, kidneys and heart
(Ksiek et al.,
2004). Second, under warm thermal conditions (23°C), low-BMR
mice have 10% lower energy intake than mice from the high-BMR line.
Accordingly, we expected that because of their smaller organ sizes, and hence
immediate reserve capacities, low-BMR mice would respond to a sudden metabolic
demand with a smaller increase in energy assimilation rate (relative to organ
size) than the high-BMR line. More specifically, we predict that metabolic
loads (defined as food intake or digestible food intake per mass of a
particular organ) incurred by a sudden increase in energy demand should be
smaller for relatively larger internal organs.
To produce a sudden metabolic challenge, we transferred animals, without
prior acclimation, from an ambient temperature of 23°C to 5°C. As
thermoregulatory heat production needs to be much higher at 5°C, we
expected a corresponding immediate increase in daily energy expenditures and
hence daily energy assimilation rate. We then analyzed the between-line
differences in changes of energy assimilation rate in relation to changes in
masses of internal organs most significantly contributing to BMR – small
intestine, liver, kidneys and heart
(Konarzewski and Diamond,
1995). However, changes in organ mass may result from an
inexpensive and functionally inconsequential tissue rebuilding (i.e. an
increase of hydration) rather than changes in mass-specific metabolic capacity
(Starck, 1999b). Therefore, we
also quantified the activity of citrate synthase (CS), a mitochondrial enzyme,
which is a good indicator of the aerobic metabolic activity of tissues
(Choi et al., 1993;
Hammond et al., 2000;
Houle-Leroy et al., 2000;
Janssens et al., 2000;
Schaarschmidt and Jürss,
2003; Tripathi and Verma,
2004).
|
MATERIALS AND METHODS |
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|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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ek et al.,
2004). Males and females characterized by highest and lowest body
mass-corrected BMR were chosen as progenitors of subsequent generations of
high (H-BMR) and low (L-BMR) lines, respectively. Multiple generations of
similar selection have resulted in significant, genetically based
differentiation of the two lines in BMR, visceral organ masses and daily food
intake (Ksiek et al.,
2004). In this study, we used males from generation 25. The
experiment was conducted on 108 mice (16–18 weeks old, 30–45 g
body mass), following measurements of BMR as part of the selection procedure.
Subjects were randomly chosen from the pool of animals not qualified as
progenitors. BMR differed considerably between high- and low-BMR individuals
entering the experiment [65.3±0.5 ml O2 h–1
vs 51.8±0.6 ml O2 h–1; analysis of
covariance (ANCOVA) with body mass as a covariate,
F1,105=405.43, P<0.0001]. A week before the onset of the experiment, all animals were placed in individual plastic cages with an elevated bottom but no bedding material, on a 12 h:12 h light schedule and ambient temperature of 23°C, which is a housing temperature in our colony. Mice had free access to food (murine laboratory chow, Labofeed, Poland) and water.
Experimental procedures
Two days prior to cold exposure, 13 randomly chosen animals from H-BMR line
and 14 L-BMR animals were subjected to 48 h-long feeding trials to determine
food consumption (C) and digestive efficiency (D) at 23°C. Upon completion
of the trial the animals were killed by cervical dislocation to determine body
composition. The remaining animals were randomly assigned to three groups and
suddenly transferred from an ambient temperature of 23°C to 5°C. Each
group consisted of 14 mice from L-BMR line and 13 mice from H-BMR line and
differed in the duration of cold exposure. The first group was maintained at
5°C for two days, the second group for four days and the third group for
six days, which is the time required to reach a new steady state of body mass,
C and D (Toloza et al.,
1991).
In each experimental group, we measured body mass, C and D. Following termination of cold exposure, animals were killed to determine internal organ masses and CS activity. All procedures were accepted by the Local Ethical Committee in Bialystok (permit no. 2005/26).
Food consumption, digestibility and morphometrics
Food consumption (C) was calculated individually for each mouse as the mass
of food disappearing from the food dispenser that day minus spilled, uneaten
food [orts (Konarzewski and Diamond,
1994)]. Orts and faeces were separated from each other, dried in
an oven at 70°C and weighed to the nearest 0.001 g. D was calculated as
the difference between C and faecal output, divided by C
(Drod, 1968). The
retention time of digesta may exceed 24 h
(Toloza et al., 1991), so C
and D were analyzed in two-day periods. Digestible food intake (DFI) was
approximated as the product of C and D.
