Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Host specificity of the gut microbiome

Abstract

Developing general principles of host–microorganism interactions necessitates a robust understanding of the eco-evolutionary processes that structure microbiota. Phylosymbiosis, or patterns of microbiome composition that can be predicted by host phylogeny, is a unique framework for interrogating these processes. Identifying the contexts in which phylosymbiosis does and does not occur facilitates an evaluation of the relative importance of different ecological processes in shaping the microbial community. In this Review, we summarize the prevalence of phylosymbiosis across the animal kingdom on the basis of the current literature and explore the microbial community assembly processes and related host traits that contribute to phylosymbiosis. We find that phylosymbiosis is less prevalent in taxonomically richer microbiomes and hypothesize that this pattern is a result of increased stochasticity in the assembly of complex microbial communities. We also note that despite hosting rich microbiomes, mammals commonly exhibit phylosymbiosis. We hypothesize that this pattern is a result of a unique combination of mammalian traits, including viviparous birth, lactation and the co-evolution of haemochorial placentas and the eutherian immune system, which compound to ensure deterministic microbial community assembly. Examining both the individual and the combined importance of these traits in driving phylosymbiosis provides a new framework for research in this area moving forward.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Current evidence of phylosymbiosis in animals.
Fig. 2: Drivers of microbial community assembly and phylosymbiosis.
Fig. 3: Prevalence of microbial and host immune traits across animal clades.
Fig. 4: Mammalian traits promoting phylosymbiosis.

References

  1. 1.

    Al Nabhani, Z. & Eberl, G. Imprinting of the immune system by the microbiota early in life. Mucosal Immunol. 13, 183–189 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  2. 2.

    Pronovost, G. N. & Hsiao, E. Y. Perinatal interactions between the microbiome, immunity, and neurodevelopment. Immunity 50, 18–36 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  3. 3.

    Sylvia, K. E. & Demas, G. E. A gut feeling: microbiome-brain-immune interactions modulate social and affective behaviors. Horm. Behav. 99, 41–49 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  4. 4.

    Visconti, A. et al. Interplay between the human gut microbiome and host metabolism. Nat. Commun. 10, 4505 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  5. 5.

    Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008). This work examines the gut microbiomes of 60 species of mammals, finding that both host diet and phylogeny strongly influenced gut microbial composition.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. 6.

    Muegge, B. D. et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970–974 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. 7.

    Delsuc, F. et al. Convergence of gut microbiomes in myrmecophagous mammals. Mol. Ecol. 23, 1301–1317 (2014).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  8. 8.

    Song, S. J. et al. Is there convergence of gut microbes in blood-feeding vertebrates? Phil. Trans. R. Soc. B 374, 20180249 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  9. 9.

    McKenney, E. A., Maslanka, M., Rodrigo, A. & Yoder, A. D. Bamboo specialists from two mammalian orders (Primates, Carnivora) share a high number of low-abundance gut microbes. Microb. Ecol. 76, 272–284 (2018).

    PubMed  Article  PubMed Central  Google Scholar 

  10. 10.

    Amato, K. R. et al. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microb. Ecol. 69, 434–443 (2015).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. 11.

    Kohl, K. D., Varner, J., Wilkening, J. L. & Dearing, M. D. Gut microbial communities of American pikas (Ochotona princeps): evidence for phylosymbiosis and adaptations to novel diets. J. Anim. Ecol. 87, 323–330 (2018).

    PubMed  Article  PubMed Central  Google Scholar 

  12. 12.

    Moeller, A. H. & Sanders, J. G. Roles of the gut microbiota in the adaptive evolution of mammalian species. Phil. Trans. R. Soc. B 375, 20190597 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  13. 13.

    Amato, K. R. et al. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J. 13, 576–587 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  14. 14.

    Amato, K. R. et al. Convergence of human and old world monkey gut microbiomes demonstrates the importance of human ecology over phylogeny. Genome Biol. 20, 201 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  15. 15.

    Mazel, F. et al. Is host filtering the main driver of phylosymbiosis across the tree of life? mSystems 3, e00097-18 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  16. 16.

    Brucker, R. M. & Bordenstein, S. R. The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science 341, 667–669 (2013). The study shows that relationships between the microbial communities of Nasonia wasps recapitulate host phylogeny when different species are reared in the same environmental conditions.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  17. 17.

    Bordenstein, S. R. & Theis, K. R. Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol. 13, e1002226 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  18. 18.

    Koskella, B. & Bergelson, J. The study of host–microbiome (co)evolution across levels of selection. Phil. Trans. R. Soc. B 375, 20190604 (2020).

    PubMed  Article  PubMed Central  Google Scholar 

  19. 19.

    Lim, S. J. & Bordenstein, S. R. An introduction to phylosymbiosis. Proc. R. Soc. B 287, 20192900 (2020).

    PubMed  Article  PubMed Central  Google Scholar 

  20. 20.

    O’Brien, P. A. et al. Diverse coral reef invertebrates exhibit patterns of phylosymbiosis. ISME J. 14, 2211–2222 (2020).

    PubMed  PubMed Central  Article  Google Scholar 

  21. 21.

    Kohl, K. D. Ecological and evolutionary mechanisms underlying patterns of phylosymbiosis in host-associated microbial communities. Phil. Trans. R. Soc. B 375, 20190251 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  22. 22.

