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.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Douglas AE. Fundamentals of microbiome science: how microbes shape animal biology. Princeton, NJ, USA: Princeton University Press; 2018.
McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA. 2013;110:3229–36.
Krumbeck JA, Walter J, Hutkins RW. Synbiotics for improved human health: Recent developments, challenges, and opportunities. Annu Rev Food Sci Technol. 2018;9:451–79.
Lemon KP, Armitage GC, Relman DA, Fischbach MA. Microbiota-targeted therapies: an ecological perspective. Sci Transl Med. 2012;4:137rv5.
Arora AK, Douglas AE. Hype or opportunity? Using microbial symbionts in novel strategies for insect pest control. J Insect Physiol. 2017;103:10–17.
Gressel J. Microbiome facilitated pest resistance: potential problems and uses. Pest Manag Sci. 2018;74:511–5.
Berasategui A, Shukla S, Salem H, Kaltenpoth M. Potential applications of insect symbionts in biotechnology. Appl Microbiol Biotechnol. 2016;100:1567–77.
Costello EK, Stagaman K, Dethlefsen L, Bohannan BJM, Relman DA. The application of ecological theory toward an understanding of the human microbiome. Science. 2012;336:1255–62.
Adair KL, Douglas AE. Making a microbiome: the many determinants of host-associated microbial community composition. Curr Opin Microbiol. 2017;35:23–9.
Tung J, Barreiro LB, Burns MB, Grenier J-C, Lynch J, Grieneisen LE, et al. Social networks predict gut microbiome composition in wild baboons. eLife. 2015;4:e05224.
Moeller AH, Suzuki TA, Lin D, Lacey EA, Wasser SK, Nachman MW. Dispersal limitation promotes the diversification of the mammalian gut microbiota. Proc Natl Acad Sci USA. 2017;201700122.
Perofsky AC, Lewis RJ, Meyers LA. Terrestriality and bacterial transfer: a comparative study of gut microbiomes in sympatric Malagasy mammals. ISMEJ. 2019;13:50–63.
Moeller AH, Peeters M, Ndjango J-B, Li Y, Hahn BH, Ochman H. Sympatric chimpanzees and gorillas harbor convergent gut microbial communities. Genome Res. 2013;23:1715–20.
Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L, et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science. 2011;332:970–4.
Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Knight R, Caporaso JG, et al. Individuals’ diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch). Ecol Lett. 2014;17:979–87.
Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SK, Wingreen NS, Sonnenburg JL. Diet-induced extinctions in the gut microbiota compound over generations. Nature. 2016;529:212–5.
David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2013;505:559–63.
Smith CCR, Snowberg LK, Caporaso GJ, Knight R, Bolnick DI. Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota. ISME J. 2015;9:1–12.
Brooks AW, Kohl KD, Brucker RM, van Opstal EJ, Bordenstein SR. Phylosymbiosis: relationships and functional effects of microbial communities across host evolutionary history. PLoS Biol. 2016;14:e2000225.
Wong AC-N, Chaston JM, Douglas AE. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J. 2013;7:1922–32.
Chandler JA, Morgan Lang J, Bhatnagar S, Eisen JA, Kopp A. Bacterial communities of diverse Drosophila species: ecological context of a host–microbe model system. PLoS Genet. 2011;7:e1002272.
Martinson VG, Douglas AE, Jaenike J. Community structure of the gut microbiota in sympatric species of wild Drosophila. Ecol Lett. 2017;20:629–39.
Adair KL, Wilson M, Bost A, Douglas AE. Microbial community assembly in wild populations of the fruit fly Drosophila melanogaster. ISME J. 2018;12:959–72.
Bost A, Martinson VG, Franzenburg S, Adair KL, Albasi A, Wells MT, et al. Functional variation in the gut microbiome of wild Drosophila populations. Mol Ecol. 2018;27:2834–45.
Staubach F, Baines JF, Künzel S, Bik EM, Petrov DA. Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment. PLoS ONE. 2013;8:e70749.
Brucker RM, Bordenstein SR. The hologenomic basis of speciation: Gut bacteria cause hybrid lethality in the genus Nasonia. Science. 2013;341:667–9.
Markow TA, O’Grady PM. Dietary considerations. In: TA Markow, PM OʼGrady (eds). Drosophila: a guide to species identification and use. Elsevier, London. 2006, p. 215–26.
Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, et al. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome. 2014;2:6.
