Animal hosts have evolved intricate associations with microbial symbionts, where both depend on each other for particular functions. In many cases, these associations lead to phylosymbiosis, where phylogenetically related species harbour compositionally more similar microbiomes than distantly related species. However, evidence for phylosymbiosis is either weak or lacking in gut microbiomes of flying vertebrates, particularly in birds. To shed more light on this phenomenon, we compared cloacal microbiomes of 37 tropical passerine bird species from New Guinea using 16S rRNA bacterial gene sequencing. We show a lack of phylosymbiosis and document highly variable microbiomes. Furthermore, we find that gut bacterial community compositions are species-specific and tend to be shaped by host diet but not sampling locality, potentially driven by the similarities in habitats used by individual species. We further show that flight-associated gut modifications, coupled with individual dietary differences, shape gut microbiome structure and variation, contributing to the lack of phylosymbiosis. These patterns indicate that the stability of symbiosis may depend on microbial functional diversity rather than taxonomic composition. Furthermore, the more variable and fluid host-microbe associations suggest probable disparities in the potential for coevolution between bird host species and microbial symbionts.

Biology Centre of Czech Academy of Sciences Institute of Entomology Ceske Budejovice Branisovska 31 37005 Czech Republic

Faculty of Science University of South Bohemia Ceske Budejovice Branisovska 1760 37005 Czech Republic

Natural History Museum of Denmark University of Copenhagen Copenhagen Denmark

New Guinea Binatang Research Centre Madang Papua New Guinea

Section for Ecology and Evolution Department of Biology University of Copenhagen Copenhagen Denmark

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Youngblut ND, Reischer GH, Walters W, Schuster N, Walzer C, Stalder G, Ley RE, Farnleitner AH. 2019. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat. Commun. 10, 2200. (10.1038/s41467-019-10191-3) PubMed DOI PMC

McFall-Ngai M, et al. 2013. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. USA 110, 3229-3236. (10.1073/pnas.1218525110) PubMed DOI PMC

Brooks AW, Kohl KD, Brucker RM, van Opstal EJ, Bordenstein SR. 2016. Phylosymbiosis: relationships and functional effects of microbial communities across host evolutionary history. PLoS Biol. 14, e2000225. (10.1371/journal.pbio.2000225) PubMed DOI PMC

Pollock FJ, McMinds R, Smith S, Bourne DG, Willis BL, Medina M, Thurber RV, Zaneveld JR. 2018. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat. Commun. 9, 4921. (10.1038/s41467-018-07275-x) PubMed DOI PMC

Kohl KD, Dearing MD, Bordenstein SR. 2018. Microbial communities exhibit host species distinguishability and phylosymbiosis along the length of the gastrointestinal tract. Mol. Ecol. 27, 1874-1883. (10.1111/mec.14460) PubMed DOI PMC

Amato KR, et al. 2019. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J. 13, 576-587. (10.1038/s41396-018-0175-0) PubMed DOI PMC

Dunaj SJ, Bettencourt BR, Garb JE, Brucker RM. 2020. Spider phylosymbiosis: divergence of widow spider species and their tissues' microbiomes. BMC Evol. Biol. 20, 104. (10.1186/s12862-020-01664-x) PubMed DOI PMC

Tinker KA, Ottesen EA. 2020. Phylosymbiosis across deeply diverging lineages of omnivorous cockroaches (Order Blattodea). Appl. Environ. Microbiol. 86, e02513-19. (10.1128/AEM.02513-19) PubMed DOI PMC

van Opstal EJ, Bordenstein SR. 2019. Phylosymbiosis impacts adaptive traits in Nasonia wasps. mBio 10, e00887-19. (10.1128/mBio.00887-19) PubMed DOI PMC

Song SJ, et al. 2020. Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats. mBio 11, e02901-19. (10.1128/mBio.02901-19) PubMed DOI PMC

Grond K, Bell KC, Demboski JR, Santos M, Sullivan JM, Hird SM. 2020. No evidence for phylosymbiosis in western chipmunk species. FEMS Microbiol. Ecol. 96, fiz182. (10.1093/femsec/fiz182) PubMed DOI

Doane MP, et al. 2020. The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge. Microbiome 8, 93. (10.1186/s40168-020-00840-x) PubMed DOI PMC

Capunitan DC, Johnson O, Terrill RS, Hird SM. 2020. Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea. Mol. Ecol. 29, 829-847. (10.1111/mec.15354) PubMed DOI

Trevelline BK, Sosa J, Hartup BK, Kohl KD. 2020. A bird's-eye view of phylosymbiosis: weak signatures of phylosymbiosis among all 15 species of cranes. Proc. Biol. Sci. 287, 20192988. PubMed PMC