    Sanders, J. G. et al. Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes. Mol. Ecol. 23, 1268–1283 (2014).

    PubMed  Article  PubMed Central  Google Scholar 

  23. 23.

    Groussin, M. et al. Unraveling the processes shaping mammalian gut microbiomes over evolutionary time. Nat. Commun. 8, 14319 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. 24.

    Thomas, T. et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat. Commun. 7, 11870 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  25. 25.

    Apprill, A. et al. Marine mammal skin microbiotas are influenced by host phylogeny. R. Soc. Open Sci. 7, 192046 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Bird, A. K., Prado-Irwin, S. R., Vredenburg, V. T. & Zink, A. G. Skin microbiomes of California terrestrial salamanders are influenced by habitat more than host phylogeny. Front. Microbiol. 9, 442 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  27. 27.

    Doane, M. P. et al. The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge. Microbiome 8, 93 (2020).

    PubMed  PubMed Central  Article  Google Scholar 

  28. 28.

    Russell, S. L., Chappell, L. & Sullivan, W. in Current Topics in Developmental Biology vol. 135 (ed. Lehmann, R.) 315–351 (Academic, 2019).

  29. 29.

    Russell, S. L., McCartney, E. & Cavanaugh, C. M. Transmission strategies in a chemosynthetic symbiosis: detection and quantification of symbionts in host tissues and their environment. Proc. R. Soc. B 285, 20182157 (2018).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  30. 30.

    Usher, K. M., Kuo, J., Fromont, J. & Sutton, D. C. Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461, 9–13 (2001).

    Article  Google Scholar 

  31. 31.

    Usher, K. M., Sutton, D. C., Toze, S., Kuo, J. & Fromont, J. Inter-generational transmission of microbial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Mar. Freshw. Res. 56, 125–131 (2005).

    Article  Google Scholar 

  32. 32.

    Nyholm, S. V. In the beginning: egg–microbe interactions and consequences for animal hosts. Phil. Trans. R. Soc. B 375, 20190593 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  33. 33.

    Funkhouser, L. J. & Bordenstein, S. R. Mom knows best: the universality of maternal microbial transmission. PLoS Biol. 11, e1001631 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  34. 34.

    Perlmutter, J. I. & Bordenstein, S. R. Microorganisms in the reproductive tissues of arthropods. Nat. Rev. Microbiol. 18, 97–111 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. 35.

    Hosokawa, T., Kikuchi, Y., Shimada, M. & Fukatsu, T. Symbiont acquisition alters behaviour of stinkbug nymphs. Biol. Lett. 4, 45–48 (2008).

    PubMed  Article  PubMed Central  Google Scholar 

  36. 36.

    Dominguez-Bello, M. G. et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl Acad. Sci USA 107, 11971–11975 (2010).

    PubMed  Article  PubMed Central  Google Scholar 

  37. 37.

    Mitchell, C. et al. Delivery mode impacts newborn gut colonization efficiency. Preprint at bioRxiv https://doi.org/10.1101/2020.01.29.919993 (2020).

    Article  Google Scholar 

  38. 38.

    Ferretti, P. et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe 24, 133–145.e5 (2018). This study uses longitudinal sampling of 25 mother–infant pairs to demonstrate persistent colonization of the infant by maternal gut microbial strains and emphasizes the importance of mother–infant microbial transmission.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. 39.

    Brandl, H. B. et al. Composition of bacterial assemblages in different components of reed warbler nests and a possible role of egg incubation in pathogen regulation. PLoS ONE 9, e114861 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  40. 40.

    Kyle, G. Z. & Kyle, P. D. Rehabilitation and Conservation of Chimney Swifts (Driftwood Wildlife Association, 2004).

  41. 41.

    Wang, Y. & Rozen, D. E. Gut microbiota colonization and transmission in the burying beetle Nicrophorus vespilloides throughout development. Appl. Environ. Microbiol. 83, e03250-16 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  42. 42.

    Hosokawa, T. et al. Diverse strategies for vertical symbiont transmission among subsocial stinkbugs. PLoS ONE 8, e65081 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  43. 43.

    Parker, E. S., Dury, G. J. & Moczek, A. P. Transgenerational developmental effects of species-specific, maternally transmitted microbiota in Onthophagus dung beetles: host-symbiont interactions in dung beetles. Ecol. Entomol. 44, 274–282 (2019).

    Article  Google Scholar 

  44. 44.

    Perofsky, A. C., Lewis, R. J., Abondano, L. A., Di Fiore, A. & Meyers, L. A. Hierarchical social networks shape gut microbial composition in wild Verreaux’s sifaka. Proc. R. Soc. B 284, 20172274 (2017).

    PubMed  Article  PubMed Central  Google Scholar 

  45. 45.

    Tung, J. et al. Social networks predict gut microbiome composition in wild baboons. eLife 4, e05224 (2015). This article shows that both shared social group membership and the frequency of social interaction predicted how similar the gut microbiome composition and function of two individuals are.

    PubMed Central  Article  Google Scholar 

  46. 46.

    Song, S. J. et al. Cohabiting family members share microbiota with one another and with their dogs. eLife 2, e00458 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  47. 47.

