The role of oxidative stress as an underlying mechanism in life-history trade-offs

A key aspect underpinning life-history theory is the existence of trade-offs. Trade-offs occur because resources are limited, meaning that individuals cannot invest in all traits simultaneously, leading to costs for traits such as growth and reproduction. Such costs may be the reason for the sub-maximal growth rates that are often observed in nature, though the fitness consequences of these costs would depend on the effects on lifetime reproductive success. Recently, much attention has been given to the physiological mechanism that might underlie these life-history trade-offs, with oxidative stress (OS) playing a key role. OS is characterised by a build-up of oxidative damage to tissues (e.g. protein, lipids and DNA) from attack by reactive species (RS). RS, the majority of which are by-products of metabolism, are usually neutralised by antioxidants, however OS occurs when there is an imbalance between the two. There are two main theories linking OS with growth and reproduction. The first is that traits like growth and reproduction, being metabolically demanding, lead to an increase in RS production. The second involves the diversion of resources away from self-maintenance processes (e.g. the redox system) when individuals are faced with enhanced growth or reproductive expenditure. Previous research investigating trade-offs involving growth or reproduction and self-maintenance has been equivocal. One reason for this could be that associations among redox biomarkers can vary greatly so that the biomarker selected for analysis can influence the conclusion reached about an individual’s oxidative status. Therefore the first aim of my thesis was to explore the strength and pattern of integration of five biomarkers of OS (three antioxidants, one damage and one general oxidation measure) in wild blue tit (Cyanistes caeruleus) adults and nestlings (Chapter 2). In doing so, I established that all five biomarkers should be included in future analyses, thus using this collection of biomarkers I explored my next aims; whether enhanced growth (Chapters 3 and 4) or reproductive effort (Chapter 5) can lead to increased OS levels, if these traits are traded off against self-maintenance. I accomplished these aims using both a meta-analytic and experimental approach, the latter involving manipulation of brood size in wild blue tits in order to experimentally alter growth rate of nestlings and provisioning rate (a proxy for reproductive expenditure) of adults. I also investigated the potential for redox integration to be used as an index of body condition (Chapter 2), allowing predictions about future fitness consequences of changes to oxidative state to be made. A growth – self-maintenance trade off was supported by my meta-analytic results (Chapter 4) which found OS to be a constraint on growth. However, when faced with experimentally enhanced growth, animals were typically not able to adjust this trade-off so that oxidative damage resulted. This might support the idea that energetically expensive growth causes resources to be diverted away from the redox system; however, antioxidants did not show an overall reduction in response to growth in the meta-analysis suggesting that oxidative costs of growth may result from increased RS production due to the greater metabolism needed for enhanced growth. My experimental data (Chapter 3) showed a similar pattern, with raised protein damage levels (protein carbonyls; PCs) in the fastest growing blue tit chicks in a brood, compared with their slower growing sibs. These within-brood differences in OS levels likely resulted from within-brood hierarchies and might have masked any between-brood differences, which were not observed here. Despite evidence for a growth – self-maintenance trade off, my experimental results on blue tits found no support for the hypothesis that self-maintenance is also traded off against reproduction, another energetically demanding trait. There was no link between experimentally altered reproductive expenditure and OS, nor was there a direct correlation between reproductive effort and OS (Chapter 5). However, there are various factors that likely influence whether oxidative costs are observed, including environmental conditions and whether such costs are transient. This emphasises the need for longitudinal studies following the same individuals over multiple years and across a wide range of habitats that differ in quality. This would allow investigation into how key life events interact; it might be that raised OS levels from rapid early growth have the potential to constrain reproduction or that high parental OS levels constrain offspring growth. Any oxidative costs resulting from these life-history trade-offs have the potential to impact on future fitness. Redox integration of certain biomarkers might prove to be a useful tool in making predictions about fitness, as I found in Chapter 2, as well as establishing how the redox system responds, as a whole, to changes to growth and reproduction. Finally, if the tissues measured can tolerate a given level of OS, then the level of oxidative damage might be irrelevant and not impact on future fitness at all.

The effects of attractiveness and underlying components on the motivational salience and the memorability of face photographs

Facial attractiveness is a particularly salient social cue that influences many important social outcomes. Using a standard key-press task to measure motivational salience of faces and an old/new memory task to measure memory for face photographs, this thesis investigated both within-woman and between-women variations in response to facial attractiveness. The results indicated that within-woman variables, such as fluctuations in hormone levels, influenced the motivational salience of facial attractiveness. However, the between-women variable, romantic relationship status, did not appear to modulate women’s responses to facial attractiveness. In addition to attractiveness, dominance also contributed to both the motivational salience and memorability of faces. This latter result demonstrates that, although attractiveness is an important factor for the motivational salience of faces, other factors might also cause faces to hold motivational salience. In Chapter 2, I investigated the possible effects of women’s salivary hormone levels (estradiol, progesterone, testosterone, and estradiol-to-progesterone ratio) on the motivational salience of facial attractiveness. Physically attractive faces generally hold greater motivational salience, replicating results from previous studies. Importantly, however, the effect of attractiveness on the motivational salience of faces was greater in test sessions where women had high testosterone levels. Additionally, the motivational salience of attractive female faces was greater in test sessions where women had high estradiol-to-progesterone ratios. While results from Chapter 2 suggested that the motivational salience of faces was generally positively correlated with their physical attractiveness, Chapter 3 explored whether physical characteristics other than attractiveness contributed to the motivational salience of faces. To address this issue, I first had the faces rated on multiple traits. Principal component analysis of third-party ratings of faces for these traits revealed two orthogonal components that were highly correlated with trustworthiness and dominance ratings respectively. Both components were positively and independently related to the motivational salience of faces. While Chapter 2 and 3 did not examine the between-woman differences in response to facial attractiveness, Chapter 4 examined whether women’s responses to facial attractiveness differed as a function of their romantic partnership status. As several researchers have proposed that partnership status influences women’s perception of attractiveness, in Chapter 4 I compared the effects of men’s attractiveness on partnered and unpartnered women’s performance on two response measures: memory for face photographs and the motivational salience of faces. Consistent with previous research, women’s memory was poorer for face photographs of more attractive men and more attractive men’s faces held greater motivational salience. However, in neither study were the effects of attractiveness modulated by women’s partnership status or partnered women’s reported commitment to or happiness with their romantic relationship. A key result from Chapter 4 was that more attractive faces were harder to remember. Building on this result, Chapter 5 investigated the different characteristics that contributed to the memorability of face photographs. While some work emphasizes relationships with typicality, familiarity, and memorability ratings, more recent work suggests that ratings of social traits, such as attractiveness, intelligence, and responsibility, predict the memorability of face photographs independently of typicality, familiarity, and memorability ratings. However, what components underlie these traits remains unknown, as well as whether these components relate to the actual memorability of face photographs. Principal component analysis of all these face ratings produced three orthogonal components that were highly correlated with trustworthiness, dominance, and memorability ratings, respectively. Importantly, each of these components also predicted the actual memorability of face photographs.