Evolution of Basal Metabolic Rate and Organ Masses in Laboratory Mice

Abstract

Animal species of similar body mass vary widely in basal metabolic rate (BMR). A central problem of evolutionary physiology concerns the anatomical/physiological origin and functional significance of that variation. It has been hypothesized that such interspecific differences in wild animals evolved adaptively from differences in relative sizes of metabolically active organs. In order to minimize confounding phenotypic effects and maximize relevant genetic variation, we tested for intraspecific correlations between body-mass-corrected BMR and masses of four organs (heart, kidney, liver, and small intestine) among six inbred strains of mice. We found significant differences between strains in BMR and in masses of all four organs. Strains with exceptionally high (or low) BMR tended to have disproportionately large (or small) organs. The mass of each organ was correlated with the masses of each of the other three organs. Variation in organ masses accounted for 52% of the observed variation in BMR, of which 42% represented between-strain variation, and 10% represented within-strain variation. This conclusion is supported by published measurements of metabolic rates of tissue slices from the four organs. The correlation between BMR and intestine or heart mass arose exclusively from differences between strains, while the correlation between BMR and liver or kidney mass also appeared in comparing individual mice within the same strain. Thus, even though the masses of the four examined organs account for no more than 17% of total body mass, their high metabolic activities or correlated factors account for much of the variation in BMR among mice. We suggest that large masses of metabolically active organs are subject to natural selection through evolutionary trade-offs. On the one hand, they make possible high-energy budgets (advantageous under some conditions), but on the other hand they are energetically expensive to maintain.

Variability in metabolic rate, feed intake and fatness among selection and inbred lines of mice

“…The larger livers and hearts of MH compared with ML mice were probably needed to accommodate the increased energy intake and expenditure of the MH line. This finding is consistent with results of Konarzewski and Diamond (1995), who reported that strains of mice with high resting metabolic rates also tended to have large organs. The MH and ML lines described here and elsewhere ) offer a unique model for future investigation of the regulation of energy utilization and fat deposition.…”

Maximum Daily Energy Intake: It Takes Time to Lift the Metabolic Ceiling

“…First, BMR is often regarded as a reference value in metabolic studies against which other measures of metabolism are compared (Blaxter 1989). Second, a portion of BMR is caused by the metabolism of the energy acquisition machinery, and BMR is therefore thought to reflect the capacity of this energy acquisition machinery (Daan et al 1990;Konarzewski and Diamond 1995;Speakman and McQueenie 1996). We did not measure basal metabolism during our experiment.…”

Associations between basal metabolic rate and reproductive performance in C57BL/6J mice

“…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 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 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.…”