Oxidative stress and life histories: unresolved issues and current needs

Life-history theory concerns the trade-offs that mold the patterns of investment by animals between reproduction, growth, and survival. It is widely recognized that physiology plays a role in the mediation of life-history trade-offs, but the details remain obscure. As life-history theory concerns aspects of investment in the soma that influence survival, understanding the physiological basis of life histories is related, but not identical, to understanding the process of aging. One idea from the field of aging that has gained considerable traction in the area of life histories is that life-history trade-offs may be mediated by free radical production and oxidative stress. We outline here developments in this field and summarize a number of important unresolved issues that may guide future research efforts. The issues are as follows. First, different tissues and macromolecular targets of oxidative stress respond differently during reproduction. The functional significance of these changes, however, remains uncertain. Consequently there is a need for studies that link oxidative stress measurements to functional outcomes, such as survival. Second, measurements of oxidative stress are often highly invasive or terminal. Terminal studies of oxidative stress in wild animals, where detailed life-history information is available, cannot generally be performed without compromising the aims of the studies that generated the life-history data. There is a need therefore for novel non-invasive measurements of multi-tissue oxidative stress. Third, laboratory studies provide unrivaled opportunities for experimental manipulation but may fail to expose the physiology underpinning life-history effects, because of the benign laboratory environment. Fourth, the idea that oxidative stress might underlie life-history trade-offs does not make specific enough predictions that are amenable to testing. Moreover, there is a paucity of good alternative theoretical models on which contrasting predictions might be based. Fifth, there is an enormous diversity of life-history variation to test the idea that oxidative stress may be a key mediator. So far we have only scratched the surface. Broadening the scope may reveal new strategies linked to the processes of oxidative damage and repair. Finally, understanding the trade-offs in life histories and understanding the process of aging are related but not identical questions. Scientists inhabiting these two spheres of activity seldom collide, yet they have much to learn from each other

Carotenoids and the costs of reproduction Studies on the lesser black-backed gull

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Warning displays may function as honest signals of toxicity

Many prey species use colourful 'aposematic' signalling to advertise the fact that they are toxic. Some recent studies have shown that the brightness of aposematic displays correlates positively with the strength of toxicity, suggesting that aposematic displays are a form of handicap signal, the conspicuousness of which reliably indicates the level of toxicity. The theoretical consensus in the literature is, however, at odds with this finding. It is commonly assumed that the most toxic prey should have less bright advertisements because they have better chances of surviving attacks and can therefore reduce the costs incurred by signalling. Using a novel theoretical model, we show that aposematic signals can indeed function as handicaps. To generate this prediction, we make a key assumption that the expression of bright displays and the storage of anti-predator toxins compete for resources within prey individuals. One shared currency is energy. However, competition for antioxidant molecules, which serve dual roles as pigments and in protecting prey against oxidative stress when they accumulate toxins, provides a specific candidate resource that could explain signal honesty. Thus, contrary to the prevailing theoretical orthodoxy, warning displays may in fact be honest signals of the level of (rather than simply the existence of) toxicit

Warning displays may function as honest signals of toxicity

Many prey species use colourful ‘aposematic’ signalling to advertise the fact that they are toxic. Some recent studies have shown that the brightness of aposematic displays correlates positively with the strength of toxicity, suggesting that aposematic displays are a form of handicap signal, the conspicuousness of which reliably indicates the level of toxicity. The theoretical consensus in the literature is, however, at odds with this finding. It is commonly assumed that the most toxic prey should have less bright advertisements because they have better chances of surviving attacks and can therefore reduce the costs incurred by signalling. Using a novel theoretical model, we show that aposematic signals can indeed function as handicaps. To generate this prediction, we make a key assumption that the expression of bright displays and the storage of anti-predator toxins compete for resources within prey individuals. One shared currency is energy. However, competition for antioxidant molecules, which serve dual roles as pigments and in protecting prey against oxidative stress when they accumulate toxins, provides a specific candidate resource that could explain signal honesty. Thus, contrary to the prevailing theoretical orthodoxy, warning displays may in fact be honest signals of the level of (rather than simply the existence of) toxicity

Oxidative damage, ageing, and life-history evolution: where now?

The idea that resources are limited and animals can maximise fitness by trading costly activities off against one another forms the basis of life-history theory. Although investment in reproduction or growth negatively affects survival, the mechanisms underlying such trade-offs remain obscure. One plausible mechanism is oxidative damage to proteins, lipids, and nucleic acids caused by reactive oxygen species (ROS). Here, we critically evaluate the premise that ROS-induced oxidative damage shapes life history, focussing on birds and mammals, and highlight the importance of ecological studies examining free-living animals within this experimental framework. We conclude by emphasising the value of using multiple assays to determine oxidative protection and damage. We also highlight the importance of using standardised and appropriate protocols, and discuss future research directions

Telomere length in early life predicts lifespan

The attrition of telomeres, the ends of eukaryote chromosomes, is thought to play an important role in cell deterioration with advancing age. The observed variation in telomere length among individuals of the same age is therefore thought to be related to variation in potential longevity. Studies of this relationship are hampered by the time scale over which individuals need to be followed, particularly in long-lived species where lifespan variation is greatest. So far, data are based either on simple comparisons of telomere length among different age classes or on individuals whose telomere length is measured at most twice and whose subsequent survival is monitored for only a short proportion of the typical lifespan. Both approaches are subject to bias. Key studies, in which telomere length is tracked from early in life, and actual lifespan recorded, have been lacking. We measured telomere length in zebra finches (n = 99) from the nestling stage and at various points thereafter, and recorded their natural lifespan (which varied from less than 1 to almost 9 y). We found telomere length at 25 d to be a very strong predictor of realized lifespan (P < 0.001); those individuals living longest had relatively long telomeres at all points at which they were measured. Reproduction increased adult telomere loss, but this effect appeared transient and did not influence survival. Our results provide the strongest evidence available of the relationship between telomere length and lifespan and emphasize the importance of understanding factors that determine early life telomere length

The price of defence:toxins, visual signals and oxidative state in an aposematic butterfly

In a variety of aposematic species, the conspicuousness of an individual's warning signal and the quantity of its chemical defence are positively correlated. This apparent honest signalling is predicted by resource competition models which assume that the production and maintenance of aposematic defences compete for access to antioxidant molecules that have dual functions as pigments and in protecting against oxidative damage. To test for such trade-offs, we raised monarch butterflies (Danaus plexippus) on different species of their milkweed host plants (Apocynaceae) that vary in quantities of cardenolides to test whether (i) the sequestration of cardenolides as a secondary defence is associated with costs in the form of oxidative lipid damage and reduced antioxidant defences; and (ii) lower oxidative state is associated with a reduced capacity to produce aposematic displays. In male monarchs conspicuousness was explained by an interaction between oxidative damage and sequestration: males with high levels of oxidative damage became less conspicuous with increased sequestration of cardenolides, whereas those with low oxidative damage became more conspicuous with increased levels of cardenolides. There was no significant effect of oxidative damage or concentration of sequestered cardenolides on female conspicuousness. Our results demonstrate a physiological linkage between the production of coloration and oxidative state, and differential costs of sequestration and signalling in monarch butterflies