The quantitative genetics of sustained energy budget in a wild mouse

We explored how morphological and physiological traits associated with energy expenditure over long periods of cold exposure would be integrated in a potential response to natural selection in a wild mammal, Phyllotis danwini. In particular, we studied sustained energy expenditure (SusMR), the rate of expenditure fueled by concurrent energy intake, basal metabolic rate (BMR), and sustained metabolic scope (SusMS = SusMR/BMR), a measure of the reserve for sustained work. We included the masses of different central processing organs as an underlying factor that could have a mechanistic link with whole animal traits. Only the liver had heritability statistically different from zero (0.73). Physiological and morphological traits had high levels of specific environmental variance (average 70%) and postnatal common environmental variance (average 30%) which could explain the low heritabilities estimates. Our results, (1) are in accordance with previous studies in mammals that report low heritabilities for metabolic traits (SusMR, BMR, SusMS), (2) but not completely with previous ones that report high heritabilities for morphological traits (masses of central organs), and (3) provide important evidence of the relevance of postnatal common environmental variance to sustained energy expenditure.     

Anatomic and energetic correlates of divergent selection for basal metabolic rate in laboratory mice

The aerobic capacity model postulates that high basal metabolic rates (BMR) associated with endothermy evolved as a correlated response to the selection on maximum, peak metabolic rate Vo2max. Furthermore, the model assumes that BMR and Vo2max are causally linked, and therefore, evolutionary changes in their levels cannot occur independently. To test this, we compared metabolic and anatomical correlates of selection for high and low body mass-corrected BMR in males of laboratory mice of F18 and F19 selected generations. Divergent selection resulted in between-line difference in BMR equivalent to 2.3 phenotypic standard deviation units. Vo2max elicited by forced swimming in 20 degrees C water was higher in the low BMR than high BMR line and did not differ between the lines when elicited by exposure to heliox at -2.5 degrees C. Moreover, the magnitude of swim- and heliox-induced hypothermia was significantly smaller in low BMR mice, whereas their interscapular brown adipose tissue was larger than in high BMR mice. Our results are therefore at variance with the predictions of aerobic capacity model. The selection also resulted in correlated response in food consumption (C) and masses of metabolically active internal organs: kidneys, liver, small intestine, and heart, which fuel maximum, sustained metabolic rate (SusMR) rather than Vo2max. These correlated responses were strong enough to claim the existence of positive, genetic correlations between BMR and the mass of viscera as well as C. Thus, our findings support the suggestion that BMR evolved as a correlated response to selection for SusMR, not Vo2max. In functional terms BMR should therefore be interpreted as a measure of energetic costs of maintenance of metabolic machinery necessary to sustain high levels of energy assimilation rate.     

黑线仓鼠繁殖输出与基础代谢率的关系

为了解黑线仓鼠繁殖输出与基础代谢率(BMR)的关系,阐明最大持续能量收支(SusMR)的限制水平, 揭示哺乳期能量收支对策,本文测定了哺乳期黑线仓鼠的体重、摄食量、BMR 和身体组成,以及哺乳期的胎仔数、胎仔重和泌乳能量支出(MEO)。结果显示,黑线仓鼠哺乳期体重降低了15.0 ± 0.8% , 摄食量显著增加, 哺乳高峰期平均摄食量为13.9 ± 0.3 g /d, 摄入能为222.1 ± 5.3 kJ/ d, 比哺乳初期增加121% , 比对照组高288% ;哺乳高峰期MEO 为62.4 ± 2.3 kJ/ d, 哺乳末期BMR 为49.7 ± 1.1 kJ/ d; 断乳时平均胎仔数4.7 ± 0.2、窝胎仔重50.5 ±1.6 g; 哺乳末期BMR 比对照组增加48% ,BMR 与消化系统各器官的相关性高于对照组; BMR 与胎仔数、胎仔重、乳腺重量和MEO 显著正相关。结果表明:初次繁殖的黑线仓鼠哺乳期SusMR 限制为4.47 ×BMR, 在自身维持和繁殖输出之间采取了“权衡分配”的原则,通过体重降低以减少BMR 的增加幅度, 从而有利于繁殖输出。     

