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

We age because we grow

Why do we age? Since ageing is a near-universal feature of complex organisms, a convincing theory must provide a robust evolutionary explanation for its ubiquity. This theory should be compatible with the physiological evidence that ageing is largely due to deterioration, which is, in principle, reversible through repair. Moreover, this theory should also explain why natural selection has favoured organisms that first improve with age (mortality rates decrease) and then deteriorate with age (mortality rates rise). We present a candidate for such a theory of life history, applied initially to a species with determinate growth. The model features both the quantity and the quality of somatic capital, where it is optimal to initially build up quantity, but to allow quality to deteriorate. The main theoretical result of the paper is that a life history where mortality decreases early in life and then increases late in life is evolutionarily optimal. In order to apply the model to humans, in particular, we include a budget constraint to allow intergenerational transfers. The resultant theory then accounts for all our basic demographic characteristics, including menopause with extended survival after reproduction has ceased

Testing evolutionary theories of menopause

Why do women cease fertility rather abruptly through menopause at an age well before generalized senescence renders child rearing biologically impossible? The two main evolutionary hypotheses are that menopause serves either (i) to protect mothers from rising age-specific maternal mortality risks, thereby protecting their highly dependent younger children from death if the mother dies or (ii) to provide post-reproductive grandmothers who enhance their inclusive fitness by helping to care and provide for their daughters' children. Recent theoretical work indicates that both factors together are necessary if menopause is to provide an evolutionary advantage. However, these ideas need to be tested using detailed data from actual human life histories lived under reasonably ‘natural’ conditions; for obvious reasons, such data are extremely scarce. We here describe a study based on a remarkably complete dataset from The Gambia. The data provided quantitative estimates for key parameters for the theoretical model, which were then used to assess the actual effects on fitness. Empirically based numerical analysis of this nature is essential if the enigma of menopause is to be explained satisfactorily in evolutionary terms. Our results point to the distinctive (and perhaps unique) role of menopause in human evolution and provide important support for the hypothesized evolutionary significance of grandmothers