Animals were killed and weighed to the nearest 0.1 g. Small intestine, liver, kidneys and heart were excised, cleared of blood or digesta and adherent fat and weighed to an accuracy of 0.001 g.
Activity of citrate synthase
CS (EC 4.1.3.7) catalyzes condensation of acetyl coenzyme A and
oxaloacetate to form citrate in the citric acid cycle (Krebs's cycle) and thus
provides a good index of oxidative metabolism in tissues
(Choi et al., 1993;
Janssens et al., 2000).
After dissection, organs (liver, kidneys and heart) were immediately frozen
in liquid nitrogen and then stored at –80°C. Frozen samples were
homogenized in ice-cold Tris-HCl buffer (100 mmol l–1, pH
7.5) using a Miccra D-1 tissue homogenizer (CARL ROTH GmbH, Karlsruhe,
Germany). Heart samples of 0.07–0.1 g were homogenized 1:20 (w/v)
whereas kidney and liver samples of 0.2–0.4 g were homogenized 1:5
(w/v). Temperature was maintained at 4°C during homogenization.
Homogenates were centrifuged at 15,000 g for 15 min at
4°C, and supernatants were stored at –80°C until used in assays.
CS activity was estimated in 10 µl of samples of assay mixture containing
0.4 ml of 200 mmol l–1 Tris-HCl (pH 8.0) buffer, 0.1 ml of 1
mmol l–1 DTNB (5,5'-dithio-bis-2-nitrobenzoic acid),
0.1 ml of 3 mmol l–1 acetyl coenzyme A and 0.29 ml of
de-ionized water. We pre-incubated the sample for 3 min at 25°C and
initiated the reaction by adding 0.1 ml oxaloacetate. The progress and
products of the reaction were monitored for 1 min and analyzed using a
temperature-controlled spectrophotometer (Beckman DU 640, Fullerton, CA, USA)
(Houle-Leroy et al., 2000;
Schaarschmidt and Jürss,
2003) at extinction of 412 nm. All enzyme assays were run in
duplicate. Specific activity of CS was expressed in international units
(µmol substrate transformed to product min–1) per gram of
tissue wet mass (Houle-Leroy et al.,
2000).
Statistics
Differences in body mass between experimental groups were tested by means
of two-way analysis of variance (ANOVA) with line-type (L-BMR or H-BMR) and
group affiliation (control group exposed to 23°C and two-, four- and
six-day cold exposure to 5°C) as the main effects. To analyze differences
in C, D, organ masses and the activity of CS, we applied similarly structured
analysis of covariance (ANCOVA)/ANOVA with body mass (minus foodstuffs
contained in the digestive tube) as a covariate.
Because measurements of BMR are very labor intensive, we were not able to
produce replicate lines in our selection experiment. The lack of replication
confounds the interpretation of the between-line differences because the
possible effect of genetic drift cannot be effectively controlled
(Garland, 2003;
Henderson, 1989;
Henderson, 1997;
Konarzewski et al., 2005). To
remedy this problem, we relied not only on ANCOVA/ANOVA models described above
but we also analyzed between-line differences according to the guidelines
suggested by Henderson (Henderson,
1989; Henderson,
1997). Briefly, we first calculated within-line means of analyzed
traits, (computed from family means) using the residual values for the
respective ANCOVA models. We then calculated the respective within-line s.d.
(hereafter called phenotypic s.d., interpreted as the products of the square
root of the heritabilities and genetic s.d.)
(Henderson, 1997). Finally, we
calculated standardized between-line difference (d) as the difference
between within-line residual mean values divided by mean within-line
phenotypic s.d. and tested them against the lower boundary of 95% confidence
interval of d (95% CI), which estimates the expected separation of a
given trait, assuming the effect of genetic drift. We computed 95% CI using
eqn 16 from Henderson (Henderson,
1997):
 | (1) |
) in
generation F25 of our selected lines was 0.37 (A.K., unpublished) and the
number of families equalled 20.
