Acquisition of beneficial gut microbes and functional trade-offs in wild avian hosts

Animals encounter a vast array of environmental microbes that colonise their bodies and fulfil a broad spectrum of symbiotic roles. Some bacterial strains, especially within the gut microbiome, provide crucial functions for hosts. Through actions of their unique genes, gut microbes profoundly shape host digestion, immunity and behaviour. Knowledge of the importance of gut microbes has been derived primarily from biomedical research, meaning that our understanding of how microbe-host processes operate to benefit wildlife is virtually non-existent. Major outstanding questions in ecology remain unanswered. A key unknown is whether the wide variation of observed taxonomic composition of wild gut microbiomes among individuals matter for hosts in nature. We will answer these questions by causally identifying which microbes are important for host fitness and determining why gut microbiomes are so variable in wildlife. We will identify beneficial bacteria by characterising their genetic function, by understanding how they support host phenotypes, and by determining the environmental conditions required for their acquisition. This programme draws on eight years of the PI’s extensive research on gut microbiome, behaviour and ecology of great tit (Parus major) and blue tit (Cyanistes caeruleus) birds in the wild. Our pioneering work has identified at least three potentially beneficial gut microbes that predict nestling survival, and we cultured a fourth host-origin microbial strain, Lactobacillus kimchicus, that can be administered naturally in the wild, affecting nestling weight. Our breakthrough findings, extensive bank of gut microbiome samples, bioinformatics pipelines, and powerful methods for quantifying suites of host phenotypes in response to gut microbiome manipulations open exciting new pathways for understanding the ecology of beneficial microbes in wildlife. This will be achieved through the following objectives: Objective 1: Identify candidate beneficial microbes by characterising their genetic functions. L. kimchicus is dominated by protein and carbohydrate metabolism genes that may increase nutrient availability to the host, thus increasing weight. Given the broad taxonomic composition of the wild avian gut microbiome, other microbes are expected to contribute similar, or additional genetic functions for hosts. Pulling from our existing bank of gut microbiome samples, we will perform whole-genome shotgun sequencing to identify potentially beneficial microbes that have host-relevant metabolic pathway genes. Objective 2: Experimentally test for microbiome-mediated host phenotypic trade-offs. Our finding that nestling weight is affected by L. kimchicus is just one of several host phenotypes in the natal environment that could be microbially influenced. Moreover, phenotypic trade-off theory predicts that enhancing one trait can come at the expense of another, meaning perceived benefits are best understood in the context of host life history strategies. We will measure multiple host phenotypes (growth, immunity, behaviour, and cognition) following microbial enrichment manipulations to test if/which gut microbiota causally alter host phenotypes, and whether these gut microbes alleviate, or contribute to, phenotypic trade-offs. Objective 3: Identify origins of beneficial gut microbes. In wildlife, there is huge variation in the composition of gut microbiota among individuals and populations where the natal environment is a critical early-life window for gut microbiome acquisition. By simultaneously sampling environmental, dietary and parental sources of microbes, sophisticated microbiome tracking analyses will be deployed to make major advances in identifying source pools of potentially beneficial gut microbes. This interdisciplinary research programme will offer unprecedented basic and applied insights into natural gut microbiome variation, gut microbe functions and microbial source pools for wildlife.