Host determinants of among-species variation in microbiome composition in drosophilid flies

Abstract

The taxonomic composition of microbial communities in animals varies among animal species, but the contribution of interspecific differences in filtering of the microbial pool by the animal host to this variation is uncertain. Here, we demonstrate significant interspecific variation in microbial community composition among laboratory-reared Drosophila species that was not related to host phylogeny. Complementary reciprocal transfer experiments yielded different microbial communities for a single microbiota administered to homologous and heterologous hosts (i.e., the same and different Drosophila species from which the microbiota was derived), indicative of among-host species differences in traits that shape microbiota composition. The difference in microbiota composition between homologous and heterologous hosts was not greater for distantly related than for closely related host species pairs. Furthermore, Drosophila survival to adulthood was significantly reduced in heterologous associations relative to homologous associations and microbiologically sterile flies, suggesting that microbial taxa that are advantageous for their homologous host species can be deleterious for other host species. We conclude that drosophilid flies display robust among-host species variation in host controls over microbiota composition that has diversified in response to selection pressures which are not tracked by host phylogeny.

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Acknowledgements

We thank Marita Wilson (Cornell University) and Dina Mostafa, Adrian Ng and Peter Denezis (University of Western Ontario) for technical assistance, and Brent J. Sinclair (University of Western Ontario) and Andrew Moeller (Cornell University) for helpful discussions. This study was funded by NSF grant Bio 1241099 to AED, and a Natural Sciences and Engineering Council of Canada Discovery Grant to BJS. SK and RK were supported by the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant Agreement No. 661122, and additionally SK was supported by the Emil Aaltonen Foundation and RK by the Finnish Cultural Foundation Grant for sabbatical research leave.

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KLA, AB, and AED designed the study; AB and VGM prepared the samples for set-1; SK, RK, and GPS prepared the samples for set-2; KLA, EB, AB, and GPS conducted the reciprocal transfer experiments; KLA, AB, and VGM processed the sequence data; KLA conducted the statistical analyses; KLA and AED wrote the manuscript; all authors contributed to manuscript revisions and agreed to the final version.

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Correspondence to Angela E. Douglas.

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Adair, K.L., Bost, A., Bueno, E. et al. Host determinants of among-species variation in microbiome composition in drosophilid flies. ISME J 14, 217–229 (2020). https://doi.org/10.1038/s41396-019-0532-7

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