Individual a priori pair-wise differences between experimental
groups (within-lines) were tested by t-statistics corresponding to
the two-sided P-values, adjusting the conventional level of
significance by applying a Bonferroni correction. To do this, we divided
=0.05 by 6, i.e. the number of inter-group tests performed. All tests
were carried out using SAS 9.1.3 statistical package (SAS Institute, Cary, NC,
USA).
|
RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Cold exposure elicited a twofold increase in C, with most of this increment realized during the first two days of the experiment (Fig. 1A). Throughout the whole experiment, C of H-BMR mice was considerably higher than in L-BMR mice (Table 1; Fig. 1A). However, the scope of cold-elicited increase in C was similar in both lines, as indicated by lack of significant interactions between line-type and experimental group (F3,99=2.01, P=0.1).
|
|
The increase in C was associated with 25% reduction of D (Fig. 1B). This reduction was significantly larger in L-BMR than H-BMR mice, as indicated by significant interaction between line-type and group affiliation (F3,100=4.89, P=0.003). When differences in D were analyzed separately for the first two days of cold exposure and the remaining part of experiment the interaction remained significant only for the former period (F1,53=8,76, P=0.004 and F2,77=0.99, P=0.4, respectively).
Digestible food intake (CxD) was significantly higher in H-BMR line and was affected by experimental group (Table 1) but there were no significant interactions.
Changes in mass of internal organs and metabolic loads
An increase in C elicited by exposure to 5°C resulted in sizable
between-line differences in metabolic loads [defined as C or DFI (g 2
days–1) per mass of a particular organ] on all internal
organs. We demonstrated this effect in two ways. First, ANCOVA with line-type
and group affiliation as fixed effects and body mass as a covariate revealed a
highly significant effect of line-type on the masses of all examined organs
(Table 1). We then visualized
metabolic loads as least-square means from the above ANCOVA plotted against
the respective mean values of C (small intestine) or digestible food intake
(DFI, other organs) of each experimental group
(Fig. 2). By using C or DFI, we
attempted to take into account the fact that intestines are responsible for
most of the processing and absorption of consumed food.
Fig. 2 shows that for the same
C or DFI, the masses of small intestine, kidneys, heart and liver of L-BMR
mice were considerably lower than those of H-BMR individuals. The smaller
organs of L-BMR mice were burdened with larger metabolic loads. This
conclusion is also strongly supported by a highly significant effect of
line-type (P<0.001) on all examined organs in an ANCOVA with
line-type as a fixed effect and body mass and C or DFI as covariates. In this
analysis, we did not include group as a fixed effect because of its
collinearity with C and DFI.
|
|
Activity of CS
Cold exposure elicited an increase in mass-specific CS activity in liver
and kidneys of mice of both lines (Table
1; Fig. 3A,B),
although throughout the experiment it was higher in H-BMR mice. By contrast,
the activity of CS in heart was not affected by cold exposure
(Table 1;
Fig. 3C) whereas the effect of
line-type was significant, with higher CS activity in L-BMR mice. In all of
these comparisons, the interaction between line-type and group was not
significant.
Effects of selection
When expressed as multiples of the phenotypic s.d. (d), the
between-line differences in C, the masses of all internal organs as well as
the activity of CS in liver, kidneys and heart were equal to or higher than
the boundary of the 95% CI estimating the stochastic effect of genetic drift
(Table 1). They therefore most
probably reflect genetic correlation with the primary, selected trait –
BMR.
|
DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). The
mechanistic basis of the upregulation was intensively studied particularly in
the context of changing food availability
(Secor and Diamond, 1998;
Starck and Beese, 2001;
Starck and Beese, 2002).
However, factors determining the magnitude of this upregulation and its
relation to the immediate spare capacities are still poorly known
(Starck, 2005). Here, we asked
if lines of mice with sizable and genetically determined differences in BMR
and the masses of major internal organs differ in their ability to immediately
increase energy throughput when faced with a sudden cold exposure.
