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First published online December 14, 2006
Journal of Experimental Biology 210, 65-74 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02625
Associations between basal metabolic rate and reproductive performance in C57BL/6J mice
1 Division of Obesity and Metabolic Health, Rowett Research Institute,
Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
2 Animal Nutrition and Health Department, Scottish Agricultural College,
Kings Buildings, West Mains Road, Edinburgh EH9 3JG, UK
3 Macaulay Institute, Craigiebuckler, Aberdeen AB15 8QH, UK
4 Sustainable Ecosystems, CSIRO - Davies Laboratory, PMB PO Aitkenvale, QLD
4814, Australia
5 Institute of Evolutionary Biology, School of Biological Sciences,
University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
6 Aberdeen Centre for Energy Regulation and Obesity (ACERO), School of
Biological Sciences, University of Aberdeen, Aberdeen AB24 2TZ, UK
Author for correspondence (e-mail:
j.speakman{at}abdn.ac.uk)
Accepted 31 October 2006
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Summary |
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Key words: resource allocation, sustained metabolic rate, fecundity, mouse, BMR
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). Despite the expectation that it would reflect some minimal
level of homeostatic cellular processes, BMR shows tremendous variability both
between and within species (McNab,
2005; Rezende et al.,
2004; Snodgrass et al.,
2005), raising two key issues: why does the variation exist and
what are the functional implications of the variability? Clearly, an
individual with a high BMR would need to feed for longer to fuel its
metabolism than one with a low BMR. Alternatively, if both animals fed for the
same time, the one with the higher BMR would have less surplus energy
available to devote to alternative activities such as reproduction
(Gadgil and Bossert, 1970).
Previous focus has therefore been on the benefits that individuals with high
BMR might derive to offset the potential disadvantages of their high rates of
metabolism.
During the late 1970s and early 1980s two similar hypotheses were published
about the potential advantages that individuals having high BMR might have.
Bennett and Ruben suggested that endotherms maintain high BMRs, as this
enables them to achieve substantially higher maximal rates of energy
expenditure than ectotherms (Bennett and
Ruben, 1979). This has been called the `aerobic capacity model'
for the evolution of endothermy (Bennett
and Ruben, 1979; Taigen,
1983; Bozinovic,
1992; Hayes and Garland,
1995). Generalising this idea to the level of the individual
within an endothermic species, the aerobic capacity model suggests that
individuals with high BMRs sustain these rates because they derive an
advantage in situations where a maximal rate of energy metabolism is required.
The aerobic capacity model links BMR to maximal rates of expenditure over
short periods of time. The second hypothesis was that a higher BMR may be
related to a higher sustained metabolic rate (SusMR); the maximal rate of
metabolism that an individual could sustain over days and weeks
(Drent and Daan, 1980). This
may also provide a context for the evolution of endothermy
(Farmer, 2000;
Koteja, 2000). SusMR is
presumed to be limited by an animal's morphology. A big gut, and associated
organs (such as the liver) that can process energy faster, makes more energy
available to support SusMR but also requires a greater amount of maintenance
(BMR) (Drent and Daan, 1980;
Hammond and Diamond, 1992;
Hammond and Diamond, 1997;
Peterson et al., 1990;
Weiner, 1989;
Weiner, 1992). Therefore, an
individual with a higher BMR will have greater capacity for SusMR and, if
available energy is unlimited, they may be able to sustain greater
reproductive output.
A direct prediction of the SusMR hypothesis is that individuals with higher
BMRs will have greater capacity for SusMR. One of the most energetically
demanding periods in a small mammal's life history is late lactation
(Thompson, 1992). Our work on
the lactating MF1 mouse (Johnson and
Speakman, 2001; Johnson et
al., 2001a; Johnson et al.,
2001b; Johnson et al.,
2001c; Krol et al.,
2003; Krol and Speakman,
2003a; Krol and Speakman,
2003b; Speakman et al.,
2001; Speakman and Johnson,
2000; Speakman and Krol,
2005; Speakman and McQueenie,
1996) and studies of other lactating small rodents
(Hammond and Diamond, 1992;
Hammond and Diamond, 1994;
Hammond et al., 1994;
Hammond et al., 1996;
Konarzewski and Diamond, 1995;
Rogowitz, 1998;
Rogowitz and McClure, 1995)
have shown that BMR and SusMR are associated because, under different
conditions (e.g. between non-breeding and lactating, or between different
groups of lactating mice held at different ambient temperatures), they share a
dependence on aspects of morphology that limit the uptake of energy or its
utilisation. However, support for the existence of such a link at the
individual level is sparse (Daan et al.,
1989; Daan et al.,
1990). In lactating mice, individual variations in BMR do not
correlate with individual variation in organ morphology
(Krol et al., 2003;
Speakman and Johnson, 2000).