Metabolic compensation during high energy output in fasting, lactating grey seals (Halichoerus grypus): metabolic ceilings revisited

Lactation is the most energetically expensive period for female mammals and is associated with some of the highest sustained metabolic rates (SusMR) in vertebrates (reported as total energy throughput). Females typically deal with this energy demand by increasing food intake and the structure of the alimentary tract may act as the central constraint to ceilings on SusMR at about seven times resting or standard metabolic rate (SMR). However, demands of lactation may also be met by using a form of metabolic compensation such as reducing locomotor activities or entering torpor. In some phocid seals, cetaceans and bears, females fast throughout lactation and thus cannot offset the high energetic costs of lactation through increased food intake. We demonstrate that fasting grey seal females sustain, for several weeks, one of the highest total daily energy expenditures (DEE; 7.4 x SMR) reported in mammals, while progressively reducing maintenance metabolic expenditures during lactation through means not explained by reduction in lean body mass or behavioural changes. Simultaneously, the energy-exported in milk is progressively increased, associated with increased lipoprotein lipase activity in the mammary gland, resulting in greater offspring growth. Our results suggest that females use compensatory mechanisms to help meet the extraordinary energetic costs of lactation. Additionally, although the concepts of SusMR and ceilings on total DEE may be somewhat different in fasting lactating species, our data on phocid seals demonstrate that metabolic ceilings on milk energy output, in general, are not constrained by the same kind of peripheral limitations as are other energy-consuming tissues. In phocid seals, the high ceilings on DEE during lactation, coupled with metabolic compensation, are undoubtedly important factors enabling shortened lactation.     

动物长期能量收支理论及研究进展

阐述了持续代谢率和持续代谢范围的概念,并介绍有关制约因子的４种假说：食物可利用性假说、外周制约假说、中心制约假说以及同形态椹制约假说。此外,还就持续代谢率的进化原因、实验验证的方法和结论,以及与最小维持消耗（ＢＭＲ）的关系和机制进行了分析。持续代谢率对动物生活具有影响,具有生态学意义。最后,分析了本领域未来的４个发展方向。     

Intraspecies variation in avian energy expenditure: correlates and constraints

Data on energy expenditure by 553 individuals of 28 species of small bird (10–150 g) are presented. All estimates of energy expenditure were obtained using the doubly-labelled water technique. Intraspecies variation in daily energy expenditure was found to be positively correlated with brood provisioning rates, percentage of time flying and the frequency of non-resting activity. Correlations were also shown with body-mass, body-size and several environmental factors. Published data on basal metabolic rates (BMR) sometimes differed substantially from estimates either made specifically as part of the studies considered here or calculated from allometric equations. For the purpose of interspecific comparisons, specific estimates of BMR are to be preferred. When expressed as a function of BMR, energy expenditures of free-living birds ranged from 1 + to 7 + times BMR with a mode at 3 +. Values of daily energy expenditure exceeding 4 times BMR were found in up to 48% of species and 30% of individuals, so that, contrary to earlier suggestions, 4 times BMR is not a universal upper limit to the sustained work rate of small birds. Observed upper limits tended to be higher in species with energy-expensive foraging habits. Energy expended by breeding birds is likely to involve a balance between the benefits a greater expenditure has for offspring production and any fitness penalty associated with the high level of energy expediture which nest provisioning involves.     

长爪沙鼠的代谢率与器官的关系

我们测定了野生长爪沙鼠（Meriones unguiculatus)的基础代谢率和冷诱导的最大代谢率,分析了动物体内11种器官或组织的大小与代谢率的关系。长爪沙鼠的基础代谢率为118.10mlO2/h,最大代谢率为659.83mlO2/h。经过残差分析表明,基础代谢率并不与任何一种器官或组织相关,而最大代谢率与小肠湿重（n=20,r=-0.478,P=0.033)和消化道全长（n=20,r=-0.487,P=0.030)显著相关,表明体内器官重量的差别并不是造成种内基础代谢率差别的原因;体内存在着与最大代谢率相关的“代谢机器”,消化系统（特别是小肠）是这一代谢机器的重要组成部分,但代谢机器的大小并不能通过基础代谢率反映出来。基础代谢率与最大代谢率不相关,因此不支持“较高的基础代谢率能够产生较高的非基础代谢率（最大代谢率等）”的假设。     

