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.

What do warming waters mean for fish physiology and fisheries?

“…The thermodynamically mediated increase in ATP demand in response to warming is therefore exacerbated by reduced mitochondrial efficiency. Consequently, greater amounts of food‐derived substrates and oxygen are required to produce the same amount of ATP to meet this demand (Salin et al ., 2019).…”

“…Oxygen supply and mitochondrial ATP production can influence growth rates. For example, increased mitochondrial inefficiency led to decreased growth rates in trout ( Salmo trutta , Linnaeus, 1758) (Salin et al ., 2019). Increased mitochondrial inefficiency means that less biomass is produced for a given amount of food eaten.…”

“…Therefore, the stoichiometry between food intake and ATP produced is not constant. The varying extent of mitochondrial efficiency has obvious repercussions for ATP supply to energy‐consuming processes such as movement and growth (Salin et al ., 2012, 2019). Mitochondrial characteristics of individuals can thereby scale up to movement of populations and population dynamics.…”

Climate change and ageing in ectotherms

“…These mechanisms might either prevent damage in cells by reducing the generation of ROS, or repair the damage already caused. Both metabolic rate, usually measured in terms of whole‐body oxygen consumption, and mitochondrial efficiency, defined as the amount of ATP generated per molecule of oxygen consumed, show great within‐ and among‐individual variation, and can change in response to environmental conditions (Salin, Auer, Rey, Selman, & Metcalfe, 2015; Salin et al., 2019). Metabolic plasticity at the organelle and tissue/organ level may allow organisms to adjust ROS production to increase their resilience to climate change (Norin & Metcalfe, 2019; Seebacher et al., 2015).…”

Mitochondrial behaviour, morphology, and animal performance

“…For example, Salin et al . () recently showed that individual differences in the growth rate of brown trout ( Salmo trutta ) are correlated with the efficiency of ATP production by the liver. While recent studies have made great strides in understanding the relationship between energy production and whole‐animal performance, there is still considerable, unexplained variation in performance among individuals and species.…”