Long-term repeatability makes basal metabolic rate a likely heritable trait in the zebra finch Taeniopygia guttata
Department of Biology, Norwegian University of Science and Technology, NO-7491 Trondheim, Norway
* Author for correspondence (e-mail: bernt.ronning{at}bio.ntnu.no)
Accepted 19 October 2005
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Summary |
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Key words: basal metabolic rate, energetics, heritability, individual variation, natural selection, repeatability, zebra finch, Taeniopygia guttata
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Introduction |
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Repeatability provides important information by setting the upper limit for
heritability (Falconer and Mackay,
1996), although this may not always be the case (see
Dohm, 2002
). Because of this
relationship with heritability, repeatability can give an indication of how
effective natural selection will be in changing the trait. Studies on
repeatability of metabolism in vertebrates have mainly been focused on maximum
metabolic rate (Hayes and Chappell,
1990
; Chappell et al.,
1995
,
1996
;
Hayes and O'Connor, 1999
),
although daily energy expenditure
(Speakman et al., 1994
;
Potti et al., 1999
), field
metabolic rate (Berteaux et al.,
1996
) and resting metabolic rate (RMR;
Vézina and Thomas,
2000
) have also been studied. Despite the large abundance of data,
we are aware of only very few studies reporting repeatability of BMR
(Bech et al., 1999
;
Hõrak et al., 2002
;
Labocha et al., 2004
;
Vézina and Williams,
2005
). Significant repeatabilities in those studies indicate
permanent inter-individual differences in BMR. In addition to inter-individual
variations (Rezende et al.,
2004a
), there also exist intra-individual variations in BMR during
an animal's life cycle (Langseth et al.,
2000
; Lindström and
Rosen, 2002
; Lindström
and Klaassen, 2003
). This intra-individual phenotypic variance is
mainly affected by the external environment that the animal experiences
(Falconer and Mackay, 1996
).
Variations in BMR between individuals are affected by genetic differences in
addition to the external environment. Because of this phenotypic flexibility
the length of the measurement period could affect the repeatability of a
physiological trait in such a way that repeatability decreases with the length
of the measurement period (Chappell et al.,
1996
; Hõrak et al.,
2002
; Vèzina and
Williams, 2005
). A long period will normally involve larger
environmental variation compared to a shorter period, and this may result in a
greater variation of the trait, which in turn will decrease the repeatability.
Several studies have reported flexibility in organ size and metabolic
physiology over short timescales depending on environmental conditions and
physiological status (see Piersma and
Lindström, 1997
). Breeding is a life-cycle event that may
lead to changes in organ mass and the metabolic machinery
(Chappell et al., 1999
;
Langseth et al., 2000
;
Vézina and Williams,
2003
).
For selection on a physiological trait to be effective the trait has to be
consistent over a period that is long enough to make it possible for the trait
to influence the fitness and/or survival of the individual. A very short
interval between repeated measurements of a metabolic trait can fail to reveal
any potential intra-individual variation in that trait because the `metabolic
machinery' has not had time to change. A changing environment might, over
time, induce changes in metabolic traits, but in spite of a change in the
absolute performance, the relative performance rankings of individuals can be
unaltered and repeatability can still be high
(Chappell et al., 1996). Even
though the absolute maximal rate of oxygen consumption
(
O2max)
increased during 8 weeks of cold acclimation in deer mice Peromyscus
maniculatus, the relative performance remained consistent and
O2max
was consequently highly repeatable over the period
(Rezende et al., 2004b
). A
change in both absolute performance and ranking with time would result in low
or zero repeatability, implying low heritability, and the effect of selection
would be weak (Chappell et al.,
1996
). Friedman et al.
(1992
) found that
O2max
in a strain of mice was highly repeatable between 2 consecutive days, and
Terblanche et al. (2004
) found
significant repeatabilities of SMR in tsetse flies Glossina
pallidipes of different ages measured during an 84 min period. It may be
argued that the time periods over which these repeatability measurements were
obtained were not long enough to pick up any potential change in the trait and
thus are less informative compared with longer measurement periods. It is
therefore important to consider the length of the measurement period carefully
according to which trait and species are being examined. This is especially
important if the results are to be interpreted in light of heritability and
natural selection.
