Differences in mitochondrial efficiency explain individual variation in growth performance

Type Article
Date 2019-08
Language English
Author(s) Salin KarineORCID1, Villasevil Eugenia M.1, Anderson Graeme J.1, Lamarre Simon G.2, Melanson Chloe A.2, McCarthy Ian3, Selman Colin1, Metcalfe Neil B.1
Affiliation(s) 1 : Univ Glasgow, Inst Biodivers Anim Hlth & Comparat Med, Glasgow G12 8QQ, Lanark, Scotland.
2 : Univ Moncton, Dept Biol, Moncton, NB E1A 3E9, Canada.
3 : Bangor Univ, Sch Ocean Sci, Menai Bridge LL59 5AB, Gwynedd, Wales.
Source Proceedings Of The Royal Society B-biological Sciences (0962-8452) (Royal Soc), 2019-08 , Vol. 286 , N. 1909 , P. 8p.
DOI 10.1098/rspb.2019.1466
WOS© Times Cited 13
Keyword(s) ATP/O ratio, brown trout, energy metabolism, intraspecific, mitochondrial plasticity, protein synthesis
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.

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Salin Karine, Villasevil Eugenia M., Anderson Graeme J., Lamarre Simon G., Melanson Chloe A., McCarthy Ian, Selman Colin, Metcalfe Neil B. (2019). Differences in mitochondrial efficiency explain individual variation in growth performance. Proceedings Of The Royal Society B-biological Sciences, 286(1909), 8p. Publisher's official version : https://doi.org/10.1098/rspb.2019.1466 , Open Access version : https://archimer.ifremer.fr/doc/00512/62368/