Like Toloza and colleagues (Toloza et
al., 1991), we found that, compared with mice housed at 23°C,
mice of both lines exposed to a sudden cold exposure were able to double their
C within the first 48 h (Fig.
1A). However, in both lines, the increase in C was accompanied by
a 25% decrease in D (Fig. 1B).
This was not observed in similar studies
(Naya et al., 2005;
Toloza et al., 1991), in which
the animals were exposed to milder temperatures. Furthermore, Toloza and
colleagues (Toloza et al.,
1991) maintained their mice on an easily digestible high-sucrose
diet whereas we fed our animals a laboratory chow containing 5% cellulose. It
is also important to note that to identify the contribution of the immediate
spare capacity, one needs to use experimental conditions that force animals to
utilize that capacity in full but not force them into negative energy balance.
For example, moderate increases in energetic demands trigger changes in
digesta distribution within the gut without simultaneous upregulation of organ
function (Naya et al., 2005).
However, sudden exposure of our mice of both lines to ambient temperatures
lower than 5°C not only causes a reduction in D but also in body mass
(M.K., unpublished). We therefore argue that the decrease in D observed during
first two days of cold exposure and the simultaneous lack of reduction of body
mass indicate an exhaustion of immediate spare capacity, which was not
associated with the utilization of energy reserves stored, e.g. in fat.
The immediate decrease of D triggered by cold exposure was greater in L-BMR than H-BMR mice, which was indicated by a significant line-type x experimental group interaction (Fig. 1B). This was the first manifestation of the low ability of L-BMR mice to respond to sudden cold exposure through the utilization of an immediate spare capacity of internal organs. This supposition is supported by a comparison of the between-line differences in masses of internal organs. For the same cold-elicited food intake (or DFI), animals from the L-BMR line had significantly smaller small intestine, kidneys, heart and liver than mice from the H-BMR line (Fig. 2A–D). We conclude that, even though L-BMR mice upregulated organ function, they were burdened with larger metabolic loads than those of H-BMR mice. However, the lack of interaction between line-type and experimental group indicates that, in relation to values at 23°C, the scope of the upregulation at 5°C did not differ between lines.
These findings also shed light on the relationship between organ masses
prior to a sudden metabolic challenge and immediate spare capacity. Similar
scopes of increase of DFI in the two lines, particularly during the first two
days of cold exposure, suggest that the functional elements of the tissues
forming the immediate spare capacity of a given organ under non-stressful
conditions are strictly proportional to its total mass. Evaluation of the
costs of maintenance of immediate reserve capacities of internal organs and
their phenotypic flexibility is one of the important and still unresolved
problems of physiological ecology (Starck,
2005). Although we did not attempt their precise evaluation, we
demonstrated that these costs most probably correlate with variation in BMR
– the primary trait under selection in our experiment. We have reported
elsewhere that at 23°C the between-line differences in the mass of studied
organs are genetically correlated with BMR
(Ksiek et al.,
2004). In the present study, we have shown that these mass
differences are maintained throughout the course of a sudden and acute cold
exposure that elicited substantial size and CS activity increases in most of
the studied organs (Fig.
2A–D; Fig. 3)
and that the differences are greater than those expected under genetic drift
(Table 1). Thus, we conclude
that the absolute magnitude of the phenotypic flexibility is, in significant
part, genetically correlated with BMR.
We believe that this finding adds an important component to the functional
understanding and interpretation of BMR. The advantages of high BMR are mainly
discussed in the context of the evolution of endothermy and are thought to be
an unavoidable result of an ability to sustain high metabolism (e.g.
Bennett and Ruben, 1979;
Koteja, 2002). Our results
suggest that high BMR confers another advantage: when faced with sudden
physiological challenges, immediate spare capacities of individuals with high
BMR enable them to consume and process substantially more food than those
having low BMR. Metabolic loads exerted on organs of low-BMR mice were
significantly larger than those observed in the H-BMR line. So, in absolute
terms, both lines of mice did not respond in a similar way to the same
metabolic challenge; other things being equal it is reasonable to conclude
that low-BMR mice were closer to entering negative energy balance. Thus, even
though high BMR is linked with high C
(Ksiek et al.,
2004), this energetic cost may turn into a selective advantage
when animals are faced with a sudden and unpredictable deterioration of
environmental conditions.
