Phylosymbiosis Across Ecosystems: Decoding Microbiome Assembly in Divergent Animal Hosts
DOI:
https://doi.org/10.55544/jrasb.4.6.26Keywords:
Phylosymbiosis, microbiome assembly, environmental filtering, hologenomeAbstract
The assembly of animal-associated microbiomes represents one of the most intricate examples of host-microbe coevolution, yet the relative contributions of host phylogeny versus environmental filtering remain contentious across diverse ecosystems. Here, we present a comprehensive cross-ecosystem analysis of microbial communities associated with 20 animal species spanning vertebrates (teleost fish, amphibians, reptiles, birds, and mammals) and invertebrates (insects, crustaceans, annelids, and cnidarians) across terrestrial, freshwater, and marine habitats. Using integrated 16S rRNA amplicon sequencing, shotgun metagenomics, and generalized linear mixed modeling, we demonstrate that host phylogeny explains 38% of variance in microbiome composition (p < 0.001), establishing it as the primary scaffold for community assembly. However, this phylogenetic signal is modulated by ecosystem type, with salinity emerging as the dominant abiotic driver (R² = 0.32, p < 0.001) and diet contributing 20% of explained variance. Beta diversity analyses revealed distinct ecosystem-level clustering (PERMANOVA: F(2,147) = 18.4, p < 0.001), yet within-ecosystem comparisons confirmed phylosymbiotic patterns where closely related hosts shared more similar microbial profiles than distantly related taxa. Notably, the strength of phylosymbiosis varied markedly across host lineages, being strongest in mammals and weakest in cnidarians, suggesting that gastrointestinal complexity and life history traits mediate evolutionary conservation of host-microbe associations. Environmental substrate microbiomes served as the background pool for host colonization, with SourceTracker analysis estimating 15–40% environmental contribution to skin communities versus only 5–12% to gut communities, indicating stronger host filtering in gastrointestinal niches. These findings advance the hologenome concept by demonstrating hierarchical assembly rules—phylogeny > diet > environment—that govern microbiome architecture across the animal kingdom, with critical implications for conservation biology and ecosystem management.
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[1] Bordenstein, S.R. & Theis, K.R. (2015). Host biology in light of the microbiome: Ten principles of holobionts and hologenomes. PLoS Biology, 13(8), e1002226.
[2] Brooks, A.W., Kohl, K.D., Brucker, R.M., van Opstal, E.J. & Bordenstein, S.R. (2016). Phylosymbiosis: Relationships and functional effects of microbial communities across host evolutionary history. PLoS Biology, 14(11), e2000225.
[3] Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A. & Holmes, S.P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581–583.
[4] Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Lozupone, C.A., Turnbaugh, P.J., (2011). Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences, 108(Suppl. 1), 4516–4522.
[5] Fuhrman, J.A., Steele, J.A., Hewson, I., Schwalbach, M.S., Brown, M.V., Green, J.L.,. (2008). A latitudinal diversity gradient in planktonic marine bacteria. Proceedings of the National Academy of Sciences, 105(22), 7774–7778.
[6] Knights, D., Costello, E.K. & Knight, R. (2011). Supervised classification of human microbiota. FEMS Microbiology Reviews, 35(2), 343–359.
[7] Kohl, K.D., Skopec, M.M. & Dearing, M.D. (2014). Captivity results in disparate loss of gut microbial diversity in closely related hosts. Conservation Physiology, 2(1), cov066.
[8] Ley, R.E., Hamady, M., Lozupone, C., Turnbaugh, P.J., Ramey, R.R., Bircher, J.S., (2008). Evolution of mammals and their gut microbes. Science, 320(5883), 1647–1651.
[9] Li, B., Zhang, X., Guo, H., Su, X., Zhang, X., Wei, W., (2024). Global landscape of gut microbiome diversity and antibiotic resistomes across vertebrates. Science of The Total Environment, 912, 168275.
[10] Love, M.I., Huber, W. & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15(12), 550.
[11] Lozupone, C.A. & Knight, R. (2007). Global patterns in bacterial diversity. Proceedings of the National Academy of Sciences, 104(27), 11436–11440.
[12] McFall-Ngai, M., Hadfield, M.G., Bosch, T.C.G., Carey, H.V., Domazet-Lošo, T., Douglas, A.E.,. (2013). Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences, 110(9), 3229–3236.
[13] Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(D1), D590–D596.
[14] Shade, A., Caporaso, J.G., Handelsman, J., Knight, R. & Fierer, N. (2013). A meta-analysis of changes in bacterial and archaeal communities with time. The ISME Journal, 7(8), 1493–1506.
[15] Song, S.J., Sanders, J.G., Delsuc, F., Metcalf, J., Amato, K., Taylor, M.W.,. (2019). Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats. mBio, 11(1), e02901-19.
[16] Zhang, Y., Li, H., Wang, X., Chen, W., Liu, J. & Zhang, X. (2025). Host phylogeny shapes gut microbiota and predicted functional profiles in captive artiodactyls. Animals, 15(5), 678.
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