The gut microbiota affects the social network of honeybees

• Published in: Nature ecology & evolution Vol. 6; no. 10; pp. 1471 - 1479
• Main Authors: Liberti, Joanito, Kay, Tomas, Quinn, Andrew, Kesner, Lucie, Frank, Erik T., Cabirol, Amélie, Richardson, Thomas O., Engel, Philipp, Keller, Laurent
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.10.2022; Nature Publishing Group
• Subjects: 631/158/856; 631/181/2469; 631/326/2565; 631/378/3919; Amino Acids; Animals; Apis mellifera; Bees; Biological and Physical Anthropology; Biomedical and Life Sciences; Biosynthesis; Brain; Chromatin; Colonies; Colonization; Ecology; Epigenetics; Evolutionary Biology; Gastrointestinal Microbiome; Intestinal microflora; Life Sciences; Metabolites; Microbiomes; Microbiota; Paleontology; Sensory perception; Social behavior; Social factors; Social interaction; Social interactions; Social Networking; Social networks; Social organization; Synaptic transmission; Zoology
• ISSN: 2397-334X; 2397-334X
• DOI: 10.1038/s41559-022-01840-w

The gut microbiota influences animal neurodevelopment and behaviour but has not previously been documented to affect group-level properties of social organisms. Here, we use honeybees to probe the effect of the gut microbiota on host social behaviour. We found that the microbiota increased the rate and specialization of head-to-head interactions between bees. Microbiota colonization was associated with higher abundances of one-third of the metabolites detected in the brain, including amino acids with roles in synaptic transmission and brain energetic function. Some of these metabolites were significant predictors of the number of social interactions. Microbiota colonization also affected brain transcriptional processes related to amino acid metabolism and epigenetic modifications in a brain region involved in sensory perception. These results demonstrate that the gut microbiota modulates the emergent colony social network of honeybees and suggest changes in chromatin accessibility and amino acid biosynthesis as underlying processes. Tracking the behaviour of normal versus microbiome-free honeybees in experimental colonies, the authors show that gut microbiota colonization was associated with an increase in the rate and specificity of social interactions among bees and higher abundances of brain metabolites linked to these interactions.