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

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.

Our research will provide information and understanding on why individual animals differ in the gut microbiome (GM) they harbour and how that affects their biological condition, reproductive success, senescence and survival

BENEFICIARIES
1. Biologists
2. Medical and general health practitioners
3. Animal breeders
4. Veterinarians and pet owners
5. Conservation stakeholders
6. The public
8. The PDRA/RA

HOW WILL THEY BENEFIT?
1. Biologists (including microbiologists and evolutionary biologists) will gain information on what factors affect an individual's GM and how these differences or changes are linked to condition, reproductive success, survival and ageing. Evolutionary biologist will also gain knowledge on how the GM may play a major role in the unexplained variation we see in individual fitness within many natural populations. This will provide a better understanding of evolution and senescence.

2. Medical and general health practitioners. The key benefit is knowledge, applicable to humans, on how the GM may affect health parameters, what constitutes a healthy gut, and how that is influenced by different environmental factors (such as diet or contact with more individuals). They will also gain insight into what happens to the GM during ageing, and potentially how that can be prevented or mitigated. This may inform health stakeholders of how lifestyle changes can be involved in maintaining a healthy GM, thus saving resources and improving public health.

3 Animal Breeders: Knowledge of if, and how, to optimize the GM health of breeding programs through changing environmental factors, or direct manipulation of the GM to maximize the productivity and welfare of animals. Understanding of the fact that a healthy GM can improve responses and outcomes to disease/conditions.

4) Veterinarians and Pet Owners: as above in point 3, knowledge of how optimize the GM health of the animals they look after. Plus understanding of how this component may be an important factor in health issues.

5. Conservation stakeholders: Knowledge on whether managing the GM of captive animals may allow us to maximize their health and productivity. Understanding that captivity may cause deleterious changes in the GM and how it can be prevented or restored to a healthy natural composition. Also understanding that the GM may be optimized for a specific environment and thus the GM may play a role in determining the success of translocations or the release of captive bred animals.

6. General Public: Understanding what causes individuals to differ in the community of microbes that live in their gut, and importantly, what impact that has on their health and fitness, will strike a chord with the general public. They will also gain knowledge about whether changing lifestyle or environments factors may benefit their own health.

8. PDRA and RA will gain valuable transferable skills sets that will advance their career opportunities whether or not they choose to remain in academia.