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The ecology of metabolic phenotypes: from cells to populations

Final Report Summary - METAPHEN (The ecology of metabolic phenotypes: from cells to populations)

This project aimed to explore the causes and consequences of variation in metabolic rate among individuals of the same species. All species of animal that have so far been studied have been found to have up to 3-fold variation in their metabolic rate, even among individuals of the same size, age, sex and nutritional history. The persistence of this level of variation in a trait presumed to have significant effects on fitness (since a higher metabolic rate implies a higher cost of living) has been a puzzle for some years. In this project we explored the cellular causes of this variation, and its ecological consequences, using studies on fish (primarily the salmonids Brown trout Salmo salar and Atlantic salmon S. salar). We developed new techniques to address these questions, and conducted experiments in both the laboratory and field in a broad-scale and innovative approach that made significant advances in the field of eco-physiology.
Mitochondria lie at the heart of an animal’s metabolism – they are the tiny structures in the body’s cells that convert food into a form of energy (known as ATP) that can be used to power all of the activities of the cell. This conversion uses up oxygen – but we discovered that the efficiency with which the mitochondria use oxygen to produce ATP varies greatly between individual fish, with some being twice as efficient as others. This variation in efficiency explains why some individuals are able to grow faster than others when eating the same amount of food. Variation in the way that the mitochondria work also influences how much food can be eaten per day – but the cost of having very efficient mitochondria is that they then produce more of the damaging free radicals that cause damage to the cells. So the animal with the most efficient mitochondria is also the one whose cells are potentially becoming most damaged, which may mean that they age faster.
The mitochondria also have an influence on the metabolic rate of the whole animal, since this is measured in terms of the rate of oxygen consumption. So animals with inefficient mitochondria have higher metabolic rates. The metabolic rate of a fish influences the amount of food it can eat and hence the rate at which it can grow. However, some individuals are able to modify their metabolic rate when conditions change, and this gives them an advantage in terms of growth rate and energy conservation (although there may be as yet unknown costs associated with this). Juvenile salmon with higher metabolic rates were found to have higher survival rates in the wild, but this was dependent on food availability in the streams in which they live; variation in metabolic rate was much more important when food was limiting, possibly because a high metabolic rate is associated with a greater competitive ability.
In summary, the variation in metabolic rates that we see in the natural world is almost certainly maintained because there is no one optimal metabolic rate, and different environments are favouring different rates of metabolism. These patterns are only apparent when we look at the mitochondria, which are the drivers of this variation.