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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.

SUBMITTER: Salin K

PROVIDER: S-EPMC6732382 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Differences in mitochondrial efficiency explain individual variation in growth performance.

Salin Karine K Villasevil Eugenia M EM Anderson Graeme J GJ Lamarre Simon G SG Melanson Chloé A CA McCarthy Ian I Selman Colin C Metcalfe Neil B NB

Proceedings. Biological sciences 20190821 1909

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 t ...[more]

PMID: 31431161

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Project description:Individual stress coping style has profound effects on how animals respond to environmental change, and individuals within a population strikingly differ in how gene expression shifts in response to challenge. This study used a wild type Zebrafish (Danio rerio) population to: 1) identify and screen for individual coping style using a screening protocol for risk taking in groups and 2) do global transcriptomics of brains from proactive, reactive or randomly chosen individuals (n=10/group) under control conditions. Results show that within our population proactive and reactive individual coping styles can be accurately identified and may represent 10-30% of individuals within the population. Microarray data analyses identify fundamental differences between the three different groups where variance in gene expression values are reduced by using coping style as an explanatory variable. Furthermore, significant differences in mRNAs and related biological processes suggest that even under identical environmental conditions the molecular mechanisms that underpin physiological processes are very different between proactive and reactive individuals within a population. Experimental tank was an 18 litre glass aquarium (dimensions (LxWxH): 40 X 25 X 20cm) lined on three sides with white paper; the front wall was not covered to allow the observer to record the behaviour and divided at 1/3 of his length with a black PVC screen with a 3cm diameter hole in the middle. All the tank surfaces around this third area of the tank were covered with dark paper and closed on the upper part with a removable lid to provide a shelter for the animals. The hole was covered with the same PVC plastic material and removed once the screening started to allow the fish enter the novel environment. Food was not supplied the day before to ensure that during the test the fish were hungry and they had to make the decision to leave a safe area in order to forage. Boldness was measured as the time taken by individual fish to leave a group from a safe, darkened area. It hence represents the willingness of a fish to explore a new, potentially dangerous environment, or boldness. Tests were conducted with groups of 9 randomly-selected fish from stocking tanks. Fish were familiar to each other in the sense that they were previously held in the same stocking tank. Test started with a 10 min. habituation period in the sheltered area with the hole closed with a PVC screen and the top of the sheltered area of the tank also covered to provide a complete quiet place. Then the lid covering the hole was gently removed. Either the first 3 fish to exit the shelter or fish with latency times inferior to 10 minutes were considered bold fish and were removed gently with a fish net from the test tank and placed apart in another tank. Latency times of emergency from the sheltered area were recorded individually. Next 3 animals to emerge before 15 minutes were considered intermediate and also removed gently. At the end of this last 15 minutes, animals that still remained inside the sheltered area were considered shy. Intermediates were discarded and fish selected for different coping strategies where placed in different tanks for posterior molecular analysis. Selected animals were killed by an overdose of MS-22 and the brains were sampled. Individual tissue samples were homogenized into 0.3 ml of Tri-Reagent and stored at -80C for further molecular analysis.

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Differences in mitochondrial efficiency explain individual variation in growth performance.

Publications

Differences in mitochondrial efficiency explain individual variation in growth performance.

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