Kropackova L, et al. 2017. Codiversification of gastrointestinal microbiota and phylogeny in passerines is not explained by ecological divergence. Mol. Ecol. 26, 5292-5304. (10.1111/mec.14144) PubMed DOI

Hird SM, Sanchez C, Carstens BC, Brumfield RT. 2015. Comparative gut microbiota of 59 neotropical bird species. Front. Microbiol. 6, 1430. PubMed PMC

Loo WT, Garcia-Loor J, Dudaniec RY, Kleindorfer S, Cavanaugh CM. 2019. Host phylogeny, diet, and habitat differentiate the gut microbiomes of Darwin's finches on Santa Cruz Island. Sci. Rep. 9, 18781. (10.1038/s41598-019-54869-6) PubMed DOI PMC

Denbow DM. 2015. Gastrointestinal anatomy and physiology. In Sturkie's Avian physiology (ed. Scanes CG), pp. 301-336. London, UK: Academic Press.

Bodawatta KH, Sam K, Jønsson KA, Poulsen M. 2018. Comparative analyses of the digestive tract microbiota of New Guinean passerine birds. Front. Microbiol. 9, 1830. (10.3389/fmicb.2018.01830) PubMed DOI PMC

Bodawatta KH, Puzejova K, Sam K, Poulsen M, Jønsson KA. 2020. Cloacal swabs and alcohol bird specimens are good proxies for compositional analyses of gut microbial communities of great tits (Parus major). BMC Anim. Microbiome 2, 9. (10.1186/s42523-020-00026-8) PubMed DOI PMC

Grond K, et al. 2019. Composition and drivers of gut microbial communities in Arctic-breeding shorebirds. Front. Microbiol. 10, 2258. (10.3389/fmicb.2019.02258) PubMed DOI PMC

Teyssier A, Matthysen E, Hudin NS, de Neve L, White J, Lens L. 2020. Diet contributes to urban-induced alterations in gut microbiota: experimental evidence from a wild passerine. Proc. Biol. Sci. 287, 20192182. PubMed PMC

Juan PAS, Hendershot JN, Daily GC, Fukami T. 2020. Land-use change has host-specific influences on avian gut microbiomes. ISME J. 14, 318-321. (10.1038/s41396-019-0535-4) PubMed DOI PMC

Gillingham MAF, et al. 2019. Offspring microbiomes differ across breeding sites in a panmictic species. Front. Microbiol. 10, 35. (10.3389/fmicb.2019.00035) PubMed DOI PMC

Hird SM, Carstens BC, Cardiff SW, Dittmann DL, Brumfield RT. 2014. Sampling locality is more detectable than taxonomy or ecology in the gut microbiota of the brood-parasitic brown-headed cowbird (Molothrus ater). PeerJ 2, peerj.321. (10.7717/peerj.321) PubMed DOI PMC

Bodawatta KH, Freiberga I, Puzejova K, Sam K, Poulsen M, Jønsson KA. 2021. Flexibility and resilience of great tit (Parus major) gut microbiomes to changing diets. BMC Anim. Microbiome 3, 20. (10.1186/s42523-021-00076-6) PubMed DOI PMC

Jackson S. 1992. Do seabird gut sizes and mean retention times reflect adaptation to diet and foraging method? Physiol. Zool. 65, 674-697. (10.1086/physzool.65.3.30157976) DOI

Wotton DM, Kelly D. 2012. Do larger frugivores move seeds further? Body size, seed dispersal distance, and a case study of a large, sedentary pigeon. J. Biogeogr. 39, 1973-1983. (10.1111/jbi.12000) DOI

Ricklefs RE. 1996. Morphometry of the digestive tracts of some passerine birds. Condor 98, 279-292. (10.2307/1369146) DOI

Tvardikova K, Novotny V. 2012. Predation on exposed and leaf-rolling artificial caterpillars in tropical forests of Papua New Guinea. J. Trop. Ecol. 28, 331-341. (10.1017/S0266467412000235) DOI

Sam K, Koane B, Jeppy S, Novotny V. 2014. Effect of forest fragmentation on bird species richness in Papua New Guinea. J. Field Ornithol. 85, 152-167. (10.1111/jofo.12057) DOI

Sam K, Koane B, Jeppy S, Sykorova J, Novotny V. 2017. Diet of land birds along an elevational gradient in Papua New Guinea. Sci. Rep. 7, 44018. (10.1038/srep44018) PubMed DOI PMC

Song SJ, Amir A, Metcalf JL, Amato KR, Xu ZZ, Humphrey G, Knight R. 2016. Preservation methods differ in fecal microbiome stability, affecting suitability for field studies. Msystems 1, e00021-16. PubMed PMC

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581-583. (10.1038/nmeth.3869) PubMed DOI PMC

Bolyen E, et al. 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852-857. (10.1038/s41587-019-0209-9) PubMed DOI PMC

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590-D596. (10.1093/nar/gks1219) PubMed DOI PMC

McMurdie PJ. 2013. Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217. (10.1371/journal.pone.0061217) PubMed DOI PMC

R Core Team. 2020. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. See https://www.R-project.org/.