Other studies have also failed to find associations between individual
variation in morphology and BMR in birds and non-lactating mammals
(Burness et al., 1998;
Corp et al., 1997;
Geluso and Hayes, 1999;
Koteja, 1996).
The absence of an association between variations in BMR and morphology is
consistent with the large number of studies that have failed to establish the
expected links between individual variations in BMR and markers of
reproductive output (Derting and McClure,
1989; Earle and Lavigne,
1990; Hayes et al.,
1992b; Johnson et al.,
2001b; Stephenson and Racey,
1993a; Stephenson and Racey,
1993b). One possible reason for this failure is that previous
studies have tended to measure BMR in pre-reproductive animals. Lactating mice
show considerable morphological plasticity during lactation relative to the
situation when they are virgins, including expansion of their alimentary
tracts and liver sizes (Fell et al.,
1963; Kennedy et al.,
1958) with associated modulations of their resting metabolic rates
(Speakman and McQueenie,
1996). Previously pregnant mice have a greater body mass,
attributed to protein accumulation, than nonparous mice
(Holinka, 1980). Therefore, we
would argue that lactating mice never return to their original
pre-reproductive form, and their post-reproduction morphology retains a shadow
of the lactation experience. Perhaps after lactation, rather than before
reproduction, is a more appropriate time to seek links between reproductive
performance and BMR, if we are to deepen our understanding of the functional
significance of its variation.
In the present study, we set out to determine whether animals with greater BMR can sustain higher levels of reproductive output or if reproduction is sacrificed for maintenance, by measuring the BMR in the post-reproductive period of a large cohort of female C57BL/6J mice (N=304). In addition to the usual ways to characterise reproductive output (litter mass and size at birth and weaning), we also set out to measure the association between BMR and the probability that dams will give birth to live pups and successfully wean pups, the offspring losses that occur during gestation and lactation, and the sex ratio of the offspring produced. We found no positive association between post-reproductive BMR and prior reproductive performance. Indeed, females with greater BMR had an increased frequency of gestational body mass losses suggestive of foetal resorption, suggesting that a high BMR was disadvantageous.
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Materials and methods |
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Measurements
Animals were placed on a 30-day measurement schedule where body mass was
measured daily for two weeks, and the basal metabolic rate (BMR) of each
animal was measured once using an open-circuit respirometry system as
described by Hayes et al. (Hayes et al.,
1992a). Briefly, individual animals were placed in sealed
PerspexTM chambers in an incubator (Sanyo Gallenkamp PLC, Leicestershire,
UK) set to 30°C (within thermoneutral). Fresh air was dried through
cylinders of self-indicating silica gel (VWR International Ltd, Dorset, UK)
and pumped through the system (Charles Austin Pumps Ltd, Surrey, UK).
Mass-flow controllers (MKS Instruments UK Ltd, Cheshire, UK) provided 500-700
ml air per min, which was monitored using Alexander Wright DM3A flow meters
(GH Zeal Ltd, London, UK). Air leaving the animal chamber was dried using
silica gel and 150 ml min-1 was passed through a gas analyser
(Servomex Group Ltd, East Sussex, UK). Gas concentrations were measured
continuously, and means were calculated every 30 s for 200 min. Values of
oxygen consumption and carbon dioxide production were calculated with
corrections for temperature and pressure from the 10 lowest consecutive
measurements (equivalent to 5 min) using the appropriate equation
(Hill, 1972). The BMR (Watts)
for each animal was calculated from the respiratory quotient using the Weir
equation, as shown by Speakman (Speakman,
2000).
