Understanding host-microbe interactions in a changing world: drivers and fitness consequences of the gut microbiome in a declining Antarctic pinniped

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Vertebrates are inhabited by vast numbers of microorganisms that are increasingly emerging as key players in their host’s biology and evolution. These microbial communities carry orders of magnitude more genes than their hosts and support functions that are not encoded in the host’s genome. Consequently, the ‘microbiome’, which includes both the microbes themselves and the molecules they produce, is of fundamental importance to host function. The richest and arguably most important microbial communities are those of the gastrointestinal tract. Reduced gut microbial diversity has been linked to many diseases in humans including autoimmune disorders, diabetes and obesity. However, little is known about the relationship between gut microbes and health in wild vertebrate populations, where higher levels of genetic variation and pronounced environmental heterogeneity may modulate or even override any effects of the gut microbiome on the host. This major gap in our knowledge of host-microbiome interactions hinders our understanding of resilience and climate change adaptation. This project will exploit an outstanding natural system, Antarctic fur seals, to investigate the fitness consequences of the gut microbiome in a wild population that is declining in response to anthropogenic reductions in food availability. Focusing on the critical developmental time window between birth and nutritional independence, it will elucidate the effects of key intrinsic and extrinsic drivers on the gut microbiome and its interplay with multiple fitness relevant phenotypes including growth, survival, stress hormone levels, immune function and gene expression. Specifically, our project will exploit a unique ‘natural experiment’ and a fully crossed repeated measures design to evaluate the effects of two interacting environmental stressors, food limitation and social density. Furthermore, a recently developed single nucleotide polymorphism array will allow robust evaluation of the modulating effects of host genotype, including heritable genetic variation and genetic quality, expressed as inbreeding and immunogenetic diversity. We hypothesise that reduced food availability will lower gut microbial diversity and increase the prevalence of mucolytic and proinflammatory taxa, negatively impacting host fitness. These effects may be especially pronounced among individuals of poor genetic quality, who may be less effective at controlling harmful microbes, as well under stressful, high density conditions. In summary, this project will combine rich individual-based life-history and phenotypic data with multi-omics approaches to produce unprecedentedly detailed and multi-layered mechanistic insights into host-microbe interactions in a declining top predator. This is essential for understanding whether gut microbes could exacerbate (or buffer) climate change impacts, and has direct implications for predicting long-term population trends and managing the Southern Ocean ecosystem.