    Moeller, A. H. et al. Dispersal limitation promotes the diversification of the mammalian gut microbiota. Proc. Natl Acad. Sci. USA 114, 201700122 (2017).

    Article  CAS  Google Scholar 

  48. 48.

    Chandler, J. A., Lang, J. M., Bhatnagar, S., Eisen, J. A. & Kopp, A. Bacterial communities of diverse Drosophila species: ecological context of a host–microbe model system. PLoS Genet. 7, e1002272 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. 49.

    Franzenburg, S. et al. Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proc. Natl Acad. Sci. USA 110, e3730–e3738 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  50. 50.

    McLoughlin, K., Schluter, J., Rakoff-Nahoum, S., Smith, A. L. & Foster, K. R. Host selection of microbiota via differential adhesion. Cell Host Microbe 19, 550–559 (2016).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  51. 51.

    Schluter, J. & Foster, K. R. The evolution of mutualism in gut microbiota via host epithelial selection. PLoS Biol. 10, e1001424 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  52. 52.

    Chu, H. & Mazmanian, S. K. Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nat. Immunol. 14, 668–675 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  53. 53.

    Brugman, S. et al. T lymphocytes control microbial composition by regulating the abundance of Vibrio in the zebrafish gut. Gut Microbes 5, 737–747 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  54. 54.

    Dimitriu, P. A. et al. Temporal stability of the mouse gut microbiota in relation to innate and adaptive immunity. Environ. Microbiol. Rep. 5, 200–210 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  55. 55.

    Kawamoto, S. et al. Foxp3+ T cells regulate immunoglobulin A selection and facilitate diversification of bacterial species responsible for immune homeostasis. Immunity 41, 152–165 (2014).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  56. 56.

    McFall-Ngai, M. J. Care for the community. Nature 445, 153–153 (2007). This article argues that the adaptive immune system may have evolved in part to regulate interactions between vertebrate hosts and commensal microorganisms given the higher-diversity microbiomes observed in vertebrates.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  57. 57.

    Hsu, E. Mutation, selection, and memory in B lymphocytes of exothermic vertebrates. Immunol. Rev. 162, 25–36 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  58. 58.

    Parra, D., Takizawa, F. & Sunyer, J. O. Evolution of B cell immunity. Ann. Rev. Anim. Biosci. 1, 65–97 (2013).

    Article  CAS  Google Scholar 

  59. 59.

    Woodhams, D. C. et al. Host-associated microbiomes are predicted by immune system complexity and climate. Genome Biol. 21, 23 (2020).

    PubMed  PubMed Central  Article  Google Scholar 

  60. 60.

    Zhang, H., Sparks, J. B., Karyala, S. V., Settlage, R. & Luo, X. M. Host adaptive immunity alters gut microbiota. ISME J. 9, 770–781 (2015). This article demonstrates that genetically immunodeficient mice have a distinct microbiome and distinct microbial developmental trajectory compared with wild-type mice.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  61. 61.

    Logan, S. L. et al. The Vibrio cholerae type VI secretion system can modulate host intestinal mechanics to displace gut bacterial symbionts. Proc. Natl Acad. Sci. USA 115, E3779–E3787 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  62. 62.

    Macfarlane, G. T., Macfarlane, S. & Gibson, G. R. Validation of a three-stage compound continuous culture system for investigating the effect of retention time on the ecology and metabolism of bacteria in the human colon. Microb. Ecol. 35, 180–187 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  63. 63.

    Schlomann, B. H., Wiles, T. J., Wall, E. S., Guillemin, K. & Parthasarathy, R. Bacterial cohesion predicts spatial distribution in the larval zebrafish intestine. Biophys. J. 115, 2271–2277 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. 64.

    Godoy-Vitorino, F. et al. Comparative analyses of foregut and hindgut bacterial communities in hoatzins and cows. ISME J. 6, 531–541 (2012).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  65. 65.

    Poole, A. C. et al. Human salivary amylase gene copy number impacts oral and gut microbiomes. Cell Host Microbe 25, 553–564.e7 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  66. 66.

    Kohl, K. D., Sadowska, E. T., Rudolf, A. M., Dearing, M. D. & Koteja, P. Experimental evolution on a wild mammal species results in modifications of gut microbial communities. Front. Microbiol. 7, 634 (2016).

    PubMed  PubMed Central  Google Scholar 

  67. 67.

    Barroso-Batista, J., Demengeot, J. & Gordo, I. Adaptive immunity increases the pace and predictability of evolutionary change in commensal gut bacteria. Nat. Commun. 6, 8945 (2015). This article shows that evolution of Escherichia coli is slower in genetically immunocompromised mice than in wild-type mice.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  68. 68.

    Foster, K. R., Schluter, J., Coyte, K. Z. & Rakoff-Nahoum, S. The evolution of the host microbiome as an ecosystem on a leash. Nature 548, 43–51 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  69. 69.

    Martens, E. C., Chiang, H. C. & Gordon, J. I. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4, 447–457 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  70. 70.

    Zhao, S. et al. Adaptive evolution within gut microbiomes of healthy people. Cell Host Microbe 25, 656–667.e8 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  71. 71.

    Garud, N. R. & Pollard, K. S. Population genetics in the human microbiome. Trends Genet. 36, 53–67 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  72. 72.

