Abstract
It is often assumed that an animal's metabolic rate can be estimated through measuring the whole-organism oxygen consumption rate. However, oxygen consumption alone is unlikely to be a sufficient marker of energy metabolism in many situations. This is due to the inherent variability in the link between oxidation and phosphorylation; that is, the amount of adenosine triphosphate (ATP) generated per molecule of oxygen consumed by mitochondria (P/O ratio). In this article, we describe how the P/O ratio can vary within and among individuals, and in response to a number of environmental parameters, including diet and temperature. As the P/O ratio affects the efficiency of cellular energy production, its variability may have significant consequences for animal performance, such as growth rate and reproductive output. We explore the adaptive significance of such variability and hypothesize that while a reduction in the P/O ratio is energetically costly, it may be associated with advantages in terms of somatic maintenance through reduced production of reactive oxygen species. Finally, we discuss how considering variation in mitochondrial efficiency, together with whole-organism oxygen consumption, can permit a better understanding of the relationship between energy metabolism and life history for studies in evolutionary ecology.
Highlights
Scientists have long acknowledged the importance of estimating an animal’s metabolic rate, given its potential impact on the rate of resource uptake from the environment and allocation of those resources [1,2,3,4]
Studies across a broad range of taxa have shown that intraspecific variation in the rate of oxygen consumption is related to performance across a diverse range of traits including work output [5,6], growth rate [7], degree of aggressiveness [8], feeding rate [9], lactation capacity [10] and lifespan [11,12,13]
The goal of this review is to emphasize the importance of considering mitochondrial function together with the rate of oxygen consumption when investigating the link between energy metabolism and animal performance
Summary
Scientists have long acknowledged the importance of estimating an animal’s metabolic rate, given its potential impact on the rate of resource uptake from the environment and allocation of those resources [1,2,3,4]. The association between oxygen consumption and performance is not straightforward, with studies reporting positive, negative or no relationship, depending on the species and trait investigated (reviewed in [14]). While these inconsistent findings are triggering extensive debates centred on theoretical and methodological issues [11,14,15,16,17,18,19,20,21], what is often overlooked is that whole-organism oxygen consumption may be only a partial proxy for energy metabolism.
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