Periodic Reporting for period 4 - MitoWild (Counting the cost of living: mitochondrial efficiency, environmental conditions, and performance in the wild)
Periodo di rendicontazione: 2024-04-01 al 2025-03-31
An organism’s metabolic rate is a central trait that links its physiology with its ecology and life history. However, while textbook definitions of metabolic rate generally refer to the rate of energy use by the animal, most empirical studies instead record it very indirectly as whole-animal oxygen consumption rate, without any actual measurement of the rate of production of the energy molecule ATP. This approach contains a conceptual weakness: it is equivalent to estimating a car’s capacity or efficiency by measuring its fuel consumption per minute, with no measurement of what that consumption actually achieves in terms of speed or distance travelled. This can significantly weaken our ability to link metabolic rates to ecological processes, and may explain why conventional measures of metabolic rate often do not predict performance or fitness. This project therefore attempted to re-dress the balance by shifting the focus onto the efficiency with which mitochondria produce ATP, which has led to completely new insights into how metabolic rate influences and constrains the behaviour and ecology of animals. The project examined the impact of metabolic efficiency on performance and the trade-off between efficiency and rates of senescence, using freshwater fish as an experimental system. Performance was measured in a wide range of relevant ecological contexts (e.g. feeding, competing for territories, providing parental care, swimming).
The start-up phase of the project involved recruiting and training the team, setting up the aquarium rooms, testing protocols for whole-animal measurements of animal performance (e.g. locomotor performance), developing methods for quantifying use of refuges (using PIT tag detectors embedded in refuges) and use of energy (by means of changes in body shape assessed from analysis of photographs), developing methods for mitochondrial respirometry, collecting fish, testing the assays and conducting the first experiments. The covid outbreak caused a significant interruption to the programme of work, but once life returned to near-normal the experimental programme was rearranged and modified, with only minor omissions from the original plan.
The project successfully measured performance in a range of ecological contexts (e.g. swimming against variable water flow rates, defending feeding territories in semi-natural streams, competing for food and mates, performing parental care etc), and demonstrated that the efficiency of ATP production by the mitochondria varies substantially between individual animals of the same age and species, and that this variation often (but not always) predicts how well the animal can perform. For instance, fish with more efficient mitochondria tended to be socially dominant, were better at defending a feeding territory, and were better at providing parental care. They also consumed larger meals and grew faster – but only when environmental conditions were more challenging. This has allowed a re-evaluation of the links between ecology and metabolic rate. This work is either already published, submitted for publication or in an advanced state of analysis and write-up.
The project successfully measured performance in a range of ecological contexts (e.g. swimming against variable water flow rates, defending feeding territories in semi-natural streams, competing for food and mates, performing parental care etc), and demonstrated that the efficiency of ATP production by the mitochondria varies substantially between individual animals of the same age and species, and that this variation often (but not always) predicts how well the animal can perform. For instance, fish with more efficient mitochondria tended to be socially dominant, were better at defending a feeding territory, and were better at providing parental care. They also consumed larger meals and grew faster – but only when environmental conditions were more challenging. This has allowed a re-evaluation of the links between ecology and metabolic rate. This work is either already published, submitted for publication or in an advanced state of analysis and write-up.
The project used new techniques for measurement of both ATP production and the production of reactive oxygen species (ROS) by the mitochondria. These approaches were used to examine the impact of metabolic efficiency on performance and the trade-off between efficiency and rates of senescence, using freshwater fish as an experimental system. By applying cutting-edge methods, so far only used on laboratory animals, to animals of wild origin living in semi-natural habitats, the project has revealed for the first time how environmental conditions select for particular mitochondrial phenotypes and hence metabolic efficiency, so allowing a re-evaluation of the links between ecology and metabolic rate.