    Kwong, W. K., Engel, P., Koch, H. & Moran, N. A. Genomics and host specialization of honey bee and bumble bee gut symbionts. Proc. Natl Acad. Sci. USA 111, 11509–11514 (2014).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  73. 73.

    Wernegreen, J. J. & Moran, N. A. Vertical transmission of biosynthetic plasmids in aphid endosymbionts (Buchnera). J. Bacteriol. 183, 785–790 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  74. 74.

    Moeller, A. H. et al. Cospeciation of gut microbiota with hominids. Science 353, 380–382 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  75. 75.

    Ochman, H. et al. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol. 8, e1000546 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  76. 76.

    Guittar, J., Shade, A. & Litchman, E. Trait-based community assembly and succession of the infant gut microbiome. Nat. Commun. 10, 512 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. 77.

    Vega, N. M. Experimental evolution reveals microbial traits for association with the host gut. PLoS Biol. 17, e3000129 (2019). This study uses experimental evolution of A. veronii in a zebrafish host system to demonstrate that improved microbial motility can be a key adaptation for successful microbial colonization of hosts.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  78. 78.

    Kuthyar, S., Manus, M. B. & Amato, K. R. Leveraging non-human primates for exploring the social transmission of microbes. Curr. Opin. Microbiol. 50, 8–14 (2019).

    PubMed  Article  PubMed Central  Google Scholar 

  79. 79.

    Sarkar, A. et al. Microbial transmission in animal social networks and the social microbiome. Nat. Ecol. Evol. 4, 1020–1035 (2020).

    PubMed  Article  PubMed Central  Google Scholar 

  80. 80.

    Parker, A., Lawson, M. A. E., Vaux, L. & Pin, C. Host-microbe interaction in the gastrointestinal tract. Environ. Microbiol. 20, 2337–2353 (2018).

    PubMed  Article  PubMed Central  Google Scholar 

  81. 81.

    d’Hennezel, E., Abubucker, S., Murphy, L. O. & Cullen, T. W. Total lipopolysaccharide from the human gut microbiome silences Toll-like receptor signaling. mSystems 2, e00046-17 (2017). This study uses computational and experimental analyses to show that lipopolysaccharide from Bacteroidales silences TLR4 signalling for the entire gut microbiota.

    PubMed  PubMed Central  Article  Google Scholar 

  82. 82.

    Jeyakumar, T., Beauchemin, N. & Gros, P. Impact of the microbiome on the human genome. Trends Parasitol. 35, 809–821 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  83. 83.

    Aldunate, M. et al. Antimicrobial and immune modulatory effects of lactic acid and short chain fatty acids produced by vaginal microbiota associated with eubiosis and bacterial vaginosis. Front. Physiol. 6, 164 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  84. 84.

    Mackie, R. I., Sghir, A. & Gaskins, H. R. Developmental microbial ecology of the neonatal gastrointestinal tract. Am. J. Clin. Nutr. 69, 1035s–1045s (1999).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  85. 85.

    Sprockett, D., Fukami, T. & Relman, D. A. Role of priority effects in the early-life assembly of the gut microbiota. Nat. Rev. Gastroenterol. Hepatol. 15, 197–205 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  86. 86.

    Amato, K. R. Incorporating the gut microbiota into models of human and non-human primate ecology and evolution. Am. J. Phys. Anthropol. 159, S196–S215 (2016).

    PubMed  Article  PubMed Central  Google Scholar 

  87. 87.

    Amato, K. R., Jeyakumar, T., Poinar, H. & Gros, P. Shifting climates, foods, and diseases: the human microbiome through evolution. BioEssays 41, e1900034 (2019).

    PubMed  Article  PubMed Central  Google Scholar 

  88. 88.

    Kolodny, O. & Schulenburg, H. Microbiome-mediated plasticity directs host evolution along several distinct time scales. Phil. Trans. R. Soc. B 375, 20190589 (2020).

    PubMed  Article  PubMed Central  Google Scholar 

  89. 89.

    Rudman, S. M. et al. Microbiome composition shapes rapid genomic adaptation of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 116, 20025–20032 (2019). This study alters D. melanogaster microbiota by means of the diet and demonstrates that these changes altered fly body mass and population size and resulted in population genome divergence over five generations.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  90. 90.

    Brucker, R. M. & Bordenstein, S. R. The roles of host evolutionary relationships (genus: Nasonia) and development in structuring microbial communities. Evolution 66, 349–362 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  91. 91.

    Dietrich, C., Köhler, T. & Brune, A. The cockroach origin of the termite gut microbiota: patterns in bacterial community structure reflect major evolutionary events. Appl. Environ. Microbiol. 80, 2261–2269 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  92. 92.

    Brooks, A. W., Kohl, K. D., Brucker, R. M., van Opstal, E. J. & Bordenstein, S. R. Phylosymbiosis: relationships and functional effects of microbial communities across host evolutionary history. PLoS Biol. 15, e2000225 (2016).

    Article  CAS  Google Scholar 

  93. 93.

    Díaz-Sánchez, S., Estrada-Peña, A., Cabezas-Cruz, A. & de la Fuente, J. Evolutionary insights into the tick hologenome. Trends Parasitol. 35, 725–737 (2019).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  94. 94.

