Mitochondrial uncoupling as a regulator of life history trajectories in birds: An experimental study in the zebra finch

Abstract

Mitochondria have a fundamental role in the transduction of energy from food into ATP. The coupling between food oxidation and ATP production is never perfect, but may nevertheless be of evolutionary significance. The 'uncoupling to survive' hypothesis suggests that 'mild' mitochondrial uncoupling evolved as a protective mechanism against the excessive production of damaging reactive oxygen species (ROS). Because resource allocation and ROS production are thought to shape animal life histories, alternative life-history trajectories might be driven by individual variation in the degree of mitochondrial uncoupling. We tested this hypothesis in a small bird species, the zebra finch (Taeniopygia guttata), by treating adults with the artificial mitochondrial uncoupler 2,4-dinitrophenol (DNP) over a 32-month period. In agreement with our expectations, the uncoupling treatment increased metabolic rate. However, we found no evidence that treated birds enjoyed lower oxidative stress levels or greater survival rates, in contrast to previous results in other taxa. In vitro experiments revealed lower sensitivity of ROS production to DNP in mitochondria isolated from skeletal muscles of zebra finch than mouse. In addition, we found significant reductions in the number of eggs laid and in the inflammatory immune response in treated birds. Altogether, our data suggest that the 'uncoupling to survive' hypothesis may not be applicable for zebra finches, presumably because of lower effects of mitochondrial uncoupling on mitochondrial ROS production in birds than in mammals. Nevertheless, mitochondrial uncoupling appeared to be a potential life-history regulator of traits such as fecundity and immunity at adulthood, even with food supplied ad libitum.

Integrative Approaches for Studying Mitochondrial and Nuclear Genome Co-evolution in Oxidative Phosphorylation

“…Fitness/metabolic performance of organisms with diverged mitolineages measured in different environments can indicate the presence of local metabolic adaptation, whereas fitness/metabolic performance of several generations of crosses can show whether mitonuclear incompatibilities have evolved between lineages. Organismal level: Heat produced from less-coupled mitochondria may be adaptive in colder environments for endothermic organisms (Pörtner et al, 1998); individuals with less-coupled metabolism are expected to produce fewer ATP molecules (leading to lower amount of energy available for growth, immune function, or reproduction) and fewer ROS (leading to lower oxidative stress and greater longevity) per unit of O 2 /nutrients consumed (Stier et al, 2014a,b). Higher O 2 /nutrient consumption could be expected to compensate for metabolic inefficiency.…”

“…In the wild, OXPHOS traits have been correlated with a wide range of environmental pressures, including heat stress (Morales et al, 2016a,b), cold stress (Cheviron et al, 2014; Stier et al, 2014a,b), nutrient limitation (da Fonseca et al, 2008), and hypoxia (da Fonseca et al, 2008; Scott et al, 2011). Consistently, there is evidence for positive selection and climate-linked differences in the sequences and expression of OXPHOS genes in a range of animal species with wide biogeographic ranges (Mishmar et al, 2003; Ruiz-Pesini et al, 2004; Toews and Brelsford, 2012; Garvin et al, 2015; Morales et al, 2016a).…”

“…It is proposed that the heat produced from less-coupled mitochondria may be particularly beneficial for adaptation of endothermic organisms to colder environments. In contrast, heat production may be deleterious in warm environments, necessitate higher nutritional intake, and is associated with high oxidative stress due to increased ROS production ( Figure 1 ) (Pörtner et al, 1998; Brand, 2000; Somero, 2002; Fangue et al, 2009; Stier et al, 2014a,b). It is important to account for variation in such predictions among organisms and environments.…”

Current versus future reproduction and longevity: a re-evaluation of predictions and mechanisms

“…The P/O ratio measures the relative coupling efficiency of the mitochondria, which constrains mechanistic models of the electron-transport chain and ATP synthase (Brand, 2005;Salin et al, 2015a). Mitochondrial coupling may contribute to individual differences in performance for select life-history variables, such as growth and ageing Salin et al, 2012; but see Stier et al, 2014) -its role in the interaction among life-history variables warrants further study. Another advantage of the P/O ratio is that it can allow identification of the energy substrate used by mitochondria owing to the different respiratory quotients of different substrates (Salin et al, 2015a).…”

How to measure mitochondrial function in birds using red blood cells: a case study in the king penguin and perspectives in ecology and evolution

“…; Hill ; Stier et al . ,b; Stier, Massemin & Criscuolo ; Salin et al . ; Schwartz, Arendsee & Bronikowski ; Bar‐Yaacov et al .…”