Telomeres as biomarkers of cost and quality in a wild vertebrate population

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Because resources, and the time it take to acquire them, are limited, every organism has a finite amount it can use in its efforts to survive and reproduce. Resources spent on one area, such as health, cannot be spent on another, such as in reproduction. Consequently organisms must trade off how best to spend their resources so as to maximise the benefits they gain. Such trade-offs are central to our understanding of the evolution of different life-history strategies, i.e. why organisms differ in aspects such as their size, reproductive rate and lifespan / a fundamental question in biology. The problem is that, although it is often relatively easy to assess the benefit to an organism of investing in one area, to understand trade-offs we also need to know the associated cost. Unfortunately, measuring such costs has proved to be extremely difficult, especially in animals in the wild. Furthermore, working out which mechanisms link the costs of alternative investments, and mediate trade-offs between areas of investment, or across the lifetime of an organism, has proved beyond us. Telomeres are long, specialized regions of DNA that protect the ends of chromosomes and prevent the cells' genes from getting damaged or mixed up each time the cell replicates. However, a section of telomere is lost during each replication and when telomeres reach a critical, short length the cell stops functioning. The accumulation of these dysfunctional cells in the bodies' tissues is thought to lead to ageing and senescence. Importantly the rate at which telomeres shorten is also greatly affected by oxidative stress / the organism's inability to cope with the damaging waste products (free radicals) of metabolism. Oxidative stress (and/or telomere shortening) has been shown to be influenced by life history and environmental stresses (e.g. accelerated growth or infection). Telomere shortening can, therefore, indicate the biological cost that such stresses exact on an individual and provide an important link between these costs and ageing and senescence. We plan to use the unique dataset compiled on the Seychelles warblers to take the opportunity to undertake a longitudinal study of telomeres within individuals in a wild vertebrate population. We are only able to do this because the intensive long-term study of island populations of this species means that highly detailed information is available on the environmental factors experienced and reproductive investments made. Importantly, annual blood samples have been collected from many individuals of known age throughout their lives. First, we will focus on whether telomere shortening can be used as a measure of biological ageing in a wild population. Key to this is confirming that age-related lengths of an individual's telomeres predicts lifespan (and/or senescence) in the Seychelles warbler. We will then investigate the relative costs of different stresses by relating the annual telomere-shortening rate to the stresses they have faced in that year. Experimental manipulations will allow us to hone in on specific factors, such as reproductive effort. Importantly, costs will be measured with generic units of currency (telomere shortening rates) that would allow comparisons, not only between stresses, but also with respect to the age and life-history stage at which they are experienced. This will allow us to compare how the costs and benefits of investment in different life-history components, or in dealing with environmental stresses, are traded off. Finally, we will test the idea that individual variation in telomere shortening rate can reflect an individual's ability to withstand these stresses and, therefore, provide an indicator of individual quality.