Variation In Metabolic Rate Research Articles

Mitochondrial Maintenance in Skeletal Muscle.

Skeletal muscle is one of the tissues with the highest range of variability in metabolic rate, which, to a large extent, is critically dependent on tightly controlled and fine-tuned mitochondrial activity. Besides energy production, other mitochondrial processes, including calcium buffering, generation of heat, redox and reactive oxygen species homeostasis, intermediate metabolism, substrate biosynthesis, and anaplerosis, are essential for proper muscle contractility and performance. It is thus not surprising that adequate mitochondrial function is ensured by a plethora of mechanisms, aimed at balancing mitochondrial biogenesis, proteostasis, dynamics, and degradation. The fine-tuning of such maintenance mechanisms ranges from proper folding or degradation of individual proteins to the elimination of whole organelles, and in extremis, apoptosis of cells. In this review, the present knowledge on these processes in the context of skeletal muscle biology is summarized. Moreover, existing gaps in knowledge are highlighted, alluding to potential future studies and therapeutic implications.

Metabolic rate and foraging behaviour: a mechanistic link across body size and temperature gradients

The mechanistic link between metabolic rate and foraging behaviour is a crucial aspect of several energy‐based ecological theories. Despite its importance to ecology however, it remains unclear whether and how energy requirements and behavioural patterns are mechanistically connected. Here we aimed to assess how modes of behaviour, including cumulative space use, patch selection and time spent in an experimental resource‐patchy environment, are related to a forager's standard metabolic rate (SMR) and its main determinants, i.e. body mass and temperature. We tested the individual behavioural patterns and metabolic rates of a model organism, the amphipod Gammarus insensibilis, across a range of body masses and temperatures. We demonstrated quantitatively that body mass and temperature exert a major influence on foraging decisions and space use behaviour via their effects on metabolic rates and the marginal value of energy. Individual cumulative space use was found to scale allometrically with body mass and exponentially with temperature, with patch giving‐up time falling as body mass and temperature increased. In response to warmer temperatures, the specimens adaptively intensified their foraging effort and explored larger spaces to offset the elevated SMR. Our results showed that SMR explained more variation than body mass and temperature combined, and had greater predictive power for behavioural patterns. Furthermore, foraging decisions regarding patch choice and partitioning were strongly related to mass‐and‐temperature‐adjusted SMR (residual), which is a component of metabolic phenotype. Individuals with higher M–T adjusted SMR initially preferred the most profitable patch and, as time progressed, abandoned the patch earlier and explored more space than the others. These results demonstrate that foraging decisions are intimately associated with variations in standard metabolic rate, whether phenotypic or due to size and temperature combined. This, in turn, sheds light on higher‐order energy‐based ecological processes.

Revealing the hidden threats: Genotoxic effects of microplastics on freshwater fish

New evidence regarding the risks that microplastics (MP) ingestion pose to human and wildlife health are being revealed with progress made in ecotoxicological research. However, comprehensive and realistic approaches that evaluate multiple physiological responses simultaneously are still scarce despite their relevance to understand whole-organism effects. To address this information gap, we performed an experiment to assess the effects of MP on freshwater fish physiology from the molecular to the organismal level. Using a model species of global commercial importance (Cyprinus carpio) and MP type (recycling industry fragments), size (range between 125-1000 µm), and two concentrations of environmental relevance (0.75 and 8.25 µg/L). Experimental design included 5 blocks containing 3 treatment levels each one: control, low, and high MP concentration, with 6 fish each aquarium (5 blocks x 3 treatments x 6 fish per aquarium = 90 fish). Our results suggest that, under the experimental conditions applied, MP exposure did not cause adverse effects at the morphological (variation in size of gut), metabolic (variation of standard metabolic rate), or ecological (growth performance) levels. Nonetheless, we observed an increased frequency of micronucleated cells with increasing MP concentration (df = 42, t-value = 3.68, p-value < 0.001), showing the potential genotoxicity of MP, which can clearly harm fish health in long-term. Thus, despite being a highly resistant species, exposure to MP may generate negative effects in juvenile C. carpio at cellular or subcellular levels. Our findings highlight that the manifestation of MP effects may vary over time, emphasizing the need for future studies to consider longer exposure durations in experimental designs.

