Mice divergently selected for high and low basal metabolic rates evolved different cell size and organ mass.

Evolution of metabolic rates of multicellular organisms is hypothesized to reflect the evolution of their cell architecture. This is likely to stem from a tight link between the sizes of cells and nuclei, which are expected to be inversely related to cell metabolism. Here, we analysed basal metabolic rate (BMR), internal organ masses and the cell/nucleus size in different tissues of laboratory mice divergently selected for high/low mass-corrected BMR and four random-bred mouse lines. Random-bred lines had intermediate levels of BMR as compared to low- and high-BMR lines. Yet, this pattern was only partly consistent with the between-line differences in cell/nucleus sizes. Erythrocytes and skin epithelium cells were smaller in the high-BMR line than in other lines, but the cells of low-BMR and random-bred mice were similar in size. On the other hand, the size of hepatocytes, kidney proximal tubule cells and duodenum enterocytes were larger in high-BMR mice than other lines. All cell and nucleus sizes were positively correlated, which supports the role of the nucleus in cell size regulation. Our results suggest that the evolution of high BMR involves a reduction in cell size in specialized tissues, whose functions are primarily dictated by surface-to-volume ratios, such as erythrocytes. High BMR may, however, also incur an increase in cell size in tissues with an intense transcription and translation, such as hepatocytes.

Locomotor activity of mice divergently selected for basal metabolic rate: a test of hypotheses on the evolution of endothermy.

The aerobic capacity model postulates that high basal metabolic rates (BMR) underlying endothermy evolved as a correlated response to the selection on maximal levels of oxygen consumption (V(O(2)max)) associated with locomotor activity. The recent assimilation capacity model specifically assumes that high BMR evolved as a by-product of the selection for effective parental care, which required long-term locomotor activity fuelled by energy assimilated from food. To test both models, we compared metabolic and behavioural correlates in males of laboratory mice divergently selected on body mass-corrected BMR. V(O(2)max) elicited by running on the treadmill did not differ between selection lines, which points to the lack of genetic correlation between BMR and V(O(2)max). In contrast, there was a positive, genetic correlation between spontaneous long-term locomotor activity, food intake and BMR. Our results therefore corroborate predictions of the assimilation capacity model of endothermy evolution.

Trade-offs between activity and thermoregulation in a small carnivore, the least weasel Mustela nivalis.

We studied factors influencing daily energy expenditures (DEE) of male least weasels (Mustela nivalis) using the doubly labelled water technique. The relationship between ambient temperature and DEE formed a triangular pattern, characterized by invariance of the maximum DEE and an inverse relationship between minimum DEE and temperature. A simple energetic model relating the DEE of male weasels to activity time (AT) and ambient temperature predicted that, across seasons, less than 10 per cent of measurements approach the upper bound of observed DEE. Male weasels were able to maintain a relatively constant maximum energy output across varying temperatures by adjusting their AT to changes in temperature. They achieved maximum energy expenditures in winter due to high thermoregulatory costs, and in spring and summer due to high levels of physical activity. This pattern exemplifies a 'metabolic niche' of a small mammal having extremely high energy expenditures primarily driven by ambient temperature.

Cell size as a link between noncoding DNA and metabolic rate scaling.

Accumulation of noncoding DNA and therefore genome size (C-value) may be under strong selection toward increase of body size accompanied by low metabolic costs. C-value directly affects cell size and specific metabolic rate indirectly. Body size can enlarge through increase of cell size and/or cell number, with small cells having higher metabolic rates. We argue that scaling exponents of interspecific allometries of metabolic rates are by-products of evolutionary diversification of C-values within narrow taxonomic groups, which underlines the participation of cell size and cell number in body size optimization. This optimization leads to an inverse relation between slopes of interspecific allometries of metabolic rates and C-value. To test this prediction we extracted literature data on basal metabolic rate (BMR), body mass, and C-value of mammals and birds representing six and eight orders, respectively. Analysis of covariance revealed significant heterogeneity of the allometric slopes of BMR and C-value in both mammals and birds. As we predicted, the correlation between allometric exponents of BMR and C-value was negative and statistically significant among mammalian and avian orders.

Effect of food shortage on the physiology and competitive abilities of sand martin (Riparia riparia) nestlings.

We examined developmental and behavioural plasticity of sand martin (Riparia riparia) nestlings hand-reared under laboratory conditions. We created six broods of six 4-day-old nestlings and randomly assigned them to one of the two following feeding regimens, each lasting for 3 days: (1) all nestmates fed a similar, limited amount of food (FR nestlings). This simulated synchronous hatching under conditions of food restriction. (2) Half the brood were food-restricted (FR/AL nestlings), and half were fed ad libitum (AL nestlings), as in asynchronously hatched broods with differential food allocation. Under both regimens, food restriction resulted in a reduction in body mass, intestinal mass, pectoral muscle mass, fat reserves, body temperature and resting metabolic rate (RMR). However, it simultaneously triggered a significant increase in intestinal uptake rates of L-proline and locomotor activity, quantified as frequency of crawling into the artificial nest tunnel by individual nestlings. Locomotor activity and intestinal uptake rates of L-proline by FR nestlings were higher than those of FR/AL young, while body temperature and RMR of FR nestlings were lower. We conclude that food-restricted nestlings responded actively to food shortages by upregulating their gut function, reducing the energy costs of maintenance and increasing locomotor activity. These behavioural and physiological responses were strongest in broods of similar-sized FR nestlings, which can be interpreted as an escalation of sibling competition. Thus, developmental and behavioural plasticity may be an important factor in the evolution of sibling rivalry.

Effects of food shortage and oversupply on energy utilization, histology, and function of the gut in nestling song thrushes (Turdus philomelos).

