The assimilation capacity (AC) hypothesis for the evolution of endothermy predicts that the maternal basal metabolic rate (BMR) should be positively correlated with the capacity for parental investment. In this study, we provide a unique test of the AC model based on mice from a long-term selection experiment designed to produce divergent levels of BMR. By constructing experimental families with cross-fostered litters, we were able to control for the effect of the mother as well as the type of pup based on the selected lines. We found that mothers with genetically determined high levels of BMR were characterized by higher parental investment capacity, measured as the offspring growth rate. We also found higher food consumption and heavier visceral organs in the females with high BMR. These findings suggested that the high-BMR females have higher energy acquisition abilities. When the effect of the line type of a foster mother was controlled, the pup line type significantly affected the growth rate only in the first week of life, with young from the high-BMR line type growing more rapidly. Our results support the predictions of the AC model.

Factors affecting contribution of spontaneous physical activity (SPA; activity associated with everyday tasks) to energy balance of humans are not well understood, as it is not clear whether low activity is related to dietary habits, precedes obesity or is a result of thereof. In particular, human studies on SPA and basal metabolic rates (BMR, accounting for >50% of human energy budget) and their associations with diet composition, metabolic thrift and obesity are equivocal. To clarify these ambiguities we used a unique animal model—mice selected for divergent BMR rates (the H-BMR and L-BMR line type) presenting a 50% between-line type difference in the primary selected trait. Males of each line type were divided into three groups and fed either a high fat, high carb or a control diet. They then spent 4 months in individual cages under conditions emulating human “sedentary lifestyle”, with SPA followed every month and measurements of metabolic risk indicators (body fat mass %, blood lipid profile, fasting blood glucose levels and oxidative damage in the livers, kidneys and hearts) taken at the end of study. Mice with genetically determined high BMR assimilated more energy and had higher SPA irrespective of type of diet. H-BMR individuals were characterized by lower dry body fat mass %, better lipid profile and lower fasting blood glucose levels, but higher oxidative damage in the livers and hearts. Genetically determined high BMR may be a protective factor against diet-induced obesity and most of the metabolic syndrome indicators. Elevated spontaneous activity is correlated with high BMR, and constitutes an important factor affecting individual capability to sustain energy balance even under energy dense diets.

Heat dissipation has been suggested as a limit to sustained metabolic effort, e.g. during lactation, when overheating is a possible risk. We tested this hypothesis using mice artificially selected for either high or low BMR that also differed with respect to parental effort. We used fixed size cross-fostered families and recorded litter mass daily until the 14th day of lactation. Midway through the experiment (day 8) half of the mothers from each group had fur from the dorsal body surface removed to increase their thermal conductance and facilitate heat dissipation. Our results showed that neither high nor low BMR mouse lines benefited from increasing their thermal conductance at peak lactation. On the contrary, growth of the litters reared by the low BMR females was compromised. Thus, our results do not support the heat dissipation limitation hypothesis.

From an evolutionary perspective, the high basal metabolic rate (BMR) of homeotherms is hypothesised to be a by-product of natural selection for effective parental care. We estimated daily milk output during two consecutive lactation bouts in mice divergently selected for high/low BMR and applied a cross-fostered design to control for potential differences in the between-line suckling abilities of nursed juveniles. Additionally, to remedy the potential limitation imposed by the ability of mother mice to dissipate excess heat, we exposed them to an ambient temperature of 17°C during the most energetically demanding second week of lactation. We found that the mice selected for high BMR produced significantly more milk in a 24 h period in both reproductive bouts. The milk samples obtained from the high BMR females had lower protein concentration and did not differ with respect to fat. However, the concentration of the primary milk carbohydrate -lactose -was higher. Although all the above between-line differences were statistically significant, their magnitude was too small to unambiguously ascribe them as stemming from a positive genetic correlation between the physiological traits underlying BMR and lactation performance. Nevertheless, our study lends such support at least at the level of phenotypic variation.

Artificial selection experiments are an effective tool for testing evolutionary hypotheses, because they allow one to separate genetic and environmental variances of the phenotype. However, it is unclear whether trait divergence typically selected early in life persists over an animal's life and altered physiological states, such as reproduction. Here we analyzed the long-term consistency of the between-line type divergence in basal metabolic rate (BMR) selected at 12 wk of age in laboratory mice. We measured BMR in nonreproducing and reproducing females at the age of 22 wk and then at 27 wk of age. Our results show that within both the reproducing group and the control group, the between-line type separation in BMR is consistently retained over time and reproductive status. Metabolically active internal organs (heart, liver, kidneys, and small intestine) also consistently differed in size between the two line types with no significant long-term effect of reproduction. The observed consistency of the between-line type divergence in BMR suggests the existence of the persistent effect of the selection on metabolic traits applied early in life. Moreover, BMR variation achieved by means of artificial selection is considerably higher than that found in natural/unmanipulated populations. The latter may therefore be characterized by insufficient variance to statistically resolve correlations involving BMR.