Limits to sustained energy intake XII: is the poor relation between resting metabolic rate and reproductive performance because resting metabolism is not a repeatable trait?

Abstract

SUMMARYMany studies have investigated the consequences of individual variation in resting metabolic rate at thermoneutrality (RMRt) on reproductive performance. Despite strong theoretical reasons for expecting such an association, results have generally been disappointing. A fundamental assumption of these studies is that RMRt is a repeatable trait. We examined repeatability of RMRt in female MF1 mice over short (15days apart; N238) and long intervals (110days apart; N33). In the long-term experiment, after the first RMRt measurement, females were separated in two groups: the first was kept virgin (N16); the second was allowed to breed (N17) and measured 15days after they had weaned their pups. We also examined the association between RMRt and reproduction. We used Pearson's correlation (r) and intraclass correlation coefficients () to estimate repeatability. There was a strong effect of body mass on RMRt for all measurements. Over the short interval, repeatability was significant for body mass (r0.86; 0.86), RMRt (r0.68; 0.68,) and residual-RMRt (r0.58; 0.58). Over long intervals, repeatability of residual-RMRt was high in virgin females (r0.59; 0.60), but not in the breeders (r0.38; 0.39); body mass was repeatable only for non-breeders measured by r (r0.55). There was no significant correlation between RMRt or residual-RMRt and litter size or litter mass. In conclusion, RMRt and residual-RMRt are highly repeatable traits in virgin MF1 female mice. The lack of association between nonreproductive RMRt and reproductive performance in MF1 mice does not come about because of its poor repeatability.Key words: Mus musculus, repetability, resting metabolic rate, mouse, reproductive performance. 1989;Weiner, 1992;Peterson et al., 1990;Hammond and Diamond, 1992;Hammond and Diamond, 1997;Lovegrove, 2000). Although the first ideas were that SusMR and BMR might be linked via the energy acquisition system, it was later recognized that links between the two might also come about because of commonality in the demands of the tissues where energy is ultimately utilized. If the tissues involved in energy utilisation have high rates of energy demand in the basal state, then a similar functional linkage between tissues, BMR (RMRt), SusMR and SusEI would emerge. THE JOURNAL OF EXPERIMENTAL BIOLOGY279 Repeatability of RMRLactation is one of the most energetically demanding periods in the lives of small rodents (reviewed by Speakman, 2008;Naya et al., 2008). Many studies have been performed comparing RMRt of lactating animals to non-breeding individuals (Hammond and Diamond, 1992;Hammond et al., 1996;Konarzewski and Diamond, 1995;Rogowitz and McClure, 1995;Rogowitz, 1998;Speakman and McQueenie, 1996;Johnson and Speakman, 2001;Johnson et al., 2001a;Johnson et al., 2001b;Johnson et al., 2001c;Król and Speakman, 2003a;Król and Speakman, 2003b;Król et al., 2003;Król et al., 2007). These studies are consistent with the idea that BMR (RMRt) and SusMR (SusEI) should be closely associated. Moreover, this association i...

Milk output and composition in mice divergently selected for BMR

“…Higher milk output ability appears to result from the greater capacity for food intake and nutrient absorption of the mice with genetically determined high levels of BMR. It is also important, as we demonstrated in the multiparous animals, that the divergence between lines in viscera mass is retained after reproduction, whereas in non-manipulated populations, BMR (RMR) repeatability is lost after a reproductive bout (Duarte et al, 2010). Together, these findings provide support for the mechanism behind the assimilation capacity hypothesis for endothermy evolution in mammals (Koteja, 2000;Koteja, 2004) and highlight the significance and potential of long-term selection experiments in testing evolutionary scenarios.…”

“…All of these processes, from food processing to milk synthesis, manifest themselves as a systematic elevation of metabolic rates in reproducing animals severalfold above what is most often quantified as the basal (measured at rest, in a post-absorptive state and within the thermoneutral zone, in nonreproducing individuals) or resting (measured at rest) metabolic rate (BMR or RMR). This phenomenon of lactation-induced elevation of metabolic rate in various mammal species has been well documented (Duarte et al, 2010) and can be regarded as the manifestation of the metabolic costs of lactation.…”

Context-dependent correlation between resting metabolic rate and daily energy expenditure in wild chipmunks

“…The significant repeatability of DEE in eastern chipmunks raises the possibility that this trait is heritable and thus may respond to selection (see Bergeron et al, 2011a), or be genetically correlated with other traits such as animal personality (Careau et al, 2008;Careau and Garland, 2012). An increasingly large number of studies report that RMR is significantly repeatable (reviewed by Duarte et al, 2010;Larivée et al, 2010;Nespolo and Franco, 2007) and heritable (reviewed by Careau et al, 2011). Despite the fact that we made several repeated measures on a large number of chipmunks, RMR was not repeatable in our population (sensu Bozinovic, 2007;Russell and Chappell, 2007).…”

“…Repeatability in highly flexible traits should be expected only when the causes behind flexibility are controlled for (Naya, 2010) and our power to detect repeatability may have been diminished as our successive samples spanned reproductive events, seasons and years. Duarte and colleagues found that RMR was repeatable in female non-reproductive mice over a relatively long interval (110days), but was not repeatable when a reproductive event separated the measurements (Duarte et al, 2010), and this may also be the case for chipmunks. Food availability in the burrow, the intensity of torpor expression and the heat increment of feeding are some of the un-quantified conditions that may have affected RMR measurements.…”

Limits to sustained energy intake. XVI. Body temperature and physical activity of female mice during pregnancy

“…We have previously studied the responses to reproduction in the outbred MF1 mouse, focusing in particular on sustained energy intake in lactation (Duarte et al, 2010;Johnson et al, 2001b;Johnson and Speakman, 2001;Król et al, 2007;Król and Speakman, 2003a;Speakman and Król, 2011). In the current paper, we used this same model system to explore the patterns of change in food intake, body mass, thermoregulation and physical activity throughout pregnancy to establish the extent to which energy budgets in pregnancy may be compensated by changes in body temperature and physical activity.…”