Oxidative stress as a life‐history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death

Abstract

Summary: 1. Oxidative stress is usually defined as an imbalance arising when the rate of production of reactive oxygen species (ROS) exceeds the capacity of the antioxidant defence and repair mechanisms, leading to oxidative damage to biomolecules, but the concept can be expanded to include the disruption of reduction : oxidation (redox) reactions involved in cellular signalling. In this review, we consider how the need to circumvent oxidation may shape the phenotypes of organisms throughout their life and that of their offspring, underpinning a diverse range of life‐history trade‐offs. 2. A recent explosion of interest in this field has shown that both ROS production and the capacity of animals to deal with it change from early development through to adulthood, and vary with environmental conditions and lifestyle. Oxidative stress may both stimulate and be caused by reproduction, although direct evidence of either process is surprisingly weak. Many forms of secondary sexual traits may signal the individual’s oxidative balance to potential mates, but the underlying mechanisms are still debated. 3. Germline cells may be especially vulnerable to oxidative stress, leading to transgenerational effects on offspring viability and possible consequences for the evolution of mate choice. 4. Both antioxidant defences and the ability to repair oxidative damage tend to decline with old age, contributing to cellular and whole organism senescence. This increasing vulnerability to oxidative stress, although little studied, appears especially marked in sexually selected traits. 5. Challenges for the future include the incorporation of longitudinal approaches into experiments that analyse oxidative balance over an individual’s lifetime (preferably under near‐natural conditions), the exploration of the genetic basis for trade‐offs involving oxidative stress, the assimilation of current redox signalling knowledge, and the study of the consequences of heritable oxidative damage to germline DNA.