The energetic and survival costs of growth in free-ranging chipmunks

The growth/survival trade-off is a fundamental aspect of life-history evolution that is often explained by the direct energetic requirement for growth that cannot be allocated into maintenance. However, there is currently no empirical consensus on whether fast-growing individuals have higher resting metabolic rates at thermoneutrality (RMRt) than slow growers. Moreover, the link between growth rate and daily energy expenditure (DEE) has never been tested in a wild endotherm. We assessed the energetic and survival costs of growth in juvenile eastern chipmunks (Tamias striatus) during a year of low food abundance by quantifying post-emergent growth rate (n = 88), RMRt (n = 66), DEE (n = 20), and overwinter survival. Both RMRt and DEE were significantly and positively related to growth rate. The effect size was stronger for DEE than RMRt, suggesting that the energy cost of growth in wild animals is more likely to be related to the maintenance of a higher foraging rate (included in DEE) than to tissue accretion (included in RMRt). Fast growers were significantly less likely to survive the following winter compared to slow growers. Juveniles with high or low RMRt were less likely to survive winter than juveniles with intermediate RMRt. In contrast, DEE was unrelated to survival. In addition, botfly parasitism simultaneously decreased growth rate and survival, suggesting that the energetic budget of juveniles was restricted by the simultaneous costs of growth and parasitism. Although the biology of the species (seed-storing hibernator) and the context of our study (constraining environmental conditions) were ideally combined to reveal a direct relationship between current use of energy and future availability, it remains unclear whether the energetic cost of growth was directly responsible for reduced survival.     

High Energy Digestion Efficiency and Altered Lipid Metabolism Contribute to Obesity in BFMI Mice

To constitute a valuable resource to identify individual genes involved in the development of obesity, a novel mouse model, the Berlin Fat Mouse Inbred line 860 (BFMI860), was established. In order to characterize energy intake and energy expenditure in obese BFMI860 mice, we performed two independent sets of experiments in male BFMI860 and B6 control mice (10 per line). In experiment 1, we analyzed body fat content noninvasively by dual‐energy X‐ray absorptiometry and measured resting metabolic rate at thermoneutrality (RMRt) and respiratory quotient (RQ) in week 6, 10, and 18. In a second experiment, energy digested (energy intake minus fecal energy loss) was determined by bomb calorimetry from week 6 through week 12. BFMI860 mice were heavier and had higher fat mass (final body fat content was 24.7% compared with 14.6% in B6). They also showed fatty liver syndrome. High body fat accumulation in BFMI860 mice was restricted to weeks 6–10 and was accompanied by hyperphagia, higher energy digestion, higher RQs, and abnormally high blood triglyceride levels. Lean mass–adjusted RMRt was not altered between lines. These results indicate that in BFMI860 mice, the excessive accumulation of body fat is associated with altered lipid metabolism, high energy intake, and energy digestion. Assuming that BFMI860 mice and their obese phenotypes are of polygenic nature, this line is an excellent model for the study of obesity in humans, especially for juvenile obesity and hyperlipidemia.     

Expanding the body mass range: associations between BMR and tissue morphology in wild type and mutant dwarf mice (<Emphasis Type="Italic">David</Emphasis> mice)

We sought to identify associations of basal metabolic rate (BMR) with morphological traits in laboratory mice. In order to expand the body mass (BM) range at the intra-strain level, and to minimize relevant genetic variation, we used male and female wild type mice (C3HeB/FeJ) and previously unpublished ENU-induced dwarf mutant littermates (David mice), covering a body mass range from 13.5 g through 32.3 g. BMR was measured at 30°C, mice were killed by means of CO₂ overdose, and body composition (fat mass and lean mass) was subsequently analyzed by dual X-ray absorptiometry (DEXA), after which mice were dissected into 12 (males) and 10 (females) components, respectively. Across the 44 individuals, 43% of the variation in the basal rates of metabolism was associated with BM. The latter explained 47% to 98% of the variability in morphology of the different tissues. Our results demonstrate that sex is a major determinant of body composition and BMR in mice: when adjusted for BM, females contained many larger organs, more fat mass, and less lean mass compared to males. This could be associated with a higher mass adjusted BMR in females. Once the dominant effects of sex and BM on BMR and tissue mass were removed, and after accounting for multiple comparisons, no further significant association between individual variation in BMR and tissue mass emerged. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Do the high energy lifestyles of shorebirds result in high maximal metabolic rates? Basal and maximal metabolic rates in least and pectoral sandpipers during migration