Temperature-dependent in vitro hepatocytotoxicity of insecticides in bats

Heterothermic insectivorous bats are supposed to experience differential adverse effects of insecticidal pollutants depending on their seasonal and/or daily variation of metabolic and detoxification rates. Here, we investigated effects of imidacloprid, cypermethrin and fipronil on Nyctalus noctula bat-derived hepatocytes through cytotoxicity, cell inhibition and death at different concentrations (0.01, 0.1, 1, 10, 100, 1000 μg/ml), exposure times (10, 24, 48 hrs), incubation temperatures simulating hibernation (8 °C), daily torpor (20 °C), normothermy (37 °C) and active flight (40 °C), and cytochrome P450 addition. Toxic effects were significantly influenced by temperature (p < 0.05), with strong cytotoxicity after 10 hour exposure to fipronil or cypermethrin at 37 and 40 °C, cell replication inhibition (all insecticides at 8 °C) and cellular stimulation, with slight culture proliferation after 48 hours (all insecticides at 40 °C). Replacing protected chiropterans with cell cultures is a way to assess and extrapolate risks of insecticides for bats.

Development of Single-Nucleotide Polymorphism Markers and Population Genetic Analysis of the Hadal Amphipod Alicella gigantea across the Mariana and New Britain Trenches

Alicella gigantea, the largest amphipod scavengers found to date, play key roles in the food web of the hadal ecosystem. However, the genetic structure of A. gigantea populations among different trenches has not been reported yet. In this study, SNP (single-nucleotide polymorphism) markers were developed for three A. gigantea geographic populations collected from the southern Mariana Trench (SMT), the central New Britain Trench (CNBT), and the eastern New Britain Trench (ENBT), based on the SLAF-seq (specific locus amplified fragment sequencing) technology. A total of 570,168 filtered SNPs were screened out for subsequent population genetic analysis. Results showed that the inbreeding levels across the three geographic populations were relatively low, and the genomic inbreeding coefficients of the three populations were similar in magnitude. Based on the results of phylogenetic analysis, population structure analysis, and principal component analysis, it is believed that the three A. gigantea geographic populations belong to the same population, and the kinship relationship between the ENBT and CNBT populations is close. Moreover, the differential candidate adaptive sites on the SNPs suggest that there may be variations in metabolic rates among the three geographic populations, possibly linked to differences in food availability and sources in different trenches, ultimately resulting in different survival strategies in A. gigantea populations within distinct trenches. Compared with the Mariana Trench, the New Britain Trench has a richer organic matter input, and it is speculated that the A. gigantea Mariana Trench population may adopt a lower metabolic rate to cope with the harsher environment of nutrient deficiency.

Temporal and spatial variability in metabolism of the Antarctic pelagic tunicate Salpa thompsoni Foxton, 1961

ABSTRACT The mass-specific metabolic rates of the Antarctic pelagic tunicate Salpa thompsoni Foxton, 1961 were studied during March-April of 1998 and March 2002. The study revealed a large variation in metabolic rates and assessed sources of this variability. The main factors driving variability included density of tunicates in incubation containers (incubation density, e.g. the salp mass per unit volume of the respirometer), diel/circadian rhythms in salps, and spatial variability of their metabolic performance related to the feeding conditions. The mass specific respiration rates of both salp life forms (oozooids and blastozooids) appeared to be independent of their body mass. The salp-specific respiration rates at 3°C were strongly negatively influenced by their incubation density ranging between 2.0 and 90.4 gWW.l−1. Salp respiration rates adjusted to an incubation density of 3 gWW.l−1 in both oozooids and blastozooids followed similar circadian rhythms with the mean respiration rates of 79.5 and 41.5 μg O2 gWW−1 h−1, respectively. Deviation of these rates from actual field-measured respiration rates corrected for the salp density and diel variability during 1998 and 2002 identified effects of food concentrations, i.e. proxy of the plankton community development and composition, on the salp population performance.

