Social environment drives sex and age‐specific variation in Drosophila melanogaster microbiome composition and predicted function

• Published in: Molecular ecology 2021-11, Vol.30 (22), p.5831-5843
• Main Authors: Leech, Thomas, McDowall, Laurin, Hopkins, Kevin P., Sait, Steven M., Harrison, Xavier A., Bretman, Amanda
• Format: Article
• Language: English
• Subjects: Age Factors; ageing; Aging; Animals; Brain; Brain-Gut Axis; Community structure; Composition; development; Drosophila melanogaster; Drosophila melanogaster - genetics; Environmental factors; Female; Fruit flies; Homogeneity; Housing; Immune response; infection; Insects; Life span; Male; Males; Microbiomes; Microbiota; Microbiota - genetics; microbiota‐gut‐brain axis; Microorganisms; Sex; Sexes; Social Environment; Social interactions; stress
• ISSN: 0962-1083; 1365-294X
• DOI: 10.1111/mec.16149

Social environments influence multiple traits of individuals including immunity, stress and ageing, often in sex‐specific ways. The composition of the microbiome (the assemblage of symbiotic microorganisms within a host) is determined by environmental factors and the host's immune, endocrine and neural systems. The social environment could alter host microbiomes extrinsically by affecting transmission between individuals, probably promoting homogeneity in the microbiome of social partners. Alternatively, intrinsic effects arising from interactions between the microbiome and host physiology (the microbiota‐gut‐brain axis) could translate social stress into dysbiotic microbiomes, with consequences for host health. We investigated how manipulating social environments during larval and adult life‐stages altered the microbiome composition of Drosophila melanogaster fruit flies. We used social contexts that particularly alter the development and lifespan of males, predicting that any intrinsic social effects on the microbiome would therefore be sex‐specific. The presence of adult males during the larval stage significantly altered the microbiome of pupae of both sexes. In adults, same‐sex grouping increased bacterial diversity in both sexes. Importantly, the microbiome community structure of males was more sensitive to social contact at older ages, an effect partially mitigated by housing focal males with young rather than coaged groups. Functional analyses suggest that these microbiome changes impact ageing and immune responses. This is consistent with the hypothesis that the substantial effects of the social environment on individual health are mediated through intrinsic effects on the microbiome, and provides a model for understanding the mechanistic basis of the microbiota‐gut‐brain axis.