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Is metabolic rate a repeatable trait? a meta-analysis

Z-transformed effect sizes of metabolic rate repeatability as a function of the interval duration between repeated measurements of metabolic rate conducted on animals free-living in the wild (black) versus housed under laboratory conditions (grey). Data are 106 published estimates from 39 studies of birds and mammals.

Metabolic rate has been linked to multiple components of fitness and is both heritable and repeatable to a certain extent. However, its repeatability can differ among studies, even after controlling for the time interval between measurements. Some of this variation in repeatability may be due to the relative stability of the environmental conditions in which the animals are living between measurements.

I compared published repeatability estimates for basal, resting, and maximum metabolic rate from studies of endotherms living in the laboratory versus those living in the wild during the interval between measurements. I found that repeatability declines over time, as demonstrated previously, but show for the first time that estimates from free-living animals are also considerably lower than those from animals living under more stable laboratory conditions.

do individuals exhibit consistent differences in metabolic rate across changing thermal regimes?

Repeatability (R) of (a-c) standard metabolic rate, (d-f) maximum metabolic rate, and (g-i) aerobic scope of juvenile brown trout (Salmo trutta) across three consecutive test temperatures.

Metabolic rate must be consistent (i.e. repeatable) over at least some portion of an individual’s in order to predict its longer-term effects on population dynamics and how it will respond to selection. Previous studies demonstrate that metabolic rates are repeatable under constant conditions but potentially less so in more variable environments. I measured the standard (= minimum) metabolic rate, maximum metabolic rate, and aerobic scope (= interval between standard and maximum rates) in juvenile brown trout (Salmo trutta) after 5 weeks acclimation to each of three consecutive test temperatures (10, 13, and then 16˚C) that simulated the warming conditions experienced throughout their first summer of growth. I found that metabolic rates are repeatable over a period of months under changing thermal conditions: individual trout exhibited consistent differences in all three metabolic traits across increasing temperatures. Initial among-individual differences in metabolism are thus likely to have significant consequences for fitness-related traits over key periods of their life history.

Do links between energy metabolism and growth depend on environmental context?

Relationships between log10-transformed standard metabolic rate (SMR), maximum metabolic rate (MMR), aerobic scope (AS) and body mass (g) of juvenile brown trout.

Mean specific growth rates of four metabolic phenotypes of juvenile brown trout at three different food levels. Shown are partial residuals after accounting for variation in fish fork length (mm).

Metabolic rates can vary as much as 3-fold among individuals of the same size and age in a population, but why such variation persists is unclear. Relationships between standard metabolic rate (SMR), growth, and survival can vary with environmental conditions, suggesting that the fitness consequences of a given metabolic phenotype may be context-dependent. Less attention has focused on the link between absolute aerobic scope (AS, the difference between maximum and standard metabolic rate) and fitness under different environmental conditions, despite the importance of aerobic scope to an organism’s total energetic capacity. 

I examined the consequences of individual variation in both SMR and AS for somatic growth rates of brown trout (Salmo trutta) under different levels of food availability.  SMR and AS were uncorrelated across individuals. In addition, SMR and AS not only had interactive effects on growth but these interactions depended on food level: AS had a positive effect at ad libitum food levels whose magnitude depended on SMR, interactive effects with SMR at intermediate food levels, but neither AS or SMR influenced growth at the low food level. As a result, there was no metabolic phenotype that performed best or worst across all food levels.

These results demonstrate the importance of aerobic scope in determining somatic growth rates and support the hypothesis that links between individual variation in metabolism and fitness are context-dependent. The larger metabolic phenotype and the environmental context in which performance is evaluated both need to be considered in order to better understand the link between metabolic rates and fitness and thereby the persistence of individual variation in metabolic rates.

Selection on metabolism in the wild: a field study

Organisms can modify their surrounding environment, but whether these changes are large enough to feed back and alter their evolutionary trajectories is not well understood, particularly in wild populations. Here my colleagues and I show that nutrient pulses from decomposing Atlantic salmon (Salmo salar) parents alter selection pressures on their offspring with important consequences for their phenotypic and genetic diversity.

We found a strong survival advantage to larger eggs and faster juvenile metabolic rates in streams lacking carcasses but not in streams containing this parental nutrient input. Differences in selection intensities led to significant phenotypic divergence in these two traits among stream types. Stronger selection in streams with low parental nutrient input also decreased the number of surviving families compared to streams with high parental nutrient levels. Observed effects of parent-derived nutrients on selection pressures provide experimental evidence for key components of eco-evolutionary feedbacks in wild populations.

Linear selection gradients in streams with low (blue, n = 5) versus high (green, n = 5) parental nutrients. Plotted are standardized selection gradients for egg-to-juvenile survival (%) as a function of (a) egg mass, (b) standard metabolic rate, and (c) maximum metabolic rate in full sibling Atlantic salmon (Salmo salar) families (n = 29). Metabolic rates were standardised to a common body mass of 1g prior to analyses.




Summaries our work can be found here and here.