Data analysis
Statistical analysis was carried out using MINITAB® Release 14.1
(MINITAB Inc., State College, PA, USA). The mean body mass
(Mb) for the two-week period was calculated and used to
correct BMR by plotting Mb vs BMR and storing the
residuals. Animals were considered successful at birth if they gave birth to
live pups and at weaning if they weaned any pups. Binary logistic regression
was performed with birth (0 or 1) as the response and either BMR or residual
BMR corrected for Mb as the model. The percentage of
animals that were successful at birth or weaning was calculated from the
number of successes out of the total observations for each centile of BMR, or
residual BMR corrected for Mb. Animals that lost some or
all pups during gestation were identified by observed deviations from normal
body mass curves following pairing with a proven breeder male. Binary logistic
regression was performed with pup loss (0 or 1) as the response and either BMR
or residual BMR corrected for Mb as the model. The
percentage of animals that lost pups was calculated for each centile of BMR or
residual BMR corrected for differences in Mb.
Least-squares linear regression was used to determine if there were any
relationships between litter mass and size at birth and weaning and
Mb, and either BMR or residual BMR corrected for
Mb. The loge ratio of female to male pups per
litter was calculated and analysed by simple linear regression for a
relationship with either BMR or the residual BMR corrected for
Mb.
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Results |
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Body mass (Mb) of females that successfully gave birth was greater than unsuccessful females at the time when BMR was measured, but BMR was not different (Table 1). The variation in BMR for successful females was large (Table 1), and although the variation in Mb for the same sample was also great, only 6.9% of the variation in BMR could be accounted for by Mb (Fig. 1). Nevertheless, for successful females, the association was significant because of the large sample size (Fig. 1). However, because Mb accounted for so little of the variance, there was a large residual variation in BMR once the effects of Mb had been accounted for. We have presented results concerning BMR as uncorrected BMR as well as residual BMR corrected for Mb effects. There was no association between BMR and Mb for animals that did not successfully give birth (Fig. 1).
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We ordered the mothers by either their absolute BMR or their residual BMR corrected for Mb and then divided these ordered data into 10 equal-sized groups. Within each group we calculated the proportion of animals that successfully gave birth to live litters (265 out of 304 mated) and those that went on to wean pups (256 out of 265 that gave birth; Fig. 4). There was no significant association between the probability of birth success and either BMR (Fig. 4A) or residual BMR corrected for Mb (Fig. 4B). From the 265 animals that gave birth to live litters, only nine failed to maintain them to weaning age. Four of the five (80%) litters with two pups did not reach weaning and four out of the 11 (36%) litters with three pups failed. One of the 57 litters with six pups (1.8%) also failed to reach weaning. Failure to maintain pups to weaning was not related to BMR (Fig. 4C) or residual BMR corrected for Mb (Fig. 4D). However, the females that lost their litters before weaning all gave birth to low numbers of pups. These two factors may have been related and may have resulted from some undiagnosed reproductive problem, so these animals were excluded from further analyses.
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There was a positive correlation between litter mass at birth and Mb of females when BMR was measured (Fig. 5A), but there was no relationship between litter mass and BMR (Fig. 5B) or BMR with the effects of Mb removed (Fig. 5C). However, litter size at birth was significantly related to both female Mb (Fig. 6A) and BMR (Fig. 6B). Females that were heavier, or had greater BMR, on average gave birth to larger litters. However, the explained variance in litter size by both Mb and BMR was small (15.3% and 2.1%, respectively) and the gradients of the least-squares fitted regression lines were very shallow. Hence, on average, a female mouse with a BMR of 0.15 W gave birth to a litter of 6.1 pups and a female with a BMR of 0.25 W (67% greater) gave birth to a litter of 6.8 pups (11% greater). Moreover, this effect of BMR on litter size was completely dependent on the shared variation in both traits due to body mass, as there was no significant association between litter size and residual BMR with the effects of mass removed (Fig. 6C).
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).
Since we have previously determined the repeatability of this trait in our
measurement protocols at around 8% (Krol
et al., 2003), only a minor proportion of the total variation we
observed can be attributed to random error. This variability in domesticated
mice is typically larger, and the corresponding relationships between BMR and
body mass poorer, than is observed in other small wild rodents
(Koteja, 1995;
Sadowska et al., 2005). This
probably reflects the high variability in the contribution of metabolically
inert body components such as adipose tissue to the variance in body mass of
domestic mice.
In this study, we set out to characterise the relationship between fecundity and BMR measured after weaning in C57BL/6J mice. Associations between individual variations in BMR and reproductive performance may not have emerged in previous studies because the traits used to reflect reproductive performance (litter mass and size at birth and weaning) appear to be inappropriate performance indicators. In addition to these measurements, we made some additional measures in the present study that might better reflect reproductive capacity. These additional traits were: the probability that the female would successfully give birth; the probability the female would successful wean offspring; the extent of losses that occurred during gestation and lactation; and the sex ratio of the offspring. Previous studies have not reported the variation in these traits nor how they were correlated with BMR. We found that weight loss in the pregnant dam, which we considered to be indicative of foetal resorption, was significantly associated with individual variability in BMR and in the residual variation in BMR with the effects of body mass removed.
