Gut microbiome variation, fitness and senescence within a natural vertebrate population

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That extensive individual variation in reproductive success, survival and senescence (ageing) exists in many animal population is clear, however what causes this variation remains largely unexplained. Understanding the drivers of this variation is of great importance, both because differential fitness is the basis of adaptive evolution, but also because such understanding may help improve the health and wellbeing of individuals.Studies on humans and captive animals have shown that variation in the composition of the gut microbiome (GM) - a complex microbial community comprising thousands of species - can play an important role in host function, influencing components such as digestion, immunity and development, and affecting the outcome of deleterious conditions and disease. Research has also suggested that changes in the GM can play a causal role in an individual's deterioration with age. Therefore, given that the GM appears to be integral to the health of its host, we can hypothesise that variation in the GM will have important consequences for an individual's survival and reproductive success. GM variation may also contribute to the extensive, and largely unexplained, differences in senescence observed among individuals within populations, including in humans. It is then surprising that so little work has been undertaken to determine how much GM variation exists among individuals within natural populations, or which factors drive this variation. More importantly, to our knowledge no studies have yet determined if individual GM variation is associated with reproductive success and senescence within a wild vertebrate population. Given that unnatural conditions can radically change an individual's GM, and complex interactions between the individual and its environment influence survival and reproductive success, studies under natural conditions are essential if we are to fully understand the causes and fitness consequences of GM variation.We aim to fill these gaps in our knowledge by undertaking a comprehensive investigation of the causes of individual variation in the bacterial GM, and, for the first time, how this is linked to fitness and senescence within a natural vertebrate population. We are perfectly placed to do this because our long-term study of a discrete population of the Seychelles warbler Acrocephalus sechellensis, allows us to follow and sample individuals throughout their lives. We have detailed environmental, genetic, biological condition and accurate survival and reproductive success data (unconfounded by dispersal) on individuals across their lives. We also have a 10-generation genetic pedigree of the population which, combined with contrasting patterns of social parentage (e.g. due to infidelity), provides the basis for a powerful analysis of the heritability of GM characteristics. Importantly, our NERC-funded pilot study successfully tested protocols for the sequencing and analysis of GM variation from faecal samples, and our results confirm that considerable individual variation in the GM exists within this population. We now have everything in place to facilitate the success of this novel and timely study.Assessing the natural co-variation that exists in a wild population is an essential step in exposing the evolutionary importance of the GM. This proposal will allow us to determine if the components required for natural selection - individual variation, differential fitness linked to that variation, and inheritance of that variation - exist in terms of the GM within a natural population. Such evidence would, for the first time, provide strong support for the idea that natural selection on vertebrate hosts is mediated by the GM. Knowledge of the causes and consequences of GM variation is also important from an applied perspective as it will inform how we can manage GM diversity to optimise our own health, and the traits and condition of the animals that we utilise or wish to conserve.