Variation in metabolic rate during low tide aerial exposure in the Asian shore crab Hemigrapsus sanguineus

Intertidal animals deal with physical gradients daily that create stressful conditions across the shore. These physical gradients influence the physiological performance of organisms, requiring responses that may differ with height on the shore. We examined the respiratory response to aerial exposure in the invasive Asian shore crab Hemigrapsus sanguineus during periods of low tide emersion using two field experiments. The first experiment simultaneously measured respiration of individuals collected from different heights on the shore, which had therefore been emersed for different lengths of time. The second experiment measured respiration of individuals collected at different times from the same tidal height. Respiration rates of crabs in both experiments increased immediately after emersion, nearly doubling by and peaking at ~ 1.5 h of aerial exposure, before decreasing again over the next 1.5 h. These results suggest that the energetic cost of low tide exposure is greatest shortly after emersion during the first half of the typical low tide period, but then decreases thereafter. These respiration patterns facilitate the broad intertidal distribution of this species on rocky shores throughout its range.

Tissue dependence of variation in metabolic rates of harvester ants

Metabolic rates vary tremendously among individuals and across species, and the causes of this variation remain controversial and challenging to identify. We utilized an Agilent Seahorse system to measure the metabolic rates of brains, flight muscles, leg muscles, jaw muscles, digestive tract, fat and reproductive organs of harvester ants of different species, sex and caste, and compared these to whole body metabolic rates. Across Pogonomyrmex species varying an order of magnitude in body size, mass-specific brain metabolic rates declined dramatically in larger species, such that the brain accounted for 43% of whole body metabolism in the smallest species and 14% in the largest. In Veromessor pergandei, males have much higher mass-specific metabolic rates than queens or workers, with queens being slightly higher than workers. The tissue specific bases to metabolic rates varied with sex and caste. Males are "flying gonads", with flight muscle, fat and gonads accounting for 44, 25 and 20%, respectively, of resting metabolic rate, and tissue-specific rates were generally higher in males than females. For queens, which have by far the largest fat content, the fat body contributes the largest fraction of the total tissue metabolic rate (38%), with flight muscle, femoral muscle, brain and gut each contributing 13 – 15% of total cost. For workers, brains are the most important contributors to total tissue metabolic rate (38%), followed by fat body (24%) and gut (19%). Together these results demonstrate that variation in whole body metabolic rate within and across closely related species is strongly affected by size, sex and caste-specific differences in tissue function, likely associated with life history variation. Supported by NSF IOS-1953419. This is the full abstract presented at the American Physiology Summit 2024 meeting and is only available in HTML format. There are no additional versions or additional content available for this abstract. Physiology was not involved in the peer review process.

Chronic Hyperoxia Augments the Hypercapnic Ventilatory Response in Adult Rats

Rats exposed to 4 – 14 days of 60% O2 as adults exhibit a modest enhancement of their hypoxic ventilatory response (HVR) (Danielson &amp; Bavis, Physiology 38(S1): 5730119, 2023). To determine whether this plasticity is unique to the HVR or a general increase in excitability of the respiratory control system, we tested the hypothesis that chronic hyperoxia would also enhance the hypercapnic ventilatory response (HCVR). The ventilatory response to 7% CO2 was measured by whole-body plethysmography in adult, Sprague-Dawley rats immediately after 4 and 14 days of exposure to 60% O2 or an equivalent time period in room air. Baseline ventilation and the HCVR were unchanged after 4 days of hyperoxia. The HCVR was increased after 14 days (Treatment × FICO2, P=0.004), with hypercapnic ventilation being approximately 15% greater than in control rats. However, this effect was no longer significant after accounting for variation in metabolic rate, and the HCVR was fully recovered when rats were restudied four weeks after they were returned to room air. In a follow-up experiment, pulse oximetry was performed in isoflurane-anesthetized rats breathing room air or 12% O2. Exposure to 4 – 14 days of 60% O2 did not impair gas exchange, so augmented ventilatory responses likely reflect changes in the neural control of breathing and/or metabolism rather than differences in the levels of hypoxemia and hypercapnia experienced by rats during the tests. In conclusion, chronic hyperoxia elicits plasticity in both the HVR and HCVR of adult rats, but these responses recover in less than one month after rats are returned to room air. Supported by NIH grant P20 GM-103423 (Maine INBRE). This is the full abstract presented at the American Physiology Summit 2024 meeting and is only available in HTML format. There are no additional versions or additional content available for this abstract. Physiology was not involved in the peer review process.

