Metabolic cold adaptation in fishes occurs at the level of whole animal, mitochondria and enzyme

Abstract

Metabolic cold adaptation (MCA), the hypothesis that species from cold climates have relatively higher metabolic rates than those from warm climates, was first proposed nearly 100 years ago and remains one of the most controversial hypotheses in physiological ecology. In the present study, we test the MCA hypothesis in fishes at the level of whole animal, mitochondria and enzyme. In support of the MCA hypothesis, we find that when normalized to a common temperature, species with ranges that extend to high latitude (cooler climates) have high aerobic enzyme (citrate synthase) activity, high rates of mitochondrial respiration and high standard metabolic rates. Metabolic compensation for the global temperature gradient is not complete however, so when measured at their habitat temperature species from high latitude have lower absolute rates of metabolism than species from low latitudes. Evolutionary adaptation and thermal plasticity are therefore insufficient to completely overcome the acute thermodynamic effects of temperature, at least in fishes.

Dynamic changes in cardiac mitochondrial metabolism during warm acclimation in rainbow trout

“…This could indicate that dysfunctional mitochondria had been eliminated from the cell after day 2. In fish, mitochondrial volume density varies with water temperature and thermal acclimation can induce changes in the cristae surface density of mitochondria as well as mitochondrial volume density (Dhillon and Schulte, 2011;Guderley, 2004;Guderley and Johnston, 1996;Guderley et al, 1997;St-Pierre et al, 1998;Tyler and Sidell, 1984;White et al, 2012) but how and when such changes occur during the acclimation process is unknown. Two different mechanisms are believed to be used by the cell to ensure mitochondrial homeostasis and survival; apoptosis and mitophagy but, to the best of our knowledge, none of these has been considered in the context of thermal acclimation.…”

“…Such thermal responses at the whole-animal level can be linked to the need to redirect fuel reserves to power the metabolic pathways leading to the aerobic production of ATP by mitochondria (Iftikar and Hickey, 2013). Indeed, mitochondrial oxygen consumption and citrate synthase (CS) activity (a key enzyme of the tricarboxylic acid cycle and a proxy for aerobic metabolism) have been shown to follow a similar pattern as the whole-animal metabolic rate during both acute and chronic temperature changes, although on a different scale (White et al, 2012). Specifically, acute warming of either whole animals (in vivo) or isolated tissues (in vitro) from ectotherms generally leads to an increase in mitochondrial oxygen consumption rates and in the overall catalytic capacities of metabolic enzymes (Hochachka and Somero, 1973).…”

The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment

“…For example, multiple studies have documented correlations between aerobic metabolic functions and gradients of latitude and altitude (Angilletta et al, 2002;Fontanillas et al, 2005;Pörtner, 2006;Hassanin et al, 2009;Cheviron and Brumfield, 2009;Scott et al, 2011;Toews et al, 2014;Stager et al, 2014). Similarly, many studies have demonstrated that variation in aerobic metabolism measured at the tissue and whole-organism levels are associated with differences in performance and fitness, or correlates of fitness (Pörtner and Knust, 2007;Farrell et al, 2008;Eliason et al, 2011;Zera, 2011;White et al, 2012;Rauhamäki et al, 2014). Also, genetic variation at the levels of the mitochondrion has been associated with differences in fitness (Rand, 2001;Ballard and Whitlock, 2004;Blier et al, 2013).…”

The repeatability of metabolic rate declines with time

“…Metabolic rate is one of the most widely measured physiological traits, with data available for hundreds of species of mammal (McNab, 2008), bird (McNab, 2009), reptile (White et al, 2006), amphibian (White et al, 2006), fish (Clarke and Johnston, 1999;White et al, 2012a), insect (Chown et al, 2007) and a host of other organisms (Makarieva et al, 2008;White et al, 2012b). These comparative databases have revealed considerable diversity between species, with similarly sized species differing severalfold in some cases (e.g.…”