The question remains whether the observed increase in organ masses reflects
metabolically costly upregulation of function or an inexpensive cellular
hypertrophy (Starck et al.,
2004). For example, postprandial growth of the small intestine of
colubrid snakes does not involve the production of new tissues
(Starck and Beese, 2001;
Starck and Beese, 2002).
However, an increase of the mammalian gut capacity to absorb nutrients is
largely determined by the rate of energetically costly cellular replacement
(Starck, 2005), with new cells
capable of producing more digestive enzymes
(Karasov and Hume, 1997). Some
studies have not found a correlation between organ masses (e.g. liver, small
intestines and kidneys) and BMR (Chappell
et al., 2007; Russell and
Chappell, 2007; Selman et al.,
2001; Speakman et al.,
2004). This inconsistency can be attributed to the variability of
mass-specific organ oxidative capacity
(Vezina and Williams, 2005) or
by contributions of other tissues (e.g. avian pectoral muscles) to BMR
(Chappell et al., 1999). The
changes of CS activity reported here suggest that an increase of kidney mass
was accompanied by a considerable increase of mass-specific metabolic
intensity (Fig. 2B;
Fig. 3B). However,
cold-elicited increase in CS activity but not mass may be important in the
liver, the largest internal organ (Fig.
2D; Fig. 3A). This
corroborates the results of earlier studies showing that upregulation of liver
oxidative capacity plays an important role in the response to cold exposure
(Villarin et al., 2003) and
significantly contributes to metabolic rates
(Vezina and Williams,
2005).
The effect of sudden cold exposure on the masses of internal organs and
their respective CS activities provides interesting information on their
relative contribution to phenotypic flexibility in relation to selection on
BMR. The response of secondary traits, such as organ mass, to selection
depends on the strength of genetic correlation between the primary (selected)
and secondary trait(s), which is partly determined by the respective
heritabilities (Falconer and Mackay,
1996). Narrow sense heritabilities (h2) of
internal organ masses are relatively high and reach 0.4
(Schlager, 1968). This
explains a substantial, indirect response of internal organ masses to
selection on BMR. Heritabilities of the activities of the underlying oxidative
capacity of enzymes are thought to be much lower
(Garland et al., 1990). If so,
the between-line differences in energy assimilation observed in our study
should be mainly determined by changes in the frequency of genes related to
cell hyperplasia, which should not directly affect the enzymatic activities.
This is in contrast to the magnitude of changes in CS activity in liver and
kidneys elicited by cold exposure, which were far greater than differences due
to line-type (Figs 2 and
3). This suggests that the
upregulation of the activity of oxidative enzymes in those organs is only
weakly related to genetically determined differences in BMR. The
organ-specific nature of the relationship between enzymatic activity, BMR and
cold acclimation is also shown by higher CS activity in the heart of L-BMR
mice and the absence of cold-elicited changes. Phenotypic plasticity per
se is heritable (Scheiner,
2002). Our results suggest that the scope of reversible
upregulation (phenotypic flexibility) of the mass-specific oxidative capacity
of internal organs can respond to artificial and, perhaps also, natural
selection.
In summary, we demonstrated that the phenotypic flexibility of internal
organs is largely determined by their size/mass and (in the case of kidneys
and liver) mass-specific CS activity prior to an increased energy demand,
which supports the corollary of Karasov and McWilliams' model
(Karasov and McWilliams,
2005). Indirectly, our results suggest that variation in BMR, by
definition measured under non-stressful conditions, most probably correlates
with the magnitude of the immediate spare capacities that handle the initial
phase of the upregulation of the function of internal organs, when challenged
with increased energy demands. Finally, the lack of line-type x
experimental group interactions points to the additive rather than
multiplicative dynamics of the phenotypic flexibility of internal organs.
|
Footnotes |
|---|
czuk and our numerous
students for technical assistance and patience in carrying out the project.
This study was supported by Polish Ministry of Science and
Higher Education (MNiSW) grant 2 PO4C 020
28 to A.K. |
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