Developmental plasticity of melanisation in a beetle reveals sex‐specific responses and performance costs

Abstract Dark pigmentation of adults resulting from cold exposure during development is ubiquitous among insects. Yet the costs associated with the developmental plasticity of melanisation have been explored only for a handful of species. We explored two hypotheses relating to colour plasticity of insects. First, if melanin pigments are costly to synthesise and require allocation of resources, increased melanisation should be negatively associated with performance traits (the cost hypothesis). Second, given the positive association between melanisation and immune responses or desiccation resistance in some species, melanisation and performance may co‐vary positively (the positive covariance hypothesis). Furthermore, given the typical differences in reproductive effort and activity between females and males, we expect these performance–melanisation relationships to differ between sexes. We assessed whether temperature‐induced melanisation of the globally invasive beetle Harmonia axyridis f. succinea (Pallas) (Coleoptera: Coccinellidae) was related to standard metabolic rate and flight performance while accounting for developmental temperature and family affiliation. Melanisation explained little variation in standard metabolic rate at most temperatures tested (15, 20, 25, 30 and 35°C). For flight performance and after the cold‐rearing regime, lighter coloured female beetles had increased flight speed compared with darker females, whereas the opposite was found in males. In addition, in warm‐reared beetles, darker individuals had lower mean flight speeds. The results suggest that at least some flight performance costs are associated with developmentally induced melanisation, supporting the cost hypothesis. Disparities in these relationships between males and females suggest that the drivers underlying variation in melanisation differ between sexes. Importantly, variation in melanisation was more acute for females reared in the warm regime compared with equally treated males and to cold‐reared individuals. We propose new directions to test hypotheses pertaining to the maintenance of colour variation and performance between sexes in nature.

Variation in Resting Metabolic Rate Affects Identification of Metabolic Change in Geographically Distinct Cohorts of Patients With ALS.

Altered metabolism is observed in amyotrophic lateral sclerosis (ALS). However, without a standardized methodology to define metabolic changes, our understanding of factors contributing to and the clinical significance of altered metabolism in ALS is limited. We aimed to determine how geographic variation in metabolic rates influences estimates and accuracy of predicted resting energy expenditure (REE) in patients with ALS and controls, while validating the effectiveness of cohort-specific approaches in predicting altered metabolic rate in ALS. Participants from 3 geographically distinct sites across Australia, China, and the Netherlands underwent REE assessments, and we considered 22 unique equations for estimating REE. Analyses evaluated equation performance and the influence of demographics on metabolic status. Comparisons were made using standardized and local reference values to identify metabolic alterations. 606 participants were included from Australia (patients with ALS: 140, controls: 154), the Netherlands (patients with ALS: 79, controls: 37) and China (patients with ALS: 67, controls: 129). Measured REE was variable across geographic cohorts, with fat-free mass contributing to this variation across all patients (p = 0.002 to p < 0.001). Of the 22 predication equations assessed, the Sabounchi Structure 4 (S4) equation performed relatively well across all control cohorts. Use of prediction thresholds generated using data from Australian controls generally increased the prevalence of hypermetabolism in Chinese (55%, [43%-67%]) and Dutch (44%, [33%-55%]) cases when compared with Australian cases (30%, [22%-38%]). Adjustment of prediction thresholds to consider geographically distinct characteristics from matched control cohorts resulted in a decrease in the proportion of hypermetabolic cases in Chinese and Dutch cohorts (25%-31% vs 55% and 20%-34% vs 43%-44%, respectively), and increased prevalence of hypometabolism in Dutch cases with ALS (1% to 8%-10%). The identification of hypermetabolism in ALS is influenced by the formulae and demographic-specific prediction thresholds used for defining alterations in metabolic rate. A consensus approach is needed for identification of metabolic changes in ALS and will facilitate improved understanding of the cause and clinical significance of this in ALS.