    Kwong, W. K. et al. Dynamic microbiome evolution in social bees. Sci. Adv. 3, e1600513 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  95. 95.

    Tinker, K. A. & Ottesen, E. A. Phylosymbiosis across deeply diverging lineages of omnivorous cockroaches (order Blattodea). Appl. Environ. Microbiol. 86, e02513–e02519 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  96. 96.

    Zolnik, C. P., Prill, R. J., Falco, R. C., Daniels, T. J. & Kolokotronis, S.-O. Microbiome changes through ontogeny of a tick pathogen vector. Mol. Ecol. 25, 4963–4977 (2016).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  97. 97.

    Parker, E. S., Newton, I. L. G. & Moczek, A. P. (My microbiome) would walk 10,000 miles: maintenance and turnover of microbial communities in introduced dung beetles. Microb. Ecol. 80, 435–446 (2020).

    PubMed  Article  PubMed Central  Google Scholar 

  98. 98.

    Novakova, E. et al. Mosquito microbiome dynamics, a background for prevalence and seasonality of West Nile virus. Front. Microbiol. 8, 526 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  99. 99.

    Osei-Poku, J., Mbogo, C. M., Palmer, W. J. & Jiggins, F. M. Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from Kenya. Mol. Ecol. 21, 5138–5150 (2012).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  100. 100.

    Colman, D. R., Toolson, E. C. & Takacs-Vesbach, C. D. Do diet and taxonomy influence insect gut bacterial communities? Mol. Ecol. 21, 5124–5137 (2012).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  101. 101.

    Wong, A. C.-N., Chaston, J. M. & Douglas, A. E. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J. 7, 1922–1932 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  102. 102.

    Easson, C. G. & Thacker, R. W. Phylogenetic signal in the community structure of host-specific microbiomes of tropical marine sponges. Front. Microbiol. 5, 532 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  103. 103.

    Schöttner, S. et al. Relationships between host phylogeny, host type and bacterial community diversity in cold-water coral reef sponges. PLoS ONE 8, e55505 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  104. 104.

    Reveillaud, J. et al. Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J. 8, 1198–1209 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  105. 105.

    Webster, N. S. & Thomas, T. The sponge hologenome. mBio 7, e00135-16 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  106. 106.

    Hentschel, U., Piel, J., Degnan, S. M. & Taylor, M. W. Genomic insights into the marine sponge microbiome. Nat. Rev. Microbiol. 10, 641–654 (2012).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  107. 107.

    Griffiths, S. M. et al. Host genetics and geography influence microbiome composition in the sponge Ircinia campana. J. Anim. Ecol. 88, 1684–1695 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  108. 108.

    Cleary, D. F. R. et al. The sponge microbiome within the greater coral reef microbial metacommunity. Nat. Commun. 10, 1644 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  109. 109.

    Hentschel, U. et al. Microbial diversity of marine sponges. Prog. Mol. Subcell. Biol. 37, 59–88 (2003).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  110. 110.

    Glasl, B., Smith, C. E., Bourne, D. G. & Webster, N. S. Exploring the diversity-stability paradigm using sponge microbial communities. Sci. Rep. 8, 8425 (2018).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  111. 111.

    Easson, C. G., Chaves-Fonnegra, A., Thacker, R. W. & Lopez, J. V. Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix. Ecol. Evol. 10, 2007–2020 (2020).

    PubMed  PubMed Central  Article  Google Scholar 

  112. 112.

    Britstein, M. et al. Sponge microbiome stability during environmental acquisition of highly specific photosymbionts. Environ. Microbiol. 22, 3593–3607 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  113. 113.

    Nishida, A. H. & Ochman, H. Rates of gut microbiome divergence in mammals. Mol. Ecol. 8, 1884–1897 (2018).

    Article  Google Scholar 

  114. 114.

    Sherrill-Mix, S. et al. Allometry and ecology of the bilaterian gut microbiome. mBio 9, e00319-18 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  115. 115.

    Knowles, S. C. L., Eccles, R. M. & Baltrūnaitė, L. Species identity dominates over environment in shaping the microbiota of small mammals. Ecol. Lett. 22, 826–837 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  116. 116.

    Kartzinel, T. R., Hsing, J. C., Musili, P. M., Brown, B. R. P. & Pringle, R. M. Covariation of diet and gut microbiome in African megafauna. Proc. Natl Acad. Sci. USA 116, 23588–23593 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  117. 117.

    Trevelline, B. K., Sosa, J., Hartup, B. K. & Kohl, K. D. A bird’s-eye view of phylosymbiosis: weak signatures of phylosymbiosis among all 15 species of cranes. Phil. Trans. R. Soc. B 287, 20192988 (2020).

    CAS  Google Scholar 

  118. 118.

    Capunitan, D. C., Johnson, O., Terrill, R. S. & Hird, S. M. Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea. Mol. Ecol. 29, 829–847 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  119. 119.

    Hird, S. M., Sánchez, C., Carstens, B. C. & Brumfield, R. T. Comparative gut microbiota of 59 neotropical bird species. Front. Microbiol. 6, 1403 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  120. 120.

    Song, S. J. et al. Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats. mBio 11, e02901-19 (2020). This study of 892 vertebrate species finds that the gut microbiomes of birds and bats do not follow a pattern of phylosymbiosis and that bat gut microbiomes are more similar to those of birds than to the gut microbiomes of other mammals.

