The Role Transition of Dietary Species Richness in Modulating the Gut Microbial Assembly and Postweaning Performance of a Generalist Herbivore

When facing a food shortage, generalist herbivores can respond by expanding their dietary species richness (DSR) to maximize energy collection, regardless of whether forages are preferred or not. Higher DSR usually indicates higher nutrient adequacy and better health. However, the high-DSR diet containing a large proportion of preferred species or a large proportion of less-preferred species means different things to an animal. It is still unknown how different shift patterns in DSR would affect distinctly the performance of animals via altering gut microbiota. We examined the gut microbial composition, diversity, community assembly processes, and performance of a generalist herbivore, Lasiopodomys brandtii, in a feeding experiment with increased levels of simulated DSR shifting from preferred plant species to less preferred ones. We found the survival rate and body growth of Brandt’s voles showed a dome-shaped association with DSR: species performance increased initially with the increase of preferred plant species but declined with the increase of less-preferred food items. Several microbial taxa and functions closely related to the metabolism of amino acids and short-chain fatty acids also showed a dome-shaped association with DSR, which is consistent with the observation of performance change. However, the alpha diversities of gut microbiota increased linearly with DSR. The null model and phylogenetic analysis suggested that stochastic processes dominate at low DSR diets, whereas deterministic processes prevail at high DSR diets. These results suggest that the role of DSR in regulating animal performance by gut microbiota depends on the number of preferred forage items. IMPORTANCE The plant species diversity varies greatly under the influence of both climate change and human disturbance, which may negatively affect the productivity as well as the variability of organisms (e.g., small herbivores) at the next trophic level. It is still unknown how gut microbiota of small herbivores respond to such changes in dietary species richness. Our manipulative food experiment revealed that dietary species richness can affect the composition, functions, and community assembly of gut microbiota of Brandt’s vole in a nonlinear way. Given the fast-growing interest in therapeutic diets to treat dysbiosis and to improve health conditions, our study highlights the need to consider not just the variety of consumed food but also the principles of rational nutrition.