Shorebirds have high resting and field metabolic rates relative to many other bird groups, and this is posited to be related to their high‐energy lifestyle. Maximum metabolic outputs for cold or exercise are also often high for bird groups with energetically demanding lifestyles. Moreover, shorebirds demonstrate flexible basal and maximal metabolic rates, which vary with changing energy demands throughout the annual cycle. Consequently, shorebirds might be expected to have high maximum metabolic rates, especially during migration periods. We captured least Calidris minutilla and pectoral C. melanotos sandpipers during spring and fall migration in southeastern South Dakota and measured maximal exercise metabolic rate (MMR; least sandpipers only), summit metabolic rate (M_sum, maximal cold‐induced metabolic rate) and basal metabolic rate (BMR, minimum maintenance metabolic rate) with open‐circuit respirometry. BMR for both least and pectoral sandpipers exceeded allometric predictions by 3–14%, similar to other shorebirds, but M_sum and MMR for both species were either similar to or lower than allometric predictions, suggesting that the elevated BMR in shorebirds does not extend to maximal metabolic capacities. Old World shorebirds show the highest BMR during the annual cycle on the Arctic breeding grounds. Similarly, least sandpiper BMR during migration was lower than on the Arctic breeding grounds, but this was not the case for pectoral sandpipers, so our data only partially support the idea of similar seasonal patterns of BMR variation in New World and Old World shorebirds. We found no correlations of BMR with either M_sum or MMR for either raw or mass‐independent data, suggesting that basal and maximum aerobic metabolic rates are modulated independently in these species.     

A strong response to selection on mass-independent maximal metabolic rate without a correlated response in basal metabolic rate

Metabolic rates are correlated with many aspects of ecology, but how selection on different aspects of metabolic rates affects their mutual evolution is poorly understood. Using laboratory mice, we artificially selected for high maximal mass-independent metabolic rate (MMR) without direct selection on mass-independent basal metabolic rate (BMR). Then we tested for responses to selection in MMR and correlated responses to selection in BMR. In other lines, we antagonistically selected for mice with a combination of high mass-independent MMR and low mass-independent BMR. All selection protocols and data analyses included body mass as a covariate, so effects of selection on the metabolic rates are mass adjusted (that is, independent of effects of body mass). The selection lasted eight generations. Compared with controls, MMR was significantly higher (11.2%) in lines selected for increased MMR, and BMR was slightly, but not significantly, higher (2.5%). Compared with controls, MMR was significantly higher (5.3%) in antagonistically selected lines, and BMR was slightly, but not significantly, lower (4.2%). Analysis of breeding values revealed no positive genetic trend for elevated BMR in high-MMR lines. A weak positive genetic correlation was detected between MMR and BMR. That weak positive genetic correlation supports the aerobic capacity model for the evolution of endothermy in the sense that it fails to falsify a key model assumption. Overall, the results suggest that at least in these mice there is significant capacity for independent evolution of metabolic traits. Whether that is true in the ancestral animals that evolved endothermy remains an important but unanswered question.     

黑线仓鼠的BMR个体差异及其应对高脂食物的能量学对策

为探讨高脂食物对小型哺乳动物能量代谢的影响及其与基础代谢率(Basal metabolic rate, BMR)的关系,将成年雌性黑线仓鼠(Cricetulus barabensis)分为高、低BMR组,每组再随机分为低脂、高脂食物组,驯化6周后,测定体重、摄入能和代谢率,以及消化酶活力、褐色脂肪组织(Brown adipose tissue, BAT)和主要内脏器官与肌肉的细胞色素c氧化酶(Cytochrome c oxidase, COX)活性、解偶联蛋白(Uncoupling protein, UCP) mRNA表达等。结果显示,高脂食物对高、低BMR组动物体重均无显著影响。与低脂食物组相比,高脂食物组的摄食量、摄入能和消化能显著下降,小肠脂肪酶活力显著增强,消化率明显增加,但高、低BMR组的组间差异不显著。夜间代谢水平显著高于昼间,高脂食物使高BMR组的夜间代谢率显著升高。BAT、肌肉和内脏器官COX活性不受高脂食物的影响,高、低BMR组的组间差异也不显著。高脂食物组仅肝脏UCP2表达显著上调。结果表明,能量摄入和消化系统形态及功能的可塑性调节是黑线仓鼠应对高脂食物的主要策略;黑线仓鼠的代谢率具有显著的昼夜节律,既受高脂食物的影响,也与动物自身的BMR水平有关,但UCP表达具有组织特异性,这可能不是导致BMR个体差异的因素。     

