Understanding diversity in oxidative status and oxidative stress: the opportunities and challenges ahead

Abstract

Oxidative stress may be of profound biological relevance. In this Commentary, I discuss some key issues faced by the emerging field of oxidative stress ecology, and seek to provide interpretations and solutions. First, I show that the way in which we define oxidative stress has far-reaching implications for the interpretation of results, and that we need to distinguish between (1) a biochemical definition in terms of the molecular outcomes of oxidative stress (e.g. generation of oxidative damage) and (2) a biological definition in terms of the fitness consequences for the organism (e.g. effects on fertility). Second, I discuss the dangers of comparing different tissues and markers. Third, I highlight the need to pay more attention to the cross-talk between oxidative stress and other important physiological costs and functions; this will allow us to better understand the mechanistic basis of fitness costs. Fourth, I propose the ‘redox signalling hypothesis’ of life history to complement the current ‘oxidative stress hypothesis’ of life history. The latter states that oxidative damage underlies trade-offs because it affects traits like growth, reproduction or cell senescence. By contrast, the redox signalling hypothesis states that a trade-off between signalling and biochemical oxidative stress underlies the regulation of reactive oxygen species production and their subsequent control. Finally, I critically appraise our current knowledge of oxidative stress ecology, highlighting key research themes and providing an optimistic overview of future opportunities for the discipline to yield considerable insight into the ecological and evolutionary meaning of oxidative stress.

Metabolic costs of altered growth trajectories across life transitions in amphibians

“…Galli et al, ). At catch‐up point, lipid peroxidation was lower at 18:6 cycles, probably indicating the benefits (less ROS) of having activated the antioxidant machinery (Costantini, ). Alternatively, lower MDA levels may indicate a lower accumulation of fat reserves in larvae (Burraco, Iglesias‐Carrasco, Cabido, & Gomez‐Mestre, ; Pérez‐Rodríguez et al, ), reflected also in the positive relationship between MDA levels and body mass at this point.…”

“…This may indicate that accelerating growth close to maximum capacity throughout the entire development can imply a high catabolic demand at life transitions (Metcalfe & Alonso‐Alvarez, ). However, such increases in antioxidant enzyme activities may not incur in later performance costs for individuals since compensatory responses seemed not to generate lipid damages or lower antioxidant levels (Costantini, ). At metamorphosis, individuals compensating for delayed hatching had lower MDA levels, which may indicate scarce lipid peroxidation favoured by antioxidant activities.…”

“…Previous studies have detected alterations in the redox machinery across taxa, as for instances in zebra finches (Alonso‐Alvarez et al, ), sticklebacks (Kim et al, ) or damselflies (De Block & Stoks, ). Perturbations in the redox status at early life can have carry‐over effects in vertebrates, such as reductions in reproduction investment or in life expectancy (Metcalfe & Alonso‐Alvarez, ; Monaghan et al, ), although long‐term studies are need to fully elucidated this question (Costantini, ).…”

“…We quantified the activity of three antioxidant enzymes: catalase (CAT), glutathione peroxidase (GPx) and glutathione reductase (GR). Antioxidant enzymes are the main defence against ROS in animals, and they protect cells from oxidative injuries (Costantini, ). We also quantified lipid peroxidation by measuring malondialdehyde (MDA) and total reduced glutathione (GSH t ) levels.…”

“…These hormones activate a cascade of catabolic routes that can unbalance the redox status of organisms and overproduce reactive oxygen species (ROS), damaging essential biomolecules like proteins or DNA (Monaghan, Metcalfe, & Torres, ). The alteration of these metabolic routes can reduce individual health and fitness (Costantini, , ; Crespi et al, ). For instance, birds compensating losses in growth experience oxidative stress and reduced immunocompetence (Alonso‐Alvarez, Bertrand, Faivre, & Sorci, ), and similar responses have been detected in insects (De Block & Stoks, , ) and fish (Kim, Noguera, & Velando, ).…”