Most mammals have evolved to invest nutrients into reproduction across
gestation and lactation (matrotrophy). Energy can be diverted away from the
growing foetus and towards maintenance at any stage, and the dam can abort or
resorb the invested energy if conditions of food availability change
(Trexler and DeAngelis, 2003).
The inbred strain of mouse used in the current study has been shown to have an
increased frequency of resorptions with aging
(Holinka et al., 1979). This
is consistent with animals allocating energy into somal protection rather than
reproduction later in life (Yearsley et
al., 2005). The re-evaluation of resources by the dam during
gestation may be the reason why we observed a greater number of gestational
body mass anomalies consistent with abortion or resorption with increasing
BMR. This information supports an inverse relationship between reproductive
output and BMR and challenges the theory that life-history demands are driving
total energy requirements and thus BMR. However, a more direct method of
measuring resorption is required to support the observations in the current
study.
By measuring BMR in the period following rather than preceding reproduction
we hoped to reveal associations between BMR and reproductive performance that
have eluded previous attempts to establish such associations
(Derting and McClure, 1989;
Earle and Lavigne, 1990;
Hayes et al., 1992b;
Johnson et al., 2001b;
Krol et al., 2003;
Stephenson and Racey, 1993a).
Despite this different protocol, the relationships between BMR and the
parameters of reproductive output commonly used (birth litter size, weaning
litter size and weaning litter mass) were all exceedingly weak and involved
BMR explaining considerably less than 20% of the observed variance in any
particular trait. Consequently, enormous differences in BMR (increased by 66%)
were associated with very modest average differences in these measures of
performance (increased by 11-13%). It might be argued that an average
difference in reproductive output of 10% would be highly significant in
evolutionary terms, supporting the idea that high BMR may be selected for
because of the advantages in the enabled sustained metabolic rate and
consequent reproductive performance enhancement. However, contrary to this
argument, the associations that we observed between BMR and litter size, and
BMR and weaning litter mass, only occurred because these traits were also
related to Mb, and Mb and BMR were
also weakly correlated. In all cases excepting the indirect measure of
resorption, when we statistically removed the effect of Mb
on BMR, the significant associations to the reproductive performance measures
disappeared. Similar patterns of association between Mb,
BMR and reproductive performance were observed in laboratory mice by Hayes and
coworkers (Hayes et al.,
1992b) utilising the BMR measured prior to rather than after
reproduction. This indicates that measuring BMR after reproduction made no
difference to the nature of the associations between these traits. Since we
only measured BMR after reproduction, it remains theoretically possible that
there was an association between BMR prior to reproduction and reproductive
performance, but after their large performance they downregulated their basal
metabolism to compensate. Additional work measuring BMR at multiple points
throughout the reproductive process might be necessary to ultimately test the
hypothesis. Nevertheless, our data provide substantial support to the body of
previous work that has suggested that individual variations in BMR in
nonreproductive individuals do not provide an enabling mechanism for greater
sustained metabolic rates leading to enhanced litter sizes or litter masses at
either birth or weaning (Derting and
McClure, 1989; Hayes et al.,
1992b; Johnson et al.,
2001b; Krol et al.,
2003; Speakman and Krol,
2005).
Although we predicted that variations in BMR would be positively associated with parameters of reproduction, the only significant relationship we found was negative. Why high BMR should be associated with a greater probability of resorption is unclear. It is possible that resources are limited in pregnancy, and hence the female with a higher BMR has fewer resources to divert towards support of the developing foetuses. Yet, why resources should be limited in pregnancy, which exerts substantially less demand than lactation, is unclear. Moreover, this interpretation assumes that the single measure we made of BMR following reproduction was reflective of the BMR throughout pregnancy, which we did not establish. An alternative view is that for some reason individuals that sustained resorptions during reproduction ended up with an elevated BMR. Our protocol, which involved only a single measure of BMR, could not distinguish these effects. Whatever turns out to be the explanation of this effect, we found no support for a positive association between BMR and aspects of reproduction in this strain of mice.
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Acknowledgments |
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Footnotes |
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