Prolonged longevity in naked mole-rats: age-related changes in metabolism,body composition and gastrointestinal function

Aging is characterized by declines in all physiological processes and concomitant changes in body composition. Age-related changes in metabolism, body composition and gastrointestinal function were investigated in naked mole-rats (Heterocephalus glaber), rodents that exhibit extended longevity. Maximum lifespan of these 40 g rodents (>27 year) is approximately 9 times greater than predicted allometrically. We investigated changes in basal metabolic rate (BMR), body composition and intestinal glucose transport in 1, 5, 10 and 20-year-old male individuals. Body composition was measured using dual X-ray absorptiometry and activity of sodium glucose co-transporters (SGLT1) determined using everted gut sleeves. One-year-olds had lower body mass than other age cohorts, as they had not attained full adult form. Among the 5, 10, and 20-year-olds, no age-related changes in body mass, BMR, percentage body fat, fat-free mass or bone mineral density were found. SGLT1 activity declined moderately (<20%) from 5 to 20 years and was similar at 10-20 years, whereas age-related declines are 40-60% in mice. Although mole-rats have low metabolic rates, their prolonged longevity results in a lifetime energy expenditure more than 4 times that of mice. Since lifetime energy expenditure is an important index of potential exposure to oxidative damage, naked mole-rats may be valuable for studying mechanisms of aging.     

Variation in energy expenditure among black-legged kittiwakes: effects of activity-specific metabolic rates and activity budgets

We sought to determine the effect of variation in time-activity budgets (TABs) and foraging behavior on energy expenditure rates of parent black-legged kittiwakes (Rissa tridactyla). We quantified TABs using direct observations of radio-tagged adults and simultaneously measured field metabolic rates (FMR) of these same individuals (n=20) using the doubly labeled water technique. Estimated metabolic rates of kittiwakes attending their brood at the nest or loafing near the colony were similar (ca. 1.3 x basal metabolic rate [BMR]), although loafing during foraging trips was more costly (2.9 x BMR). Metabolic rates during commuting flight (7.3 x BMR) and prey-searching flight (6.2 x BMR) were similar, while metabolic rates during plunge diving were much higher (ca. 47 x BMR). The proportion of the measurement interval spent foraging had a positive effect on FMR (R2=0.68), while the combined proportion of time engaged in nest attendance and loafing near the colony had a negative effect on FMR (R2=0.72). Thus, more than two-thirds of the variation in kittiwake FMR could be explained by the allocation of time among various activities. The high energetic cost of plunge diving relative to straight flight and searching flight suggests that kittiwakes can optimize their foraging strategy under conditions of low food availability by commuting long distances to feed in areas where gross foraging efficiency is high.     

温州地区4种雀形目鸟类基础代谢率与器官重量的相关性分析

动物代谢率存在差异的原因及其意义是进化牛理学上的一个核心问题.为了解代谢率的影响因素和功能意义,测定了红头长尾山雀Aegithalos concinnus、白头鹎Pycnonotus sinensis、丝光椋鸟Stumus sericeus和小鸦Emberi-za pusilla的基础代谢率,分析了动物体内的8种器官或者组织的大小与代谢率的关系.结果显示,基础代谢率与脑、肝脏,.肾脏、胃、小肠和总消化道干重(胃、小肠与直肠的干重之和)相关显著.     