We measured food intake, digestive efficiency, body mass increments, resting metabolic rate (RMR), carcass fat content, size and histological structure of the gut, and the rate of intestinal brush border uptake of l-proline in song thrush (Turdus philomelos) nestlings subjected to food shortage or food surplus under laboratory conditions. We assigned nestlings between 3 and 7 d of age to one of the following treatments: (1) food restriction, which resulted in a slowed growth at the rate found in undernourished, wild nestlings; (2) overfeeding, which totally suppressed begging; and (3) intermediate feeding. Threefold differences in energy consumption caused fivefold differences in body mass increments of the nestlings. Despite this, body mass-corrected RMR and intestinal mass were not affected by the feeding regime. The energy content of fecal output was highest in food-restricted birds, while their carcass fat content was lowest among treatment groups. Intestinal uptake rates of l-proline were low in the overfed and intermediate-fed young but significantly increased in the food-restricted birds, who attempted to maximize their rates of growth and development within the restrictive limits set by feeding regime. We noted a marked decrease of intestinal villi height in overfed birds as compared to intermediate-fed and food-restricted nestlings. We conclude that song thrush nestlings are characterized by a limited plasticity of their developmental program, which prohibits overfed nestlings from significantly up-regulating their gut function to accommodate increased food intake. This suggests that they already grew at a rate close to their physiological maximum. We suggest two interpretations: (1) under natural conditions, song thrush nestlings do not face frequent, unpredictable fluctuations in food abundance that could select for developmental plasticity, or (2) strong selection for uniform adult phenotypes prevents flexible developmental trajectories, which would result in a diversity of adult phenotypes.

Metabolic and organ mass responses to selection for high growth rates in the domestic chicken (Gallus domesticus).

Evolutionary hypotheses suggest that higher rates of postembryonic development in birds should either lower the resting metabolic rate (RMR) in a trade-off between the costs of growth and maintenance or increase RMR because of a buildup of metabolic machinery. Furthermore, some suggest that higher rates of postembryonic development in birds should reduce peak metabolic rate (PMR) through delayed tissue maturation and/or an increased energy allocation to organ growth. We studied this by comparing metabolic rates and organ sizes of fast-growing meat-type chickens (broilers) with those of birds from a laying strain, which grow much slower. During the first week of life, despite growing six times faster, the RMR of the broiler chickens was lower than that of birds of the laying strain. The difference between strains in RMR disappeared thereafter, even though broilers continued to grow twice as fast as layers. The differences between strains in growth rate during the first week after hatching were not reflected in similar differences in the relative masses of the heart, liver, and small intestine. However, broilers had heavier intestines once they reached a body mass of 80 g. In contrast, broilers had relatively smaller brains than did layers. There was a positive correlation, over both strains, between RMR and the masses of leg muscles, intestine, and liver. Furthermore, despite delayed maturation of muscle tissue, broilers exhibited significantly higher PMR. We hypothesize that a balance between the larger relative muscle mass but lower muscle maturation level explains this high PMR. Another correlation, between leg muscle mass and PMR, partly explained the positive correlation between RMR and PMR.

Analgesia in selectively bred mice exposed to cold in helium/oxygen atmosphere.

In order to evaluate the stressing role of swim hypothermia in producing swim stress-induced analgesia (SSIA), we examined whether a mere decrease in the animals' core temperature without swimming would be sufficient to elicit analgesia. The subjects were Swiss-Webster mice selectively bred for 37 and 40 generations for divergent magnitudes of SSIA. High (HA) and low analgesia (LA) mice were exposed for 15 min to temperatures in the range between -5 and +20 degrees C in 79% He/21% O2 (Heliox) atmosphere. The Heliox exposure produced ambient temperature-dependent hypothermia and analgesia, as assessed with a hot-plate test (56 degrees C). The post-Heliox analgesia was of much higher magnitude in HA than in LA mice. The steeper slope of regression of the magnitude of analgesia upon hypothermia in HA mice indicates that these mice are far more sensitive to the analgesic effect of hypothermia than LA mice. Naltrexone HCl (10 mg/kg i.p.) attenuated analgesia in ambient temperature-dependent manner in HA, but not in LA mice. In view of the apparent similarity of Heliox-induced analgesia and SSIA we suggest that hypothermia is a powerful component of swim stress to induce SSIA in the mouse.

Metabolic correlates of selection for swim stress-induced analgesia in laboratory mice.

The upper limits of metabolic rates and the links between maximal and resting metabolic rates in vertebrates have recently received a lot of attention, mainly due to their possible relationship to the evolution of endothermy. We measured peak metabolic rates during 3 min swimming in 20 degrees C water (Vo2swim), maximal metabolic rate (Vo2max) in -2.5 degrees C Helox, and basal metabolic rate (BMR) in two lines of mice selected for high (HA) and low (LA) swim stress-induced analgesia (SSIA). We found that exercise combined with heat loss used for producing SSIA also acted as a selection agent, resulting in a 15% HA/LA line difference in Vo2swim. Core body temperature of HA mice (characterized by lower Vo2swim) was also on average 3.2 degrees C lower than that of LA mice. Furthermore, Vo2max of HA mice was lower than that of LA mice by 8% and accompanied by larger hypothermia. Thus mice with exceptionally high (or low) Vo2max tended to have exceptionally high (or low) Vo2swim, resulting in a positive correlation between Vo2swim and Vo2max. All these suggest that selection for SSIA produced genetically correlated responses in both Vo2swim and Vo2max. However, we did not observe HA/LA differences in BMR. Hence, changes in resting and maximum metabolic rates are not necessarily correlated. We hypothesize that the lack of such a correlation was partially due to the modulation of metabolic responses by SSIA.