Metabolic adjustments to winter severity in two geographically separated great tit (Parus major) populations.

Understanding the potential limits placed on organisms by their ecophysiology is crucial for predicting their responses to varying environmental conditions. A main hypothesis for explaining avian thermoregulatory mechanisms is the aerobic capacity model, which posits a positive correlation between basal (basal metabolic rate [BMR]) and summit (Msum) metabolism. Most evidence for this hypothesis, however, comes from interspecific comparisons, and the ecophysiological underpinnings of avian thermoregulatory capacities hence remain controversial. Indeed, studies have traditionally relied on between-species comparisons, although, recently, there has been a growing recognition of the importance of intraspecific variation in ecophysiological responses. Therefore, here, we focused on great tits (Parus major), measuring BMR and Msum during winter in two populations from two different climates: maritime-temperate (Gontrode, Belgium) and continental (Zvenigorod, Russia). We tested for the presence of intraspecific geographical variation in metabolic rates and assessed the predictions following the aerobic capacity model. We found that birds from the maritime-temperate climate (Gontrode) showed higher BMR, whereas conversely, great tits from Zvenigorod showed higher levels of Msum. Within each population, our data did not fully support the aerobic capacity model's predictions. We argued that the decoupling of BMR and Msum observed may be caused by different selective forces acting on these metabolic rates, with birds from the continental-climate Zvenigorod population facing the need to conserve energy for surviving long winter nights (by keeping their BMR at low levels) while simultaneously being able to generate more heat (i.e., a high Msum) to withstand cold spells.

The hidden costs of resistance: Contrasting the energetics of successfully and unsuccessfully fighting infection

Abstract Exposure to a pathogen is predicted to lead to increased energy use as hosts attempt to activate a costly immune system and repair damaged tissue. To meet this demand, metabolic rates, which capture the rate at which a host can use, transform and expend energy, are expected to increase. Yet for many host–pathogen systems, metabolic rates after encountering a pathogen are just as likely to decrease as increase, suggesting that increased energy expenditure may not always be best for fighting infection. Diverging metabolic trajectories have been previously attributed to the different pathways that specific pathogen classes, such as bacteria or viruses, induce in a host. Here, we test how the magnitude and direction of metabolic change following pathogen exposure might also depend on whether a host has cleared infection or is instead fighting to reduce pathogen burden, as well as interactions between host and pathogen genotypes of a single host–pathogen system. Using a model system, Daphnia magna and its bacterial pathogen, we quantified changes in mass‐independent metabolic rates over a 30‐day period for multiple host and pathogen genotypes. We found that the metabolic trajectory of an exposed host diverged quickly during the infection process. For hosts that were exposed to a pathogen and resisted infection, their mass‐independent metabolic rates remained suppressed long after exposure, leading to a sustained reduction in total energy use compared to unexposed animals. The reverse was true for hosts in which the pathogen was able to establish an infection. Underlying these changes were differences in the energetic burden that each pathogen genotype imposed on its host, as well as changes in the way host genotype and the outcome of infection shaped underlying scaling relationships between host body mass and metabolic rates. Our results demonstrate how variation in an organism's metabolic rate and overall energy use can arise from within a single host–pathogen encounter and depend on the likelihood of pathogen clearance, as well as the within‐species genetic variability of both hosts and pathogens. Read the free Plain Language Summary for this article on the Journal blog.

Climate‐related variation of metabolic rate across the distribution of a broadly tolerant invasive forest pest