Lahti L, Shetty S. 2017. Microbiome: tools for microbiome analysis in R. Version 2.1.24. See https://github.com/microbiome/microbiome.

Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463-1464. (10.1093/bioinformatics/btq166) PubMed DOI

Paradis E, Schliep K. 2019. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526-528. (10.1093/bioinformatics/bty633) PubMed DOI

Ning D, et al. 2020. A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming. Nat. Commun. 11, 4717. (10.1038/s41467-020-18560-z) PubMed DOI PMC

Oksanen J, et al. . 2019. vegan: Community Ecology Package. R package version 2.5-4. See https://CRAN.R-project.org/package=vegan.

Arbizu MP. 2019. pairwiseAdonis: Pairwise multilevel comparison using adonis R package version 0.3. See https://github.com/pmartinezarbizu/pairwiseAdonis.

Andersen KS, Kirkegaard RH, Karst SM, Albertsen M. 2018. ampvis2: an R package to analyse and visualise 16S rRNA amplicon data. bioRxiv 2018:299537.

Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973. (10.1093/molbev/mss075) PubMed DOI PMC

Rambaut A, Suchard MA, Xie D, Drummond AJ. 2014. Tracer v1.6. See http://beast.bio.ed.ac.uk/Tracer.

Jombart T, Dray S. 2009. adephylo: exploratory analyses for the phylogenetic comparative method. See https://CRAN.R-project.org/package=adephylo.

Schliep KP. 2011. phangorn: phylogenetic analysis in R. Bioinformatics 27, 592-593. (10.1093/bioinformatics/btq706) PubMed DOI PMC

Orme D, et al. 2018. caper: comparative analyses of phylogenetics and evolution in R. R package version 1.0.1. ed. See https://cran.r-project.org/web/packages/caper.

Ogle PH, Wheeler P, Dinno A. 2020. FSA: fisheries stock analysis. R package version 0.8.30. See https://derekogle.com/FSA.

Wickham H. 2016. Ggplot2: elegant graphics for data analysis. New York, NY: Springer-Verlag.

Garnier S. 2018. viridis: Default Color Maps from 'matplotlib'. See https://CRAN.R-project.org/package=viridis.

Gilbert B, Levine JM. 2017. Ecological drift and the distribution of species diversity. Proc. Biol. Sci. 284, 20170507. PubMed PMC

Orrock JL, Watling JI. 2010. Local community size mediates ecological drift and competition in metacommunities. Proc. Biol. Sci. 277, 2185-2191. PubMed PMC

Siqueira T, et al. 2020. Community size can affect the signals of ecological drift and niche selection on biodiversity. Ecology 101, e03014. (10.1002/ecy.3014) PubMed DOI

Groussin M, Mazel F, Sanders JG, Smillie CS, Lavergne S, Thuiller W, Alm EJ. 2017. Unraveling the processes shaping mammalian gut microbiomes over evolutionary time. Nat. Commun. 8, 14319. (10.1038/ncomms14319) PubMed DOI PMC

Moya A, Ferrer M. 2016. Functional redundancy-induced stability of gut microbiota subjected to disturbance. Trends Microbiol. 24, 402-413. (10.1016/j.tim.2016.02.002) PubMed DOI

Grond K, Sandercock BK, Jumpponen A, Zeglin LH. 2018. The avian gut microbiota: community, physiology and function in wild birds. J. Avian Biol. 49, e01788. (10.1111/jav.01788) DOI

Groussin M, Mazel F, Alm EJ. 2020. Co-evolution and co-speciationof host-gut bacteria systems. Cell Host Microbe 28, 12-22. (10.1016/j.chom.2020.06.013) PubMed DOI

Moeller AH, et al. 2016. Cospeciation of gut microbiota with hominids. Science 353, 380-382. (10.1126/science.aaf3951) PubMed DOI PMC

Moeller AH, Sanders JG. 2020. Roles of the gut microbiota in the adaptive evolution of mammalian species. Phil. Trans. R Soc. B 375, 20190597. (10.1098/rstb.2019.0597) PubMed DOI PMC

Moeller AH, Suzuki TA, Phifer-Rixey M, Nachman MW. 2018. Transmission modes of the mammalian gut microbiota. Science 362, 453-457. (10.1126/science.aat7164) PubMed DOI

Gut microbiota variation between climatic zones and due to migration strategy in passerine birds

Within-community variation of interspecific divergence patterns in passerine gut microbiota

Specific gut bacterial responses to natural diets of tropical birds

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