    PubMed  PubMed Central  Article  Google Scholar 

  121. 121.

    Grond, K. et al. No evidence for phylosymbiosis in western chipmunk species. FEMS Microbiol. Ecol. 96, fiz182 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  122. 122.

    Lutz, H. L. et al. Ecology and host identity outweigh evolutionary history in shaping the bat microbiome. mSystems 4, e00511-19 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  123. 123.

    Gaulke, C. A., Arnold, H. K., Kembel, S. W., O’Dwyer, J. P. & Sharpton, T. J. Ecophylogenetics reveals the evolutionary associations between mammals and their gut microbiota. mBio 9, e01348-18 (2017).

    Article  Google Scholar 

  124. 124.

    Gaulke, C. A. & Sharpton, T. J. The influence of ethnicity and geography on human gut microbiome composition. Nat. Med. 24, 1495–1496 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  125. 125.

    Engelberts, J. P. et al. Characterization of a sponge microbiome using an integrative genome-centric approach. ISME J. 14, 1100–1110 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  126. 126.

    Gauthier, M.-E. A., Watson, J. R. & Degnan, S. M. Draft genomes shed light on the dual bacterial symbiosis that dominates the microbiome of the coral reef sponge Amphimedon queenslandica. Front. Mar. Sci. 3, 196 (2016).

    Article  Google Scholar 

  127. 127.

    Hird, S. M. Context is key: comparative biology illuminates the vertebrate microbiome. mBio 11, e00153-20 (2020).

    PubMed  PubMed Central  Article  Google Scholar 

  128. 128.

    Youngblut, N. D. et al. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat. Commun. 10, 2200 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  129. 129.

    Price, J. T. et al. Characterization of the juvenile green turtle (Chelonia mydas) microbiome throughout an ontogenetic shift from pelagic to neritic habitats. PLoS ONE 12, e0177642 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  130. 130.

    Cabrera-Rubio, R. et al. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am. J. Clin. Nutr. 96, 544–551 (2012).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  131. 131.

    Cioffi, C. C., Tavalire, H. F., Neiderhiser, J. M., Bohannan, B. & Leve, L. D. History of breastfeeding but not mode of delivery shapes the gut microbiome in childhood. PLoS ONE 15, e0235223 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  132. 132.

    Ding, J. et al. The composition and function of pigeon milk microbiota transmitted from parent pigeons to squabs. Front. Microbiol. 11, 1789 (2020).

    PubMed  PubMed Central  Article  Google Scholar 

  133. 133.

    Lane, A. A. et al. Household composition and the infant fecal microbiome: The INSPIRE study. Am. J. Phys. Anthropol. 169, 526–539 (2019).

    PubMed  Article  PubMed Central  Google Scholar 

  134. 134.

    Manus, M., Kuthyar, S., Perroni-Marañón, A. G., Nuñez de la Mora, A. & Amato, K. R. Infant skin bacterial communities vary by skin site and infant age across populations in Mexico and the USA. mSystems https://doi.org/10.1128/mSystems.00834-20 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  135. 135.

    Biedermann, P. H. & Rohlfs, M. Evolutionary feedbacks between insect sociality and microbial management. Curr. Opin. Insect Sci. 22, 92–100 (2017).

    PubMed  Article  PubMed Central  Google Scholar 

  136. 136.

    Chambers, S. A. & Townsend, S. D. Like mother, like microbe: human milk oligosaccharide mediated microbiome symbiosis. Biochem. Soc. Trans. 48, 1139–1151 (2020). This study demonstrates the importance of the microbial properties of breast milk in shaping the infant gut microbiota.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  137. 137.

    Donovan, S. M. et al. Host-microbe interactions in the neonatal intestine: role of human milk oligosaccharides. Adv. Nutr. 3, 450S–455S (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  138. 138.

    Gopalakrishna, K. P. & Hand, T. W. Influence of maternal milk on the neonatal intestinal microbiome. Nutrients 12, 823 (2020).

    CAS  PubMed Central  Article  Google Scholar 

  139. 139.

    Hasselquist, D. & Nilsson, J.-Å. Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Phil. Trans. R. Soc. B 364, 51–60 (2009).

    PubMed  Article  PubMed Central  Google Scholar 

  140. 140.

    Flajnik, M. F. A cold-blooded view of adaptive immunity. Nat. Rev. Immunol. 18, 438–453 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  141. 141.

    Omenetti, S. & Pizarro, T. T. The Treg/Th17 axis: a dynamic balance regulated by the gut microbiome. Front. Immunol. 6, 639 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  142. 142.

    Chaouat, G. Reconsidering the Medawar paradigm placental viviparity existed for eons, even in vertebrates; without a “problem”: why are Tregs important for preeclampsia in great apes? J. Reprod. Immunol. 114, 48–57 (2016).

    PubMed  Article  PubMed Central  Google Scholar 

  143. 143.

    Samstein, R. M., Josefowicz, S. Z., Arvey, A., Treuting, P. M. & Rudensky, A. Y. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell 150, 29–38 (2012). This article argues that the adaptive immune system may have evolved in part to regulate interactions between vertebrate hosts and commensal microorganisms given the higher-diversity microbiomes observed in vertebrates.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  144. 144.