The energy economy of the arctic-breeding Kittiwake (Rissa tridactyla): a review

The present paper reviews recent studies on changes in body mass, body composition and rates of energy expenditure during the breeding season in the black-legged Kittiwake (Rissa tridactyla) on Svalbard (79 degrees N). The main characteristic of the energy budget is a pronounced decrease in body mass as well as basal metabolic rate (BMR) after the eggs have hatched. While most internal organs lose mass in direct proportion to the general decrease in body mass, the liver and kidney masses decrease to a disproportionately greater extent. Since both the liver and the kidney have high intrinsic metabolic rates, these results support an earlier notion that the reduction in body mass is an adaptation to reduce maintenance costs. Alternatively, the reduced BMR is due to a decrease in energy uptake from the gastrointestinal tract, thereby ensuring that undigested food is ready to be regurgitated to the chicks. At the end of the chick-rearing period, the field metabolic rate (FMR) reaches its highest level, probably due to an increased workload associated with chick feeding. This occurs at a time of low body mass and BMR. A pronounced increase in the metabolic scope (FMR/BMR) during the latter part of the chick-rearing period demonstrates that BMR and FMR may change independently of each other and that the ratio FMR/BMR may not be a good measure of energy stress.     

Anatomic and molecular correlates of divergent selection for basal metabolic rate in laboratory mice

Proximal mechanisms describing the evolution of high levels of basal metabolic rate (BMR) in endotherms are one of the most intriguing problems of evolutionary physiology. Because BMR mostly reflects metabolic activity of internal organs, evolutionary increase in BMR could have been realized by an increase in relative organ size and/or mass-specific cellular metabolic rate. According to the "membrane pacemaker" theory of metabolism, the latter is mediated by an increase in the average number of double bonds (unsaturation index) in cell membrane fatty acids. To test this, we investigated the effect of divergent artificial selection for body-mass-corrected BMR on the mass of internal organs and the fatty acid composition of cell membranes in laboratory mice (Mus musculus). Mice from the high-BMR line had considerably larger liver, kidneys, heart, and intestines. In contrast, the unsaturation index of liver cell membranes was significantly higher in low-BMR mice, mainly because of the significantly higher content of highly polyunsaturated 22 : 6 docosahexanoic fatty acid. Thus, divergent selection for BMR did not affect fatty acyl composition of liver and kidney phospholipids in the direction predicted by the membrane pacemaker theory. We conclude that an intraspecific increase in BMR may rapidly evolve mainly as a result of the changes in size of internal organs, without simultaneous increase of the unsaturation index in cell membrane lipids.     

Effects of body mass and reproduction on the basal metabolic rate of brown long-eared bats (Plecotus auritus)

We measured basal metabolic rate (BMR) of nonreproductive and of breeding (pregnant and lactating) female brown long-eared bats (Plecotus auritus) to investigate the effects of intra- and interindividual variation in body mass and of reproduction on metabolism. The BMR of six nonreproductive females was measured between five and seven times at approximately 2-wk intervals over a period of 2.5 mo. There was a highly significant effect (P<0.001) of body mass on BMR of these nonreproductive females. The pooled within-individual scaling exponent (1.88) significantly exceeded the established mammalian interspecific exponent (0.75). In addition, we made single observations on 14 nonreproductive females to establish the effects of differences in mass between individuals. The mean BMR across all 14 individuals was 82 mW (+/-24 SD). There was a significant positive relationship between BMR and body mass across these individuals (r2=0.39), with a between-individual scaling exponent of 0.75. Inter- and intraindividual effects of mass on BMR were combined in a regression analysis that included mean body mass and deviation from mean mass on any given day as predictors. This regression model explained 55% of the variation in BMR. We made longitudinal measurements of BMR throughout reproduction and compared these with the predicted BMR of nonreproductive bats of the same body mass. Reproductive females exhibited temporal flexibility in BMR. BMR during pregnancy increased on a whole-animal basis but was significantly lower (by, on average, 15%) than BMR predicted for nonreproductive females of the same mass. Over a period of 1-75 d following birth, whole-animal BMR was greater than that during pregnancy, even though body mass declined after parturition. Hence, postbirth BMR was greater than the level predicted for nonreproductive females of the same mass. This study indicates that the scaling of BMR with body mass differs significantly within and between individuals and that there is a reduction of BMR in pregnancy and an elevation of BMR during lactation.