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Abstract: To what extent host‐associated microbiota assembly is driven by host selection or simply by happenstance remains an open question in microbiome research. Here, we take a first step towards elucidating the relative importance of host selection on the establishing gut microbial community in an ecologically relevant organism. We presented germ‐free bumblebee, Bombus terrestris, workers from 10 colonies with a “global” microbial species pool comprised of an equal mixture of the gut microbiota of all colonies. By means of 16S amplicon sequencing, we found that overall microbiota community composition was generally shifted between pool‐exposed workers compared to workers that naturally acquired their gut microbiota, but that the specific composition of the established microbiota also depended on colony identity (e.g. genetic background). Because the microbiota is protective against parasite infection in this system, variation in the filtering of a beneficial microbial community can have important consequences for host resistance and eventual co‐evolution with parasites. [ABSTRACT FROM AUTHOR]