In the present study, rates of BMR were obtained over a 2.5 year period in zebra finches Taeniopygia guttata Vieillot in order to obtain short- as well as long-term repeatabilities of BMR. We are not aware of any previous study of repeatability of any metabolic trait over such a long time period. The present study, which involves repeated individual measurements over a considerable part of the zebra finches reproductive lifespan (2.54.5 years), should consequently be adequate to reveal any long-term repeatability of BMR within individuals.
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Materials and methods |
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All birds had been kept in sex-specific holding aviaries since 6 weeks of age and had consequently not been breeding. The birds did breed in smaller breeding cages in a period from the start of September to the end of December, 2002. When the breeding experiment concluded at the end of December 2002 the birds were moved back into their sex-specific holding aviaries.
Metabolic measurements
For each bird four measurements of BMR were obtained during the period
March to May, 2002. The birds were measured in random order, but with a
minimum of 5 days between each measurement. In 2004, BMR was again measured
twice in each bird, once in April/May and once in October/November. Hence, a
total of six BMR measurements were obtained from each bird during the period
March 2002 to November 2004.
Basal metabolic rate was measured as O2-consumption rates using
an open flow system. Dry air was pumped through four metabolic chambers made
from 1.5 l metal boxes. For each metabolic chamber a calibrated Bronkhorst
High-Tech mass flowmeter (Ruurlo, The Netherlands) was used to adjust the flow
to 400 ml min1. Both influent and effluent air was dried
with Drierite® (Krugersdorp, South Africa). A Serwomex Xentra,
type 4100, two-channel oxygen analyser (Crowborough, England) measured the
oxygen concentration in the effluent air. Dry outside air (set to 20.95%
oxygen) was used to calibrate the oxygen analyser and pure stock nitrogen was
used for zero calibration. An automatic valve-system switched between the
chambers, so that two chambers were measured simultaneously for 26 min, with
fresh air being pumped through the system for 4 min between each switching.
The birds were taken from their holding aviaries and placed individually in
the metabolic chambers at about 19:00 h in the evening, i.e. at the time of
the normal start of their resting phase. Measurements of oxygen consumption
were obtained throughout the night, and the birds were removed again around
08:00 h, 1 h after the time of light-on in the morning. The voltage outputs
from the oxygen analyser and mass flowmeters were stored on a Grant Squirrel,
type 1200 datalogger (Cambridge, England) at 30 s intervals. The data was
later transferred to a computer for subsequent analyses. The rate of oxygen
consumption (O2)
was calculated using formula 3A given by Withers
(1977
). Since the birds were
assumed to be postabsorptive during the measurement a respiratory quotient of
0.71 was used. The lowest
O2, which was
calculated as the lowest 10 min running average value during the night, was
used to represent the BMR. This was usually attained during the latter part of
the night or in the early morning, supporting our assumption that the birds
were postabsorptive. Body mass at the time of the lowest oxygen consumption
was used when calculating the mass-specific BMR. Body mass was obtained just
before birds were placed in the metabolic chamber and again when the birds
were taken out. A linear body mass reduction was assumed for obtaining the
body mass at the time of the lowest
O2. The
temperature in the room containing the metabolic chambers was 35°C, which
is within the thermoneutral zone for the zebra finch
(Calder, 1964
; B.R., B.M. and
C.B., personal observations).
Since BMR is an energetic measure it should actually be expressed in energetic units. Since in the present study we are focusing on the consistency of the BMR values and not the absolute values, we have chosen to present BMR as rates of oxygen consumption, which are the actual measurements obtained.
Data analyses
Variance components derived from a one-way analysis of variance (ANOVA)
were used to calculate the repeatability of BMR after the procedure described
by Lessells and Boag (1987).
Since whole-animal rate of O2-consumption is highly dependent on
mass, we removed body mass as a factor by using unstandardized residuals based
on reduced major axes (RMA) regressions of log10 mass-dependent BMR
on log10 body mass in the ANOVA. The residuals were calculated for
each sex from all six measurement periods separately. The standard error of
repeatabilities was calculated following Becker
(1984
). Short-term
repeatabilites (over approximately 1.5 months) were calculated using the four
measurements of BMR obtained in 2002. Despite the rather long measurement
period (1.5 months) used as our shortest time period compared with many other
studies on repeatability, we have decided to refer to this as the short
period. Each individual bird was used for both the short-term and the
long-term repeatability analyses. When calculating long-term repeatabilities,
the two last BMR measurements from spring 2002 and the two measurements
obtained in 2004 were used. This means that the two last measurements used in
the short-term analyses are the same measurements used as the two first in the
long-term analyses. A few birds died during the experimental period. Hence,
the male group was reduced from 19 to 18 individuals and the female group from
20 to 18 individuals between the short- and long-term analyses.