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the Miseq Illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112–20.
Koyle ML, Veloz M, Judd AM, Wong AC-N, Newell PD, Douglas AE, et al. Rearing the fruit fly Drosophila melanogaster under axenic and gnotobiotic conditions. J Vis Exp. 2016;e54219.
Wong AC-N, Luo Y, Jing X, Franzenburg S, Bost A, Douglas AE. The host as the driver of the microbiota in the gut and external environment of Drosophila melanogaster. Appl Environ Microbiol. 2015;81:6232–40.
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet C, Al-Ghalith GA, et al. QIIME 2: Reproducible, interactive, scalable, and extensible microbiome data science. Epub ahead of print 2018. https://doi.org/10.7287/peerj.preprints.27295v2.
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.
Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B, Grisel O, et al. Scikit-learn: machine learning in python. J Mach Learn Res. 2012;12:2825–30.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl Acids Res. 2013;41:D590–6.
R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2018.
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, et al. Vegan: community ecology package. R package version 2.3-4.
Hsieh TC, Ma KH, Chao A. iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0.8.
Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001;26:32–46.
Kindt R, Coe R. Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. Nairobi, Kenya: World Agroforestry Centre (ICRAF); 2005.
Mazel F, Davis KM, Loudon A, Kwong WK, Groussin M, Parfrey LW. Is host filtering the main driver of phylosymbiosis across the tree of life? mSystems. 2018;3:e00097–18.
Robinson DF, Foulds LR. Comparison of phylogenetic trees. Math Biosci. 1981;53:131–47.
Van Der Linde K, Houle D, Spicer GS, Steppan SJ. A supermatrix-based molecular phylogeny of the family Drosophilidae. Genet Res. 2010;92:25–38.
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B. 1995;57:289–300.
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.
Wong AC, Dobson AJ, Douglas AE. Gut microbiota dictates the metabolic response of Drosophila to diet. J Exp Biol. 2014;217:1894–901.
Miguel-Aliaga I, Jasper H, Lemaitre B. Anatomy and physiology of the digestive tract of Drosophila melanogaster. Genetics. 2018;210:357–96.
Coyte KZ, Schluter J, Foster KR. The ecology of the microbiome: Networks, competition, and stability. Science. 2015;350:663–6.
Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2010;8:15–25.
Inamine H, Ellner SP, Newell PD, Luo Y, Buchon N, Douglas AE. Spatiotemporally heterogeneous population dynamics of gut bacteria inferred from fecal time series data. mBio. 2018;9:e01453–17.
Pais IS, Valente RS, Sporniak M, Teixeira L. Drosophila melanogaster establishes a species-specific mutualistic interaction with stable gut-colonizing bacteria. PLoS Biol. 2018;16:e2005710.
Blum JE, Fischer CN, Miles J, Handelsman J. Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster. mBio. 2013;4:e00860–13-e00860-13.
Ryu J-H, Kim S-H, Lee H-Y, Bai JY, Nam YD, Bae JW, et al. Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science. 2008;319:777–82.
Broderick NA, Buchon N, Lemaitre B. Microbiota-induced changes in Drosophila melanogaster host gene expression and gut morphology. mBio. 2014;5:e01117–14.
Clark RI, Salazar A, Yamada R, Fitz-Gibbon S, Morselli M, Alcaraz J, et al. Distinct shifts in microbiota composition during Drosophila aging impair intestinal function and drive mortality. Cell Rep. 2015;12:1656–67.
Guo L, Karpac J, Tran SL, Jasper H. PGRP-SC2 promotes gut immune homeostasis to limit commensal dysbiosis and extend lifespan. Cell. 2014;156:109–22.
Buchon N, Broderick NA, Chakrabarti S, Lemaitre B. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 2009;23:2333–44.
Overend G, Luo Y, Henderson L, Douglas AE, Davies SA, Dow JAT. Molecular mechanism and functional significance of acid generation in the Drosophila midgut. Sci Rep. 2016;6:27242.
Sackton TB, Lazzaro BP, Schlenke TA, Evans JD, Hultmark D, Clark AG. Dynamic evolution of the innate immune system in Drosophila. Nat Genet. 2007;39:1461–8.
Chaston JM, Newell PD, Douglas AE. Metagenome-wide association of microbial determinants of host phenotype in Drosophila melanogaster. mBio. 2014;5:1–12.
