Arctic greening drives changes in the diet and gut microbiome of a resident herbivore with consequences for fitness

Rapid climate warming is "greening" the tundra due to higher plant productivity, particularly of deciduous shrubs and grasses, potentially changing the nutritional base for herbivores. However, the consequences for herbivores are unclear. Although the gut microbiome is an essential factor, mediating the capacity to adapt to dietary change, few studies have investigated the effect of annual changes in the diet-gut microbiome nexus on fitness traits. In a model system, the Svalbard reindeer, a species experiencing the greatest rate of climate warming on Earth, we investigate how climate-induced changes in diet and the gut microbiome impact reindeer body mass. Using high-resolution DNA metabarcoding, we quantified diet and microbiome composition in rumen samples from 97 animals culled in October from 1998 to 2004 in four different valleys. Overall diet diversity and grass consumption were significantly higher following warmer summers, while intake of the dwarf shrub Salix polaris increased with the maximum normalised difference vegetation index (NDVI). The proportion of Salix had a significant positive effect on autumn body mass, which in turn increases ovulation rates and overwinter survival. There was a significant positive effect of Salix on the microbiome diversity, while between-year variation in Bacteroidota, the most common bacteria phylum, was also significantly, positively related to maximum NDVI. However, a structural equation model revealed that the direct "path" effect of the proportion of Salix in the diet on reindeer body mass was stronger than the indirect path effect, mediated through the gut microbiome. Our results suggest a positive impact of climate-driven Arctic greening on Svalbard reindeer fitness, operating through a change in diet composition, partially mediated by the changes in the gut microbiome. These findings advance our understanding of the mechanistic underpinnings of Arctic warming on herbivore populations and contribute to the debate about the importance of the diet-gut microbiome nexus in facilitating species resilience in the face of climate change.