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Reactive Oxygen Species and the Evolution of Life Histories

Final Report Summary - ROSELH (Reactive Oxygen Species and the Evolution of Life Histories)

TARGETING THE PHYSIOLOGICAL UNDERPINNINGS OF LIFE-HISTORY TRADE-OFFS
The presence of life history trade-offs is well established; fitness-related traits, such as reproductive output and survival, are often negatively associated with each other, constraining their independent evolution. However, the physiological mechanisms underlying these trade-offs remain elusive. A key mechanism may be oxidative stress induced by metabolic processes. Oxidative stress arises in tissues when there is an excess of what are called ‘free radicals’ and it results in cellular oxidative damage. This research project used an evolutionary approach to examine the role of oxidative stress as a mediator of reproductive costs, the costs associated with immune system activation and how these costs contribute to ageing.

A) OUTGOING PHASE
The out-going phase of this project integrated field studies and laboratory experiments using the Australian Painted dragon lizard (Ctenophorus pictus) as a study species. The Painted dragon is a formidable species to study the effects of free radicals on age-related aspects of reproduction and immunity due to it short lifespan (only ca. 15% survive to a second year), its pronounced sexual coloration that diminishes with age (males only) and its relatively high reproductive output (females lay 3-6 eggs in 3-4 clutches during their short life time).

*Color as a “health certificate”
Our results also show that the age-related loss of sexual head coloration is positively correlated with the levels of DNA damage experienced by individual male lizards (Olsson, Tobler et al. 2012, Evolution, 66, 2475-2483). This suggests that male color may act as a “health certificate” and visualize underlying antioxidation and detoxification quality to potential partners and overall viability to challenging rivals. Experiments with testosterone implants further demonstrate that male sexual coloration is also regulated by this hormone. High testosterone levels mitigate the age-related color loss in males. This is intriguing since testosterone (and other steroids) have also been suggested to be important modifiers of the oxidative stress balance. Our results indicate that testosterone can impact on free radical (and antioxidant) levels through the immune system. Phagocytic production of free radicals, which is essential for inhibition of bacterial growth and therefore important part of the innate immune system, was significantly lowered in lizards with elevated testosterone levels. Lowered phagocytic production of free radicals may have profound negative consequences for disease resistance. Only males of superior quality may be able to maintain high testosterone levels and strong coloration while at the same time coping with attrition of oxidative insults and increased disease susceptibility.
Furthermore, our results suggest that expression of another non-specific ornament, the yellow throat color (bib), also affects lizard oxidative stress physiology. Bibbed males appear to be more costly phenotypes in terms of free radical-physiology compared to non-bibbed males, but this effect is reversed in females (Olsson et al. 2012, Journal of Experimental Biology, 215, 575-577). This may have important consequences for sexual selection.

*Sex differences in immune-oxidative stress
Although it is well known that immune system activation increases the production of free radicals which may pose a potential threat to self, little is known about the regulation of immune system-generated free radical production in non-traditional model species and how it may vary between the sexes. Experiments on the painted dragon suggest that different factors (antioxidant status, current free radical load) regulate the production of immune system-generated radicals and that there may be considerable differences between the sexes.

*The cost of reproduction
Reproduction increases metabolic activity/demand and, hence, may lead to increased production of free radicals. For painted dragons, we have shown that females closer to ovulation, hence with less remaining, circulating vitellogenin, have higher superoxide (a primary free radical) levels and females that produced more clutches over time suffered more DNA damage. Moreover, females with higher levels of circulating superoxide dismutase levels (i.e. higher antioxidant protection) suffered less DNA damage (Olsson et al. 2012, Oecologia 170, 917-924).


B) RETURN PHASE

During the return phase, the zebra finch (Taeniopygia guttata) was used as a study species. This small passerine bird (ca 12 g) is nowadays considered the most important captive model passerine. Zebra finches start breeding already at an age of ca 70 days, which is extraordinary compared to all other passerine model species that do not breed until ca 1 year old. In addition, they can easily be kept and bred under laboratory conditions which makes them exceptionally suited for longitudinal studies on various aspects of reproduction, physiology and behaviour.

Effects that impact early during the development can have long-lasting consequences for physiological and behavioral plasticity in adulthood. The work conducted in this phase of the project has targeted the influence of hormonal fetal programming and oxidative stress during early development on the physiological status (oxidative damage, immune function) in adulthood. Analyses on this project are in progress. They will show how the long-term oxidative stress phenotype is formed.

GENERAL IMPACT
Oxidative stress has long been in the focus of science and the public due to its associations with cancer, infertility and ageing. However, whether and how oxidative stress influences organism health is still an issue of much debate. This project provides new insights about the role of oxidative stress in biology and has the potential to open up new avenues for interdisciplinary research.