Daily variation of thermoregulatory costs in laboratory mice selected for high and low basal metabolic rate

Most mammals are known to have clear circadian rhythms of body temperature (T_b) and metabolic rate. Large parts of the rhythms correspond to the oscillation of nonshivering thermogenesis (NST), dependent on visceral organ mass, and, affected by mass of brown adipose tissue (BAT). I tested whether: (1) a different levels of BMR result in respective changes of T_b values and the magnitude of daily RMR oscillations both within and below thermoneutrality; (2) the amplitude of daily variation of RMR depends on ambient temperature (T_a). I studied: (1) daily variation of body temperature at T_a of 23 °C, and (2) the rate of resting metabolism (RMR) within and below thermoneutrality at the time of minimum and increasing T_b (minimum and maximum NST capacity), in two lines of laboratory mice subjected to divergent, artificial selection toward high (HBMR) and low (LBMR) basal rate of metabolism (BMR). All mice had a clear circadian rhythm of T_b with minimum of 36.4±0.2 °C at 7:00 and maximum of 37.8±0.2 °C at 21:00. Their RMR measured below thermoneutrality exhibited significant daily variation, with the maximum between 16:00 and 19:00, when T_b was rising. Within thermoneutral zone (TNZ) I found between-line, but not between-time, differences in RMR. All between-line differences in RMR could be explained by the magnitude of BMR. I did not find any between-line differences of RMR value in temperatures below thermoneutrality. The amplitude of daily variation of RMR measured below TNZ depended neither on the T_a value nor on level of BMR (or visceral organs).     

小鼠基础代谢率与繁殖输出和繁殖期末器官的关系

以封闭式流体压力呼吸计测定KM小鼠(Mus musculus)的基础代谢率(BMR);采用残差分析和Pearson相关分析检验BMR与繁殖输出、内脏器官的相关性。哺乳末期BMR显著高于繁殖前,繁殖前BMR与繁殖输出不相关,但哺乳末期BMR与体重、摄食量、胎仔数和胎仔重、内脏器官和消化道显著正相关;与消化道器官的相关性高于其他内脏器官。研究结果支持"哺乳期较高的BMR有利于消化系统增强消化和吸收能力,以增加能量摄入用于繁殖输出"的假设。     

食物限制对黑线仓鼠能量代谢和产热的影响

为阐明动物应对食物短缺的能量学对策与其自身的代谢水平的关系,测定了不同限食程度下黑线仓鼠的体重、基础代谢率和非颤抖性产热。结果发现,限食使基础代谢率、非颤抖性产热、褐色脂肪组织细胞色素c氧化酶活性降低。90% 限食驯化4 周后,存活率为80% ,60% 限食驯化4 周后,存活率为30% 。低温驯化使黑线仓鼠基础代谢率和非颤抖性产热显著增加,使80% 限食动物的体重和存活率显著降低。高基础代谢率组的摄食量比低基础代谢率组多23.8% ,80% 限食后两组体重降低的幅度和存活率差异不显著。结果表明:高水平的代谢率使黑线仓鼠对食物资源短缺的敏感性增加;支持“代谢率转换假说”,符合“具有储食习性的动物对食物短缺的生理耐受性较低” 的预测。     

随机饥饿和重喂食对小鼠能量代谢和行为的影响

为阐明能量代谢和行为的可塑性对动物适应食物资源变化的意义,将成年雄性KM 小鼠随机饥饿驯化4
周,再重喂食驯化4 周。采用食物平衡法测定摄食量、封闭式流体压力呼吸计测定基础代谢率(BMR) 和非颤
抖性产热(NST)、观察法测定行为。随机饥饿使摄食量、消化道重量显著增加,BMR 和NST 显著降低。与对照
组相比,饥饿组休息行为显著增加,活动显著降低。重喂食后,上述指标均恢复到对照组水平,表现出显著的
可塑性。研究结果表明,动物适应难以预测的食物资源短缺的主要策略包括:增加自由取食期间的摄食量;降
低BMR、NST 和活动行为,从而保存身体贮存的能量。能量代谢和活动行为在较短的时间尺度内表现出显著的
可塑性对小鼠适应不可预测的食物资源短缺的应激环境具有重要意义。     

When nonshivering thermogenesis equals maximum metabolic rate: thermal acclimation and phenotypic plasticity of fossorial Spalacopus cyanus (Rodentia)