Segata N. On the road to strain-resolved comparative metagenomics. mSystems. 2018;3:e00190–17.
Winans NJ, Walter A, Chouaia B, Chaston JM, Douglas AE, Newell PD. A genomic investigation of ecological differentiation between free-living and Drosophila-associated bacteria. Mol Ecol. 2017;26:4536–50.
Nishida AH, Ochman H. Rates of gut microbiome divergence in mammals. Mol Ecol. 2018;27:1884–97.
Clayton JB, Vangay P, Huang H, Ward T, Hillmann BM, Al-Ghalith GA, et al. Captivity humanizes the primate microbiome. Proc Natl Acad Sci USA. 2016;113:10376–81.
Ericsson AC, Montonye DR, Smith CR, Franklin CL. Modeling a superorganism – considerations regarding the use of “dirty” mice in biomedical research. Yale J Biol Med. 2017;90:361–71.
Schuelke T, Pereira TJ, Hardy SM, Bik HM. Nematode-associated microbial taxa do not correlate with host phylogeny, geographic region or feeding morphology in marine sediment habitats. Mol Ecol. 2018;27:1930–51.
Hird SM, Sánchez C, Carstens BC, Brumfield RT. Comparative gut microbiota of 59 neotropical bird species. Front Microbiol. 2015;6:1403.
Ingala MR, Simmons NB, Wultsch C, Krampis K, Speer KA, Perkins SL. Comparing microbiome sampling methods in a wild mammal: Fecal and intestinal samples record different signals of host ecology, evolution. Front Microbiol. 2018;9:803.
Phillips C, Phelan G, Dowd S, McDonough MM, Ferguson AW, Delton Hanson J, et al. Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography. Mol Ecol. 2012;21:2617–27.
Duar RM, Lin XB, Zheng J, Martino ME, Grenier T, Pérez-Muñoz ME, et al. Lifestyles in transition: evolution and natural history of the genus Lactobacillus. FEMS Microbiol Rev. 2017;41:S27–48.
Vogel H, Müller A, Heckel DG, Gutzeit H, Vilcinskas A. Nutritional immunology: Diversification and diet-dependent expression of antimicrobial peptides in the black soldier fly Hermetia illucens. Dev Comp Immunol. 2018;78:141–8.
Kohl KD, Dearing MD, Bordenstein SR. Microbial communities exhibit host species distinguishability and phylosymbiosis along the length of the gastrointestinal tract. Mol Ecol. 2018;27:1874–83.
Oldroyd GEDD, Murray JD, Poole PS, Downie JA. The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet. 2011;45:119–44.
McFall-Ngai M. Divining the essence of symbiosis: Insights from the squid-Vibrio model. PLoS Biol. 2014;12:e1001783.
Stagaman K, Burns AR, Guillemin K, Bohannan BJM. The role of adaptive immunity as an ecological filter on the gut microbiota in zebrafish. ISME J. 2017;11:1630–9.
Burns AR, Stephens WZ, Stagaman K, Wong S, Rawls JF, Guillemin K, et al. Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J. 2016;10:655–64.
Baxter NT, Wan JJ, Schubert AM, Jenior ML, Myers P, Schloss PD. Intra- and interindividual variations mask interspecies variation in the microbiota of sympatric Peromyscus populations. Appl Environ Microbiol. 2015;81:396–404.
Obadia B, Güvener ZT, Zhang V, Ceja-Navarro JA, Brodie EL, Ja WW, et al. Probabilistic invasion underlies natural gut microbiome stability. Curr Biol. 2017;27:1999–2006.e8.
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.
Author information
Authors and Affiliations
Contributions
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.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/s41396-019-0532-7
This article is cited by
-
Effects of species and sex on the gut microbiome of four laboratory-reared fruit fly lines (Diptera: Tephritidae) using full-length 16S rRNA PacBio Kinnex sequencing
BMC Microbiology (2025)
-
The plant-sucking insect selects assembly of the gut microbiota from environment to enhance host reproduction
npj Biofilms and Microbiomes (2024)
-
Mechanisms of fungal community assembly in wild stoneflies moderated by host characteristics and local environment
npj Biofilms and Microbiomes (2022)
-
Horizontal gene transfer-mediated bacterial strain variation affects host fitness in Drosophila
BMC Biology (2021)
-
Stabilization and optimization of host-microbe-environment interactions as a potential reason for the behavior of natal philopatry
Animal Microbiome (2021)
