THE INTEGRATED PHENOTYPE

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Is there a LINK BETWEEN MINIMUM AND MAXIMUM RATES of metabolism? 

  Phylogeny and distribution of effect sizes for the intra-specific correlation between minMR and exercise-induced maximum metabolic rate (VO2max), cold-induced summit metabolic rate (Msum), and daily energy expenditure (DEE). Correlations were assessed using different measures of minMR: standard and basal metabolic rate (circles) or resting metabolic rate (squares).

Phylogeny and distribution of effect sizes for the intra-specific correlation between minMR and exercise-induced maximum metabolic rate (VO2max), cold-induced summit metabolic rate (Msum), and daily energy expenditure (DEE). Correlations were assessed using different measures of minMR: standard and basal metabolic rate (circles) or resting metabolic rate (squares).

  Means and 95% confidence intervals for effect sizes of the intra- and inter-specific correlation between minimum metabolic rate and exercise-induced maximum metabolic rate (VO2max), cold-induced summit metabolic rate (Msum), and daily energy expenditure (DEE).

Means and 95% confidence intervals for effect sizes of the intra- and inter-specific correlation between minimum metabolic rate and exercise-induced maximum metabolic rate (VO2max), cold-induced summit metabolic rate (Msum), and daily energy expenditure (DEE).

Whether at rest or active, animals are constrained to operate within the energetic bounds determined by their minimum (minMR) and sustained or maximum metabolic rates (upperMR). MinMR and upperMR can differ considerably among individuals and species but are often presumed to be mechanistically linked to one another. Specifically, minMR is thought to reflect the idling cost of the machinery needed to support upperMR. However, previous analyses based on limited datasets have come to conflicting conclusions regarding the generality and strength of their association.

Here I conducted the first comprehensive assessment of their relationship, based on a large number of published estimates of both the intra-specific (n = 176) and inter-specific (n = 41) phenotypic correlations between minMR and upperMR, estimated as either exercise-induced maximum metabolic rate (VO2max), cold-induced summit metabolic rate (Msum), or daily energy expenditure (DEE).

The meta-analysis shows that there is a general positive association between minMR and upperMR that is shared among vertebrate taxonomic classes. However, there was stronger evidence for intra-specific correlations between minMR and Msum and between minMR and DEE than there was for a correlation between minMR and VO2max across different taxa. As expected, inter-specific correlation estimates were consistently higher than intra-specific estimates across all traits and vertebrate classes. An interesting exception to this general trend was observed in mammals, which contrast with birds and exhibit no correlation between minMR and Msum. This may be due to the evolution and recruitment of brown fat as a thermogenic tissue, which illustrates how some species and lineages might circumvent this seemingly general association.  

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Does metabolic rate evolve in parallel with the life history?

Metabolic rates differed among populations according to their pace of life history. (a) Standard metabolic rate was lower in naturally-occurring populations with a slow (grey) relative to a fast-paced (blue) life history in both the Oropuche and Yarra River drainages. Standard metabolic rate was also lower in a population transplanted from high to low predation sites in 1981 that has since evolved a slow-paced life history (green) versus their naturally-occurring ancestral population with a fast-paced life history (blue) in the Caroni River drainage.

Standard metabolic rate was positively correlated with a suite of life history traits across six populations. Included are naturally-occurring populations with fast-paced (blue) and slow-paced life histories (grey) and a population transplanted from a high to low predation site 35 years ago that has since evolved a slow-paced life history (green).

Metabolic rates and life history strategies are both thought to set the ‘pace of life’ but whether they evolve in tandem is not well understood. Here, using a common garden experiment that compares replicate paired populations, I show that Trinidadian guppy (Poecilia reticulata) populations that evolved a fast-paced life history in high predation environments have consistently higher metabolic rates than guppies that evolved a slow-paced life history in low predation environments.

Furthermore, by transplanting guppies from high to low predation environments, we show that metabolic rate evolves in parallel with the pace of life history, at a rapid rate, and in the same direction as found for naturally occurring populations. Together, these multiple lines of inference provide evidence for a tight evolutionary coupling between metabolism and the pace of life history.  

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is phenotypic plasticity in metabolic rate accompanied by changes in behavior?   

Correlation between activity and metabolic rates of juvenile brown trout (Salmo trutta) at the start (initial: r = −0.16, P = 0.45) and end (final: r = −0.69, p < 0.01) of a 5 week period of decreasing rations at 7.5 °C.

Correlation between changes in standard metabolic rate and activity rate (r = −0.63, p < 0.02) among individual juvenile brown trout (Salmo trutta) over a 5 week period of decreasing rations at 7.5 °C.

Energy stores are essential for the overwinter survival of many temperate and polar animals, but individuals within a species often differ in how quickly they deplete their reserves. These disparities in overwinter performance may be explained by differences in their physiological and behavioral flexibility in response to food scarcity. However, little is known about whether individuals exhibit correlated or independent changes in these traits, and how these phenotypic changes collectively affect their winter energy use.

I examined individual flexibility in both standard metabolic rate and activity level in response to food scarcity and their combined consequences for depletion of lipid stores among overwintering brown trout (Salmo trutta). Metabolism and activity tended to decrease, yet individuals exhibited striking differences in their physiological and behavioral flexibility. The rate of lipid depletion was negatively related to decreases in both metabolic and activity rates, with the smallest lipid loss over the simulated winter period occurring in individuals that had the greatest reductions in metabolism and/or activity. However, changes in metabolism and activity were negatively correlated; those individuals that decreased their SMR to a greater extent tended to increase their activity rates, and vice versa, suggesting among-individual variation in strategies for coping with food scarcity.

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Does aerobic capacity influence food intake?

  Average daily maximum food consumption as a function of aerobic scope in juvenile brown trout ( Salmo trutta ) fed  ad libitum  ( R 2 = 0.35). Plotted are partial residuals evaluated at the mean body mass (6.5 g) and standard metabolic rate (0.66 mg O2 h-1).

Average daily maximum food consumption as a function of aerobic scope in juvenile brown trout (Salmo trutta) fed ad libitum (R2 = 0.35). Plotted are partial residuals evaluated at the mean body mass (6.5 g) and standard metabolic rate (0.66 mg O2 h-1).

Links between metabolism and components of fitness such as growth, reproduction, and survival can depend on food availability. A high standard metabolic rate (baseline energy expenditure) or aerobic scope (the difference between an individual’s maximum and standard metabolic rate) is often beneficial when food is abundant or easily accessible but can be less important or even disadvantageous when food levels decline. While the mechanisms underlying these context-dependent associations are not well understood, they suggest that individuals with a higher standard metabolic rate or aerobic scope are better able to take advantage of high food abundance. Here I show that juvenile brown trout (Salmo trutta) with a higher aerobic scope were able to consume more food per day relative to individuals with a lower aerobic scope. These results help explain why a high aerobic capacity can improve performance measures such as growth rate at high but not low levels of food availability.