Does ecological drift explain variation in microbiome composition among groups in a social host species?

Within a given species, considerable inter-individual, spatial, and temporal variation in the composition of the host microbiome exists. In group-living animals, social interactions homogenize microbiome composition among group members, nevertheless divergence in microbiome composition among related groups arise. Such variation can result from deterministic and stochastic processes. Stochastic changes, or ecological drift, can occur among symbionts with potential for colonizing a host and within individual hosts, and drive divergence in microbiome composition among hosts or host groups. We tested whether ecological drift associated with dispersal and foundation of new groups cause divergence in microbiome composition between natal and newly formed groups in the social spider Stegodyphus dumicola. We simulated the initiation of new groups by splitting field-collected nests into groups of 1, 3, and 10 individuals respectively, and compared variation in microbiome composition among and within groups after 6 weeks using 16S rRNA gene sequencing. Theory predicts that ecological drift increases with decreasing group size. We found that microbiome composition among single founders was more dissimilar than among individuals kept in groups, supporting this prediction. Divergence in microbiome composition from the natal nest was mainly driven by a higher number of non-core symbionts. This suggests that stochastic divergence in host microbiomes can arise during the process of group formation by individual founders, which could explain the existence of among-group variation in microbiome composition in the wild. Individual founders appear to harbour higher relative abundances of non-core symbionts compared with founders in small groups, some of which are possible pathogens. These symbionts vary in occurrence with group size, indicating that group dynamics influence various core and non-core symbionts differently.

Automated summary

Considerable variation in the composition of the host microbiome exists within a given species. Social interactions in group-living animals homogenize microbiome composition among group members, but still give rise to divergence in microbiome composition among related groups. This variation can result from deterministic and stochastic processes. We tested whether ecological drift associated with dispersal and foundation of new groups cause divergence in microbiome composition between natal and newly formed groups in the social spider Stegodyphus dumicola. The results suggest that stochastic divergence in host microbiomes can arise during the process of group formation by individual founders.