Since ordinary least-square regressions might underestimate the true
allometric exponent scaling BMR to body mass
(Pagel and Harvey, 1988), a
RMA-regression was used for calculating the allometric exponent and the
residuals used in the calculation of repeatabilities. The allometric exponent
in the RMA-regression was calculated as the ratio of the standard deviation
(S.D.) of y (log10 mass-dependent
BMR) to the S.D. of x (log10 body
mass). The mixed linear model was performed using S-PLUS (Insight-ful Corp.,
Seattle, USA). All other analyses were performed using SPSS ver. 12.01 (SPSS
inc., Chicago, USA). Values reported are means ± 1
S.E.M. The significance level was set at
P=0.05.
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Results |
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|
|
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Repeatability
The repeatability of BMR was highly significant (P<0.001) for
both sexes for the short (male R=0.501;
F18,57=5.02 and female R=0.413;
F19,60=3.81) as well as the long period (male
R=0.465; F17,54=4.48 and female R=0.522;
F17,54=5.36; Table
3). Hence, a significant portion of the variation in the BMR can
be attributed to permanent between-individual variations
(Fig. 2). For both sexes pooled
the repeatability was 0.571 (F38,117=6.32;
P<0.001) for the short period and 0.567
(F35,108=6.24; P<0.001) for the long period.
The 95% confidence intervals (i.e. 2 S.E.M.)
substantially overlapped the means, and, consequently, the short- and
long-term repeatability values were not significant different. This applied to
the pooled sample as well as the sex-specific samples
(Table 3).
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Discussion |
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Metabolism in wild living birds appears to exhibit considerable flexibility
(Langseth et al., 2000). In
laboratory studies we are able to control environmental factors such as
temperature, photoperiod, humidity, food availability and breeding activity,
which all influence the metabolic rate in the wild. Different activity
patterns can influence the RMR of zebra finches
(Nudds and Bryant, 2001
). Our
birds were kept in uniform large cages during the experimental period, and any
intraspecific differences in BMR are therefore unlikely to be explained by
differences in activity patterns.
Repeatability
Body mass is shown to be a highly repeatable trait in birds and mammals
(Hayes and Chappell, 1990;
Hõrak et al., 2002
).
Since there is a strong linkage between body mass and BMR, the repeatability
of mass-dependent BMR values and, to some extent, also mass-specific BMR,
could be influenced by repeatability of body mass. In the present study,
however, this was controlled for by using residual values of BMR.
In the present study we found a highly significant repeatability of BMR for
both sexes of zebra finches over a 1.5 month as well as a 2.5 year period. To
our knowledge no other study has examined the repeatability of BMR over such a
long time period, so it is difficult to find results for direct comparison. A
field study of black-legged kittiwakes Rissa tridactyla showed a
significant repeatability of BMR over 1 month (R=0.642) and 1 year
(R=0.347; Bech et al.,
1999). BMR in captive greenfinches Carduelis chloris
showed significant repeatability over both short periods of 4 and 8 days
(R=0.89 and 0.84, respectively) and a time period of 4 months
(R=0.65; Hõrak et al.,
2002
). In both of these studies, the repeatability decreased from
the short to the long measurement interval, but was still high and significant
during the longest time period. Hence, the present data on the zebra finches
differ in that the repeatability was of the same magnitude even when measured
during the long (2.5 year) period. In a recent study, Vézina and
Williams (2005
) reported a
decline in the repeatability of RMR over time for non-breeding captive male
zebra finches. Their short measurement period was 8 days (with
R=0.626), and their long measurement periods were 127249 days
(R=0.445) and 135257 days (R=0.287). The two longest
time periods were thus of approximately the same length, but gave quite
different repeatability values. Their short period was much shorter than our
short period of 1.5 months, and they used two measurements when calculating
the repeatabilities while we used four. Except for those differences between
their and our study we can offer no explanation as to why the results
differ.