Many small mammals inhabiting fluctuating and cold environments display enhanced capacity for seasonal changes in nonshivering thermogenesis (NST) and thermoregulatory maximum metabolic rate (MMR). However, it is not known how this plasticity remains in a mammal that rarely experiences extreme thermal fluctuations. In order to answer this question, we determined body mass (m(b)), basal metabolic rate (BMR), NST, MMR, and minimum thermal conductance (C) on a Chilean fossorial caviomorph (Spalacopus cyanus) from a coastal population, acclimated to cold (15 degrees C) and warm (30 degrees C) conditions. NST was measured as the maximum response of metabolic rate (NST(max)) after injection of norepinephrine (NE) in thermoneutrality minus BMR. Maximum metabolic rate was assessed in animals exposed to enhanced heat-loss atmosphere (He-O2) connected with an open-flow respirometer. Body mass and metabolic variables increased significantly after cold acclimation with respect to warm acclimation but to a low extent (BMR, 26%; NST, 10%; and MMR, 12%). However, aerobic scope (MMR/BMR), calculated shivering thermogenesis (ST), and C did not change with acclimation regime. Our data suggest that physiological plasticity of S. cyanus is relatively low, which is in accordance with a fossorial mode of life. Although little is known about MMR and NST in fossorial mammals, S. cyanus has remarkably high NST; low MMR; and surprisingly, a nil capacity of ST when compared with other rodents.     

Is BMR repeatable in deer mice? Organ mass correlates and the effects of cold acclimation and natal altitude

Basal metabolic rate (BMR) is probably the most studied aspect of energy metabolism in vertebrate endotherms. Numerous papers have explored its mass allometry, phylogenetic and ecological relationships, and ontogeny. Implicit in many of these studies (and explicit in some) is the view that BMR responds to selection, which requires repeatability and heritability. However, BMR is highly plastic in response to numerous behavioral and environmental factors and there are surprisingly few data on its repeatability. Moreover, the mechanistic underpinnings of variation in BMR are unclear, despite considerable research. We studied BMR repeatability in deer mice (Peromyscus maniculatus) across intervals of 30–60 days, and also examined the influence of birth altitude (3,800 m versus 340 m) and temperature acclimation (to ∼5 or ∼20°C) on BMR, and the relationship between BMR and organ size. Neither acclimation temperature nor natal altitude alone influenced BMR, but the combination of birth at high altitude and cold acclimation significantly increased BMR. Few visceral organ masses were correlated to BMR and most were inconsistent across natal altitudes and acclimation temperatures, indicating that no single organ ‘controls’ variation in BMR. In several treatment groups, the mass of the ‘running motor’ (combined musculoskeletal mass) was negatively correlated to BMR and the summed mass of visceral organs was positively correlated to BMR. We found no repeatability of BMR in any treatment group. That finding—in sharp contrast to high repeatability of BMR in several other small endotherms—suggests little potential for direct selection to drive BMR evolution in deer mice.     

Quantitative genetics of bioenergetics and growth-related traits in the wild mammal, Phyllotis darwini

We studied the potential for response to selection in typical physiological-thermoregulatory traits of mammals such as maximum metabolic rate (MMR), nonshivering thermogenesis (NST) and basal metabolic rate (BMR) on cold-acclimated animals. We used an animal model approach to estimate both narrow-sense heritabilities (h2) and genetic correlations between physiological and growth-related traits. Univariate analyses showed that MMR presented high, significant heritability (h2 = 0.69 +/- 0.35, asymptotic standard error), suggesting the potential for microevolution in this variable. However, NST and BMR presented low, nonsignificant h2, and NST showed large maternal/common environmental/nonadditive effects (c2 = 0.34 +/- 0.17). Heritabilities were large and significant (h2 > 0.5) for all growth-related traits (birth mass, growth rate, weaning mass). The only significant genetic correlations we found between a physiological trait and a growth-related trait was between NST and birth mass (r = -0.74; P < 0.05). Overall, these results suggest that additive genetic variance is present in several bioenergetic traits, and that genetic correlations could be present between those different kinds of traits.     

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.     

EVOLUTION OF BASAL METABOLIC RATE AND ORGAN MASSES IN LABORATORY MICE

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.     

冷驯化条件下高山姬鼠能量对策的初步研究

为进一步了解横断山区小型哺乳动物的能量代谢对策,本文主要研究了横断山的外来物种——高山姬鼠(Apodemus chevrieri)持续冷暴露28d的能量变化。结果表明,随着冷驯化时间延长,体重和体温降低;摄入能、消化能和可代谢能增加,至21d后这3项指标又下降;BMR和NST增加,并且28d后它们分别是对照组的187.19%和155.97%;(NST-BMR)/BMR比值7d时增加到1.02,21d后下降至0.53,并保持稳定。因此,在持续冷暴露下,高山姬鼠采取适当降低体重和体温、增加能量摄入、增加BMR和NST产热等途径来维持能量代谢平衡,但是NST在产热中的作用逐渐降低。这种能量模式很可能代表了一种外来小型啮齿动物对于在横断山生存独特的能量适应策略。     