AbstractAimMetabolic rate is a widely studied physiological species trait related to energetics, climate, and geographical distributions. Hypotheses have been proposed to explain variation in metabolic rate, but evidence has been mixed due to the limited sampling scope of intraspecific studies. Successful biological invasions offer a unique opportunity to examine the development of intraspecific physiological variation and how it relates to climate, invasive spread and species range limits. The aim of this study was to determine if metabolic rate variation across the spongy moth invasive range was consistent with a pattern of adaptation to local climate.LocationNortheastern United States of America.TaxonLymantria dispar dispar L. (Lepidoptera: Erebidae).MethodsLarvae were sourced from 14 populations across the invasion front and interior of the current L. d. dispar invasive range and were reared at a constant temperature. Routine metabolic rates (RMR) of larvae were assayed at three ecologically relevant temperatures. These data were analysed to determine if there were differences in RMR and temperature sensitivity of RMR among populations. Population‐level variation in RMR was then analysed as a function of local climate and geographical position to test for patterns consistent with local adaptation.ResultsLarval RMR showed significant variation among populations across all assay temperatures, but there was no difference in temperature sensitivity (i.e. slope). This variation followed a positive latitudinal cline with RMR increasing from the southern range to the north. This cline also showed a significant relationship with local climate variables.Main ConclusionsLarval metabolic rate variation was consistent with a pattern of adaptation by L. d. dispar to divergent climates across its invasive range. These results indicated that thermal adaptation of whole‐organism physiology may play a key role in promoting species spread and expansion for biological invasions like L. d. dispar.

Metabolism, population growth, and the fast‐slow life history continuum of marine fishes

AbstractThe maximum intrinsic rate of population increase (rmax) represents a population's maximum capacity to replace itself and is central to fisheries management and conservation. Species with lower rmax typically have slower life histories compared to species with faster life histories and higher rmax. Here, we posit that metabolic rate is related to the fast–slow life history continuum and the connection may be stronger for maximum metabolic rate and aerobic scope compared to resting metabolic rate. Specifically, we ask whether variation in rmax or any of its component life‐history traits – age‐at‐maturity, maximum age, and annual reproductive output – explain variation in resting and maximum metabolic rates and aerobic scope across 84 shark and teleost species, while accounting for the effects of measurement temperature, measurement body mass, ecological lifestyle, and evolutionary history. Overall, we find a strong connection between metabolic rate and the fast‐slow life history continuum, such that species with faster population growth (higher rmax) generally have higher maximum metabolic rates and broader aerobic scopes. Specifically, rmax is more important in explaining variation in maximum metabolic rate and aerobic scope compared to resting metabolic rate, which is best explained by age‐at‐maturity (out of the life history traits examined). In conclusion, teleosts and sharks share a common fast–slow physiology/life history continuum, with teleosts generally at the faster end and sharks at the slower end, yet with considerable overlap. Our work improves our understanding of the diversity of fish life histories and may ultimately improve our understanding of intrinsic sensitivity to overfishing.

Among-individual variation in thermal plasticity of fish metabolic rates causes profound variation in temperature-specific trait repeatability, but does not co-vary with behavioural plasticity.

Conspecifics of the same age and size differ consistently in the pace with which they expend energy. This among-individual variation in metabolic rate is thought to influence behavioural variation, since differences in energy requirements should motivate behaviours that facilitate energy acquisition, such as being bold or active in foraging. While there is evidence for links between metabolic rate and behaviour in constant environments, we know little about whether metabolic rate and behaviour change together when the environment changes-that is, if metabolic and behavioural plasticity co-vary. We investigated this using a fish that becomes dormant in winter and strongly reduces its activity when the environment cools, the cunner (Tautogolabrus adspersus). We found strong and predictable among-individual variation in thermal plasticity of metabolic rates, from resting to maximum levels, but no evidence for among-individual variation in thermal plasticity of movement activity, meaning that these key physiological and behavioural traits change independently when the environment changes. The strong among-individual variation in metabolic rate plasticity resulted in much higher repeatability (among-individual consistency) of metabolic rates at warm than cold temperatures, indicating that the potential for metabolic rate to evolve under selection is temperature-dependent, as repeatability can set the upper limit to heritability. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Temperature and nutrition do not interact to shape the evolution of metabolic rate.