    Campbell, C. et al. Extrathymically generated regulatory T cells establish a niche for intestinal border-dwelling bacteria and affect physiologic metabolite balance. Immunity 48, 1245–1257.e9 (2018). This article shows that reduction of pTreg cell activity alters host epithelial cells, reduces gut microbial diversity and alters gut microbiome function.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  145. 145.

    Yadav, M., Stephan, S. & Bluestone, J. A. Peripherally induced Tregs — role in immune homeostasis and autoimmunity. Front. Immunol. 4, 232 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  146. 146.

    Lund, F. E. & Randall, T. D. Effector and regulatory B cells: modulators of CD4+ T cell immunity. Nat. Rev. Immunol. 10, 236–247 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  147. 147.

    McCoy, K. D., Burkhard, R. & Geuking, M. B. The microbiome and immune memory formation. Immunol. Cell Biol. 97, 625–635 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  148. 148.

    Azad, M. B. et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ 185, 385–394 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  149. 149.

    Younge, N. E., Araújo-Pérez, F., Brandon, D. & Seed, P. C. Early-life skin microbiota in hospitalized preterm and full-term infants. Microbiome 6, 98 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  150. 150.

    Perofsky, A. C., Lewis, R. J. & Meyers, L. A. Terrestriality and bacterial transfer: a comparative study of gut microbiomes in sympatric Malagasy mammals. ISME J. 13, 50–63 (2019).

    PubMed  Article  PubMed Central  Google Scholar 

  151. 151.

    Grieneisen, L. E. et al. Genes, geology and germs: gut microbiota across a primate hybrid zone are explained by site soil properties, not host species. Proc. R. Soc. B 286, 20190431 (2019).

    PubMed  Article  PubMed Central  Google Scholar 

  152. 152.

    Rutayisire, E., Huang, K., Liu, Y. & Tao, F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants’ life: a systematic review. BMC Gastroenterol. 16, 86 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  153. 153.

    Wampach, L. et al. Colonization and succession within the human gut microbiome by archaea, bacteria, and microeukaryotes during the first year of life. Front. Microbiol. 8, 738 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  154. 154.

    Cullender, T. C. et al. Innate and adaptive immunity interact to quench microbiome flagellar motility in the gut. Cell Host Microbe 14, 571–581 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  155. 155.

    Suzuki, K. et al. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc. Natl Acad. Sci. USA 101, 1981–1986 (2004).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  156. 156.

    Stagaman, K., Burns, A. R., Guillemin, K. & Bohannan, B. J. The role of adaptive immunity as an ecological filter on the gut microbiota in zebrafish. ISME J. 11, 1630–1639 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  157. 157.

    Lochmiller, R. L. & Deerenberg, C. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87–98 (2000).

    Article  Google Scholar 

  158. 158.

    Martin, L. B., Weil, Z. M. & Nelson, R. J. Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Phil. Trans. R. Soc. B 363, 321–339 (2008).

    PubMed  Article  PubMed Central  Google Scholar 

  159. 159.

    Ingala, M. R., Becker, D. J., Bak Holm, J., Kristiansen, K. & Simmons, N. B. Habitat fragmentation is associated with dietary shifts and microbiota variability in common vampire bats. Ecol. Evol. 9, 6508–6523 (2019).

    PubMed  PubMed Central  Google Scholar 

  160. 160.

    Phillips, C. D. et al. Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography. Mol. Ecol. 21, 2617–2627 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  161. 161.

    Banerjee, A. et al. Novel insights into immune systems of bats. Front. Immunol. 11, 26 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  162. 162.

    Brun, A. et al. Morphological bases for intestinal paracellular absorption in bats and rodents. J. Morphol. 280, 1359–1369 (2019).

    PubMed  PubMed Central  Google Scholar 

  163. 163.

    Caviedes-Vidal, E. et al. Paracellular absorption: a bat breaks the mammal paradigm. PLoS ONE 3, e1425 (2008).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  164. 164.

    Price, E. R., Brun, A., Caviedes-Vidal, E. & Karasov, W. H. Digestive adaptations of aerial lifestyles. Physiology 30, 69–78 (2015).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  165. 165.

    Rodriguez-Peña, N., Price, E. R., Caviedes-Vidal, E., Flores-Ortiz, C. M. & Karasov, W. H. Intestinal paracellular absorption is necessary to support the sugar oxidation cascade in nectarivorous bats. J. Exp. Biol. 219, 779–782 (2016).

    PubMed  Article  PubMed Central  Google Scholar 

  166. 166.

    Hayman, D. T. S. Bat tolerance to viral infections. Nat. Microbiol. 4, 728–729 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  167. 167.

    O’Shea, T. J. et al. Bat flight and zoonotic viruses. Emerg. Infect. Dis. 20, 741–745 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  168. 168.

    Zhang, G. et al. Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science 339, 456–460 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  169. 169.

    Ahn, M., Cui, J., Irving, A. T. & Wang, L.-F. Unique loss of the PYHIN gene family in bats amongst mammals: implications for inflammasome sensing. Sci. Rep. 6, 21722 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  170. 170.

    Härtlova, A. et al. DNA damage primes the type I Interferon system via the cytosolic DNA sensor STING to promote anti-microbial innate immunity. Immunity 42, 332–343 (2015).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  171. 171.