Heritability of energetics in a wild mammal,the leaf-eared mouse (Phyllotis darwini)

Abstract.— As a first examination of the additive genetic variance of thermoregulatory traits in a natural population of endotherms, we studied the quantitative genetics of key physiological ecology traits in the leaf-eared mouse, Phyllotis darwini. We measured basal metabolic rate (BMR), nonshivering thermogenesis (NST), maximum metabolic rate for thermoregulation (MMR), thermal conductance (C_T), body temperature (T_b), and factorial aerobic scope (FAS) in individuals acclimated to cold and warm conditions. For comparability with previous studies, we included the following morphological traits: foot length (F_L), total length (T_L), body mass (mb, at birth, sexual maturity, 6 months, and 8 months). Variance components were obtained from two different procedures: the expected variance component in an ANOVA Type III sum of squares and an animal model approach using restricted maximum likelihood. Results suggest the presence of additive genetic variance in F_L (h²= 0.47, P = 0.045), C_T of cold-acclimated animals (h²= 0.66, P = 0.041), and night body temperature, measured in cold-acclimated animals (h²= 0.68, P = 0.080). Heritabilities of m_b were near zero at all ages, but maternal effects and common environment effects were high and significant. We found no evidence of additive genetic variance in BMR, NST, MMR, or FAS (i.e., estimates were not significantly different from zero for all tests). Our results are in general agreement with previous studies of mammals that reported low heritability for: (1) BMR and MMR; (2) daytime body temperature; and (3) body mass for wild, but not laboratory or domestic, populations.     

Effect of food restriction on energy intake and thermogenesis in Yunnan red-backed vole (Eothenomys miletus) with different metabolic levels

Shortage of food resources has significant effects on many physiological parameters of animals. The aim of the present study was to examine the relationship between the energetics countermeasures in response to food restriction and the levels of metabolism in Eothenomy miletus. Survival rate, body mass, basal metabolic rate (BMR), nonshivering thermogenesis (NST), body fat mass, serum leptin levels and other physiological parameters were measured. Animals were divided into high-BMR (hBMR) and low-BMR (lBMR) group. The two groups were restricted to 70% of ad libitum food intake for 4 weeks. The data showed that food intake increased by 24.5% in hBMR group than that in lBMR group before the experiment. Body mass, body fat mass, BMR and NST with hBMR or lBMR group significantly decreased after food restricting. Eighty percent of E. miletus survived with hBMR group, but 60% of E. miletus survived with lBMR group. Serum leptin levels were positively correlated with body mass, BMR and NST. The results suggested that E. miletus could apply physiological adjustments to adapt the period of food shortage by reducing energy metabolism, providing the support for the “metabolism switch hypothesis”. E. miletus with hBMR had decreased energy expenditure to maintain the normal physiological function. However, lBMR group could not decrease energy expenditure to meet the stress of available energy resource, which led to body mass decreased and mortality rate increased. Serum leptin levels may be involved in the regulation of energy balance and body mass in E. miletus during the food restriction.     

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。     

Role of inferior olive and thoracic IML neurons in nonshivering thermogenesis in rats

Removal of the midbrain tonic inhibitory mechanism on nonshivering thermogenesis (NST) results in increased temperatures of the interscapular brown adipose tissue (IBAT) and rectum (T(IBAT) and T(rec), respectively) via an enhanced central sympathetic output. Because it is unlikely that neurons (primary) of the midbrain inhibitory mechanism tonically inhibit the IBAT monosynaptically, there must be secondary or tertiary neurons posterior to the midbrain. Such neurons, therefore, may increase their activity during enhanced NST after removal of the midbrain tonic inhibition. The aim of the present experiments was to localize these secondary or tertiary neurons and establish descending neuronal pathway(s) that may project to the major NST effector IBAT. T(IBAT) and T(rec) increases induced by removal of the tonic inhibition by midbrain procaine microinjections were accompanied with appearance of c-Fos-positive neurons in the inferior olive (IO) and the intermediolateral (IML) cell column of the thoracic spinal cord. Electrical stimulation of and L-glutamate microinjections into the IO increased T(IBAT) and T(rec). Midbrain procaine-induced T(IBAT) and T(rec) increases were blocked by electrolytic IO lesions. These results suggest that central thermal signals produced from the lower midbrain are transmitted to IBAT through the IO and IML and that the IO has a role in the central sympathetic functions.     

Genetic variances and covariances of aerobic metabolic rates in laboratory mice

The genetic variances and covariances of traits must be known to predict how they may respond to selection and how covariances among them might affect their evolutionary trajectories. We used the animal model to estimate the genetic variances and covariances of basal metabolic rate (BMR) and maximal metabolic rate (MMR) in a genetically heterogeneous stock of laboratory mice. Narrow-sense heritability (h²) was approximately 0.38 ± 0.08 for body mass, 0.26 ± 0.08 for whole-animal BMR, 0.24 ± 0.07 for whole-animal MMR, 0.19 ± 0.07 for mass-independent BMR, and 0.16 ± 0.06 for mass-independent MMR. All h² estimates were significantly different from zero. The phenotypic correlation of whole animal BMR and MMR was 0.56 ± 0.02, and the corresponding genetic correlation was 0.79 ± 0.12. The phenotypic correlation of mass-independent BMR and MMR was 0.13 ± 0.03, and the corresponding genetic correlation was 0.72 ± 0.03. The genetic correlations of metabolic rates were significantly different from zero, but not significantly different from one. A key assumption of the aerobic capacity model for the evolution of endothermy is that BMR and MMR are linked. The estimated genetic correlation between BMR and MMR is consistent with that assumption, but the genetic correlation is not so high as to preclude independent evolution of BMR and MMR.     

Contribution of shivering and nonshivering thermogenesis to thermogenic capacity for the deer mouse (Peromyscus maniculatus)

Small mammals that are active all year must develop ways to survive the cold winters. Endotherms that experience prolonged cold exposure often increase their thermogenic capacity. Thermogenic capacity incorporates basal metabolic rate (BMR), nonshivering thermogenesis (NST), and shivering thermogenesis (ST). Increasing the capacity of any of these components will result in increased thermogenic capacity. It is often thought that NST should be the most plastic component of thermogenic capacity and as such is the most likely to increase with cold acclimation. We used deer mice to test this hypothesis by acclimating 27 animals to one of two temperatures (5 degrees or 22 degrees C) for 8 wk. We then measured and compared values for thermogenic capacity--BMR, ST, and NST--between the two groups. Thermogenic capacity and NST increased by 21% and 42%, respectively, after cold acclimation. Neither BMR nor ST showed any change after acclimation. Therefore, it appears that deer mice raise their thermogenic capacity in response to prolonged cold by altering NST only.     

Metabolic adjustments in breeding female kittiwakes (<Emphasis Type="Italic">Rissa tridactyla</Emphasis>) include changes in kidney metabolic intensity

Black-legged kittiwakes (BLKIs) reduce self-maintenance cost through reductions in mass-specific basal metabolic rate (BMR), body mass and the size of visceral organs during the chick-rearing period. In the present study, we measured kidney in vitro oxygen consumption and plasma 3,3',5-triiodo-L: -thyronine (T3) levels of incubating and chick-rearing female BLKIs, to test whether the decrease in BMR is caused mainly by decreased metabolic intensity or simply by reductions in the size of organs with high metabolic intensity. Body mass and body condition were lower in chick-rearing birds compared with the incubating birds. In contrast to the previous findings, however, the kidney mass did not differ between the two breeding stages. Plasma T3 levels decreased substantially during the breeding season, indicating a reduction in BMR. Over the same period, kidney mass-specific oxygen consumption decreased (by 17.2%) from the incubating to the chick-rearing stage. Thus, the reduction in BMR found in breeding BLKIs seems partly explained by adjustments in metabolic intensity of visceral organs. Lowered metabolic intensity of visceral organs would permit increased allocation of energy to offspring at the expense of their own self-maintenance.     

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。     

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。     

Seasonal adjustments in body mass and thermogenesis in Mongolian gerbils (<Emphasis Type="Italic">Meriones unguiculatus</Emphasis>): the roles of short photoperiod and cold

Seasonal adjustments in body mass and thermogenesis are important for the survival of small mammals during acclimatization in the temperate zone. To determine the contributions of short photoperiod and cold temperatures to seasonal changes in thermogenesis and body mass in Mongolian gerbils (Meriones unguiculatus), body mass, basal metabolic rate (BMR), nonshivering thermogenesis (NST), energy intake and energy digestibility were determined in seasonally acclimatized and laboratory acclimated animals. Body mass showed significant seasonal changes and decreased to a minimum in winter. Both BMR and NST increased in winter, and these changes were mimicked by exposing animals to short photoperiod or cold temperatures in the animal house. Digestible energy intake also increased significantly in winter, and also during exposure of housed animals to both short photoperiod and cold. These results suggest that Mongolian gerbils overcome winter thermoregulatory challenges by increasing energy intake and thermogenesis, and decreasing body mass to reduce total energy requirements. Short photoperiod and cold can serve as effective environmental cues during seasonal acclimatization.