Depending on the flexibility of a particular trait, the repeatability would
generally be expected to decrease with an increase in the time period over
which it is measured. In the present study there were only small and
non-significant differences in the repeatability values of BMR between the
short and long measurement period, both in the pooled sample as well as the
sex-specific samples. Hence, the repeatability of BMR for the zebra finches
was unaffected by the length of the measurement period. There might be several
reasons why BMR for the zebra finches in our study shows high stability over
such a long time period compared with other metabolic traits in other species
(O2max
in Belding's ground squirrels Spermophilus beldingi,
Chappell et al., 1995
; field
metabolic rate in meadow voles Microtus pennsylvanicus,
Berteaux et al., 1996
). It
should be kept in mind that the zebra finches in this present study, although
going through a breeding period, were being kept under laboratory conditions
when the BMR measurements were conducted. Such an environment does not
generate phenotypic adjustments to the same extent as in the wild. However,
this cannot be the only explanation since the BMR of the greenfinches in the
study by Hõrak et al.
(2002
) showed a marked
decrease in repeatability with time despite being held in laboratory
conditions, as did those measured by Vèzina and Williams
(2005
) in laboratory-held
zebra finches. It is possible that BMR has higher potential stability,
compared with metabolic traits like
O2max
and field metabolic rate, because BMR mainly represents the anatomical and
physiological characteristics of an animal
(Daan et al., 1990
;
Burness et al., 1998
), and
hence is not so influenced by behavioural variation.
The BMR measurements used for the repeatability estimation from the long
time period were not evenly distributed. The two first measurements used were
obtained in spring 2002 and only separated by a few days, while the last two
were obtained in 2004 and separated by approximately 7 months. During the 2
year period, when no measurements of BMR were obtained, all the finches
underwent a breeding period, which is known to induce large changes in BMR
(Bech et al., 1999;
Langseth et al., 2000
;
Nilsson, 2002
;
Vézina and Williams,
2005
). As mentioned above, an increase in the population mean
value does not necessary lead to a change in the variance between the
individuals. There is no way of knowing for certain if the repeatability
estimates would have been different if the BMR-measurements were evenly
distributed through the long period. Breeding is a stressful challenge and may
evoke individual adjustments in metabolism that can lead to lower
repeatability in BMR. In the present study BMR still showed a high
repeatability even when measurements, conducted after these potential
adjustments made during breeding, were incorporated in the analyses. In a
study of zebra finches, Vézina and Williams
(2005
) found a significant
repeatability of RMR between two breeding periods. Our results are noteworthy
because we report that repeatability persists when comparing periods before
and after a breeding event.
Natural selection
The significant repeatability of BMR over 2.5 years, which constitutes a
substantial part of the reproductive lifetime in free-living zebra finches
(maximum lifespan 2.54.5 years;
Zann and Runciman, 1994),
clearly shows that there is significant between individual variation in this
particular trait, upon which natural selection can work, provided that the
trait is heritable. However, it should be mentioned that it also could be the
capacity to change BMR rapidly in response to changing ecological conditions
that is the selective trait. An important question to ask is: over what
timescale does the trait have to be repeatable to consider the possibility
that natural selection is working upon it? Huey and Dunham
(1987
) concluded that in the
lizard Sceloporus merriami, which has a maximum lifespan of 6 years
and a cohort generation time of 1.5 years, repeatability in running speed over
a 1 year period is sufficient to render it convenient for studies of natural
selection. It seems likely that the required length of the measurement period
of a trait to test if it is sufficiently repeatable to be a possible target
for natural selection varies with the lifespan and generation time. In other
words: to detect selection in a trait, it has to be repeatable over the
timescale during which selection occurs; it is obvious that this timescale is
longer for long-lived species with long generation times than for short-lived
animals with short generation times.
In addition to having a significant repeatability to be affected by natural
selection, the trait also has to be heritable and have a consequence for
fitness (Falconer and Mackay,
1996). The repeatability provides little information about the
actual value of heritability, and a trait with high repeatability might have a
heritability of zero (Merilä and
Sheldon, 2001
). The few studies on heritability of BMR indicate
that the heritability of BMR might be very low
(Dohm et al., 2001
;
Nespolo et al., 2003
).
However, a recent study by Sadowska et al.
(2005
) reports a relative high
narrow-sense heritability of BMR in the bank vole Clethrionomys
glareolus. One of the important advantages of a laboratory study like
ours is that genealogy is easy to record, and this simplifies heritability
estimates compared to a field study.
In summary, we have found a significant repeatability of BMR in zebra finches over a considerable time period. Hence, one of the prerequisites for natural selection to act upon this trait is fulfilled. It remains to be seen if these differences in metabolism will have consequences on fitness. Whether BMR is heritable and if natural selection is acting on the inter-individual variation in this particular trait remains to be fully answered.
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Acknowledgments |
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