Diet induces parallel changes to the gut microbiota and problem solving performance in a wild bird

Abstract

The microbial community in the gut is influenced by environmental factors, especially diet, which can moderate host behaviour through the microbiome-gut-brain axis. However, the ecological relevance of microbiome-mediated behavioural plasticity in wild animals is unknown. We presented wild-caught great tits (Parus major) with a problem-solving task and showed that performance was weakly associated with variation in the gut microbiome. We then manipulated the gut microbiome by feeding birds one of two diets that differed in their relative levels of fat, protein and fibre content: an insect diet (low content), or a seed diet (high content). Microbial communities were less diverse among individuals given the insect compared to those on the seed diet. Individuals were less likely to problem-solve after being given the insect diet, and the same microbiota metrics that were altered as a consequence of diet were also those that correlated with variation in problem solving performance. Although the effect on problem-solving behaviour could have been caused by motivational or nutritional differences between our treatments, our results nevertheless raise the possibility that dietary induced changes in the gut microbiota could be an important mechanism underlying individual behavioural plasticity in wild populations.

Flexibility and resilience of great tit (Parus major) gut microbiomes to changing diets

“…Exploration of host-gut microbiome dynamics of wild hosts is important to better understand the flexibility, resilience and long-term associations of symbiotic interactions under dietary changes. By examining the flexibility and resilience of wild omnivorous passerine bird gut microbiomes through diet manipulation, our findings document a rapid and significant impact of diet, aligning with other studies on passerine birds [ 51 , 52 ]. We observed a significant deviation in microbial community structure from the initial gut microbiomes after diet manipulation, but we found no significant differences in gut communities between the three diet groups (Fig.…”

“…This is potentially associated with more homogeneous nutrient availability in the mealworm diet [ 58 ] compared to the more heterogeneity from multiple types of seeds (e.g., sunflower seeds [ 59 ], millet [ 60 ], and wheat [ 61 ]). Additionally, the taxonomic diversity of initial gut microbiomes of P. major differed markedly from the other diet manipulation study [ 52 ], where Proteobacteria dominated the gut microbiomes, indicating regional or population differences. However, the observed similarity in the overall community-level response of gut microbiomes for individuals on seed or insect diets in the two studies suggest that despite these differences, microbial communities respond in similar ways to similar diet changes.…”

“…Microbiomes of birds fed with mealworms experienced significantly lower individual variation than birds fed with a standard or a seed diet (Additional file 8 : Figure S4). The reduced individual variation in insectivores has been demonstrated in wild birds [ 14 ] and in another diet manipulation study of P. major [ 52 ], suggesting that a strictly insectivorous diet (mealworms) might be associated with a specific and narrower set of gut microbes [ 58 ] compared to the seed diet. This is potentially associated with more homogeneous nutrient availability in the mealworm diet [ 58 ] compared to the more heterogeneity from multiple types of seeds (e.g., sunflower seeds [ 59 ], millet [ 60 ], and wheat [ 61 ]).…”

“…Intra-specific differences in bird populations from habitats with potentially different food availabilities further support the plastic nature of bird gut microbiomes [ 28 , 31 , 45 – 50 ], as does the higher individual variation and gut bacterial diversity of omnivorous birds compared to bird species with more specialized diets (e.g., insectivores) [ 14 ]. The gap in pinpointing the impact of diet on gut microbiomes has to some extent been filled by recent diet manipulation studies of Passer domesticus (house sparrows) [ 51 ] and Parus major (great tits) [ 52 ], in which gut microbiomes respond according to dietary contents. If dietary changes are regular (e.g., seasonality and migration) we would expect gut microbiomes to cyclically change over time depending on temporal changes in food availability [ 24 , 53 ].…”

A time‐lagged association between the gut microbiome, nestling weight and nestling survival in wild great tits

“…Full library preparation details are described in Supporting Information and in Davidson, Wiley, et al., 2020). Briefly, the V3‐V4 variable region of the 16S rRNA gene was amplified from the DNA extracts using the 16S metagenomic sequencing library protocol (Illumina).…”