Sarah F Worsley, Chuen Zhang Lee , Terry Burke, Jan Komdeur, Hannah L Dugdale , David S Richardson

Environmental variation is a key factor shaping microbiome communities in wild animals. However, most studies have focussed on separate populations distributed over large spatial scales. How ecological factors shape inter-individual microbiome variation within a single landscape and host population remains poorly understood. Here, we use dense sampling of individuals in a natural, closed population of Seychelles warblers on Cousin Island (<0.7 km diameter, 0.34 km2 total area) to determine whether gut microbiome communities exhibit high-resolution spatial variation over fine scales (average territory area is 0.0023 km2). We identified a strong quadratic relationship between geographic distance and gut microbiome beta diversity across the island. Microbiome composition initially diverged with increasing geographic distance between territories. However, after > ca 300 m microbiome composition became increasingly similar among individuals situated on different sides of the island. This relationship was robust to the effects of host relatedness, age, and sex. Further analysis showed that microbiome composition differed between individuals inhabiting coastal and inland territories. Warblers in coastal territories harboured greater abundances of marine bacteria and lower abundances of anaerobic taxa commonly linked to host metabolic health, suggesting that exposure to different environmental microbes and variation in host condition (which is lower in coastal territories) could drive spatial patterns of gut microbiome variation across the island. This work demonstrates that host-microbe interactions can be extremely plastic even at very fine spatial scales. Such plasticity may have implications for how species respond to anthropogenic disturbance in wild habitats.