Metabolic cold adaptation, or Krogh's rule, is the controversial hypothesis that predicts a monotonically negative relationship between metabolic rate and environmental temperature for ectotherms living along thermal clines measured at a common temperature. Macrophysiological patterns consistent with Krogh's rule are not always evident in nature, and experimentally evolved responses to temperature have failed to replicate such patterns. Hence, temperature may not be the sole driver of observed variation in metabolic rate. We tested the hypothesis that temperature, as a driver of energy demand, interacts with nutrition, a driver of energy supply, to shape the evolution of metabolic rate to produce a pattern resembling Krogh's rule. To do this, we evolved replicate lines of Drosophila melanogaster at 18, 25 or 28°C on control, low-calorie or low-protein diets. Contrary to our prediction, we observed no effect of nutrition, alone or interacting with temperature, on adult female and male metabolic rates. Moreover, support for Krogh's rule was only in females at lower temperatures. We, therefore, hypothesize that observed variation in metabolic rate along environmental clines arises from the metabolic consequences of environment-specific life-history optimization, rather than because of the direct effect of temperature on metabolic rate. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Metabolic scaling as an emergent outcome of variation in metabolic rate.

The allometric scaling of metabolic rate and what drives it are major questions in biology with a long history. Since the metabolic rate at any level of biological organization is an emergent property of its lower-level constituents, it is an outcome of the intrinsic heterogeneity among these units and the interactions among them. However, the influence of lower-level heterogeneity on system-level metabolic rate is difficult to investigate, given the tightly integrated body plan of unitary organisms. In this context, social insects such as honeybees can serve as important model systems because unlike unitary organisms, these superorganisms can be taken apart and reassembled in different configurations to study metabolic rate and its various drivers at different levels of organization. This commentary discusses the background of such an approach and how combining it with artificial selection to generate heterogeneity in metabolic rate with an analytical framework to parse out the different mechanisms that contribute to the effects of heterogeneity can contribute to the various models of metabolic scaling. Finally, the absence of the typical allometric scaling relationship among different species of honeybees is discussed as an important prospect for deciphering the role of top-down ecological factors on metabolic scaling. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Interactive effects of intrinsic and extrinsic factors on metabolic rate.

Metabolism energizes all biological processes, and its tempo may importantly influence the ecological success and evolutionary fitness of organisms. Therefore, understanding the broad variation in metabolic rate that exists across the living world is a fundamental challenge in biology. To further the development of a more reliable and holistic picture of the causes of this variation, we review several examples of how various intrinsic (biological) and extrinsic (environmental) factors (including body size, cell size, activity level, temperature, predation and other diverse genetic, cellular, morphological, physiological, behavioural and ecological influences) can interactively affect metabolic rate in synergistic or antagonistic ways. Most of the interactive effects that have been documented involve body size, temperature or both, but future research may reveal additional 'hub factors'. Our review highlights the complex, intimate inter-relationships between physiology and ecology, knowledge of which can shed light on various problems in both disciplines, including variation in physiological adaptations, life histories, ecological niches and various organism-environment interactions in ecosystems. We also discuss theoretical and practical implications of interactive effects on metabolic rate and provide suggestions for future research, including holistic system analyses at various hierarchical levels of organization that focus on interactive proximate (functional) and ultimate (evolutionary) causal networks. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Tissue-specific metabolic enzyme levels covary with whole-animal metabolic rates and life-history loci via epistatic effects.

Metabolic rates, including standard (SMR) and maximum (MMR) metabolic rate have often been linked with life-history strategies. Variation in context- and tissue-level metabolism underlying SMR and MMR may thus provide a physiological basis for life-history variation. This raises a hypothesis that tissue-specific metabolism covaries with whole-animal metabolic rates and is genetically linked to life history. In Atlantic salmon (Salmo salar), variation in two loci, vgll3 and six6, affects life history via age-at-maturity as well as MMR. Here, using individuals with known SMR and MMR with different vgll3 and six6 genotype combinations, we measured proxies of mitochondrial density and anaerobic metabolism, i.e. maximal activities of the mitochondrial citrate synthase (CS) and lactate dehydrogenase (LDH) enzymes, in four tissues (heart, intestine, liver, white muscle) across low- and high-food regimes. We found enzymatic activities were related to metabolic rates, mainly SMR, in the intestine and heart. Individual loci were not associated with the enzymatic activities, but we found epistatic effects and genotype-by-environment interactions in CS activity in the heart and epistasis in LDH activity in the intestine. These effects suggest that mitochondrial density and anaerobic capacity in the heart and intestine may partly mediate variation in metabolic rates and life history via age-at-maturity. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.