Differences in mitochondrial efficiency explain individual variation in growth performance

Abstract

The physiological causes of intraspecific differences in fitness components such as growth rate are currently a source of debate. It has been suggested that differences in energy metabolism may drive variation in growth, but it remains unclear whether covariation between growth rates and energy metabolism is: (i) a result of certain individuals acquiring and consequently allocating more resources to growth, and/or is (ii) determined by variation in the efficiency with which those resources are transformed into growth. Studies of individually housed animals under standardized nutritional conditions can help shed light on this debate. Here we quantify individual variation in metabolic efficiency in terms of the amount of adenosine triphosphate (ATP) generated per molecule of oxygen consumed by liver and muscle mitochondria and examine its effects, both on the rate of protein synthesis within these tissues and on the rate of whole-body growth of individually fed juvenile brown trout (Salmo trutta) receiving either a high or low food ration. As expected, fish on the high ration on average gained more in body mass and protein content than those maintained on the low ration. Yet, growth performance varied more than 10-fold among individuals on the same ration, resulting in some fish on low rations growing faster than others on the high ration. This variation in growth for a given ration was related to individual differences in mitochondrial properties: a high whole-body growth performance was associated with high mitochondrial efficiency of ATP production in the liver. Our results show for the first time, to our knowledge, that among-individual variation in the efficiency with which substrates are converted into ATP can help explain marked variation in growth performance, independent of food intake. This study highlights the existence of inter-individual differences in mitochondrial efficiency and its potential importance in explaining intraspecific variation in whole-animal performance.

Keywords: ATP/O ratio; brown trout; energy metabolism; intraspecific; mitochondrial plasticity; protein synthesis.

Figure 1.

Relationship between the fractional rate of protein synthesis (Ks) in the muscle and mitochondrial efficiency (ATP/O ratio) in the liver of juvenile brown trout at low versus high food intake. Continuous lines show significant effect. n = 28–30 fish per food level. See table 1 for statistical analyses.

Figure 2.

Relationships between indices of growth performance and mitochondrial efficiency (ATP/O ratio) in juvenile brown trout at low versus high food levels. (a) Specific growth rate in relation to liver ATP/O ratio, and (b) growth efficiency in relation to liver ATP/O ratio. Continuous lines show significant effects. n = 29–30 fish per food level. See table 2 for statistical analyses. (a) Plotted are partial residuals of specific growth rate for fish at high food ration evaluated at mean initial body mass = 9.59 g. (b) Plotted are partial residuals of growth efficiency evaluated at mean initial body mass = 9.02 mg.