    Rathinam, V. A. K. et al. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11, 395–402 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  172. 172.

    Xie, J. et al. Dampened STING-dependent interferon activation in bats. Cell Host Microbe 23, 297–301.e4 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  173. 173.

    Zhou, P. et al. Contraction of the type I IFN locus and unusual constitutive expression of IFN-α in bats. Proc. Natl Acad. Sci. USA 113, 2696–2701 (2016).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  174. 174.

    Stockmaier, S., Dechmann, D. K. N., Page, R. A. & O’Mara, M. T. No fever and leucocytosis in response to a lipopolysaccharide challenge in an insectivorous bat. Biol. Lett. 11, 20150576 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  175. 175.

    Kohl, K. D. & Dearing, M. D. Experience matters: prior exposure to plant toxins enhances diversity of gut microbes in herbivores. Ecol. Lett. 15, 1008–1015 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  176. 176.

    Gomez, A. et al. Plasticity in the human gut microbiome defies evolutionary constraints. mSphere 4, e00271-19 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  177. 177.

    Wooding, P. and Burton, G. Comparative Placentation: Structures, Functions and Evolution (Springer, 2008).

  178. 178.

    Andersen, K. G., Nissen, J. K. & Betz, A. G. Comparative genomics reveals key gain-of-function events in Foxp3 during regulatory T cell evolution. Front. Immunol. 3, 113 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  179. 179.

    Mess, A. & Carter, A. M. Evolution of the placenta during the early radiation of placental mammals. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 148, 769–779 (2007).

    Article  CAS  Google Scholar 

  180. 180.

    Wildman, D. E. et al. Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc. Natl Acad. Sci. USA 103, 3203–3208 (2006). This article concludes that the ancestral from of the mammalian placenta was the invasive, haemochorial form.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

Download references

Acknowledgements

K.R.A. is supported as a fellow in CIFAR’s Humans & the Microbiome programme. E.K.M. is supported by the Vanderbilt Microbiome Initiative and was partially supported by CIFAR.

Author information

Affiliations

Authors

Contributions

The authors contributed equally to all aspects of the article.

Corresponding author

Correspondence to Katherine R. Amato.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Microbiology thanks K. Kohl; R. Ley, who co-reviewed with N. Youngblut; and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Related links

TimeTree: http://timetree.org

Supplementary information

Glossary

Phylosymbiosis

Similarities in host-associated microbial community structure that mirror the phylogenetic relationships of the hosts.

Vertical transmission

A pathway of transmission where a symbiotic organism is transmitted from the host parent to offspring.

Co-evolution

Reciprocal genetic change in two species that occurs as a result of the selective pressures that each imposes on the other.

Priority effects

A phenomenon in which species that arrive first at a site alter the abiotic and/or biotic conditions such that this impacts the colonization success of species arriving later.

Ecological drift

The random fluctuation of species abundances in a community or population, often as a result of isolation from other populations.

Horizontal transmission

A pathway of transmission where a symbiotic organism is transmitted between individuals via the social or physical environment instead of from parent to offspring.

Oviparous animals

Animals that lay eggs and in which embryonic development does not occur internally in the mother.

Ovipositors

Tubes through which a female animal lays or deposits eggs; most often refers to a structure found in insects.

Viviparous animals

Animals characterized by live birth (viviparity) of offspring with embryonic development occurring internally in the mother.

Innate immune system

A non-specific immune response to potential pathogens found in invertebrates and vertebrates. In vertebrates, the innate immune system has a role in activating the adaptive immune system.

Adaptive immune system

The portion of the immune system that, in vertebrates, allows an organism to identify, learn about and respond to specific pathogens.

Sacculated foregut

A multichambered stomach which allows microbial fermentation before food moves further into the digestive tract.

Co-diversification

Diversification of two species at the same pace and that have a shared evolutionary history as a result of either co-evolution or a shared environment.

Niche construction

When a species changes its local environment, altering the selective pressures acting on it and other organisms in its environment.

Succession

The process of change in the composition of an ecological community over time, often involving increasing community diversity.

Endosymbionts

Symbiotic, often mutualistic, organisms living inside the tissue of another organism. Symbionts are transmitted either horizontally or vertically, and the symbiosis relationship can be obligatory or not obligatory.

Host specificity

Microbial ability to colonize a host depending on physiological interactions with the host and environmental requirements (for example, pH tolerance, biofilm regulation and polysaccharide utilization loci).

Monotremes

Egg-laying mammals.

Matrilineal species

Species in which females remain in their natal group, males disperse, dominance rank is inherited by females from their mothers and social bonds between closely related females are strong.

Prebiotics

Dietary items which provide substrates for bacterial growth in the digestive tract.

Sympatric terrestrial species

Distinct species living in the same terrestrial habitat.

Sympatric arboreal species

Distinct species living in the same arboreal habitat.

Host selectivity

Host ability to limit the microbial strains that associate with it via various physiological filters (for example, immune system, gut anatomy and diet/nutrients).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mallott, E.K., Amato, K.R. Host specificity of the gut microbiome. Nat Rev Microbiol (2021). https://doi.org/10.1038/s41579-021-00562-3

Download citation

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing