1932

Abstract

Animals harbor diverse communities of microbes within their gastrointestinal tracts. Phylogenetic relationship, diet, gut morphology, host physiology, and ecology all influence microbiome composition within and between animal clades. Emerging evidence points to host genetics as also playing a role in determining gut microbial composition within species. Here, we discuss recent advances in the study of microbiome heritability across a variety of animal species Candidate gene and discovery-based studies in humans, mice, , , cattle, swine, poultry, and baboons reveal trends in the types of microbes that are heritable and the host genes and pathways involved in shaping the microbiome. Heritable gut microbes within a host species tend to be phylogenetically restricted. Host genetic variation in immune- and growth-related genes drives the abundances of these heritable bacteria within the gut. With only a small slice of the metazoan branch of the tree of life explored to date, this is an area rife with opportunities to shed light into the mechanisms governing host–microbe relationships.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-020420-032054
2022-02-15
2024-06-19
Loading full text...

Full text loading...

/deliver/fulltext/animal/10/1/annurev-animal-020420-032054.html?itemId=/content/journals/10.1146/annurev-animal-020420-032054&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Gilbert JA, Jansson JK, Knight R. 2014. The Earth Microbiome project: successes and aspirations. BMC Biol. 12:69
    [Google Scholar]
  2. 2. 
    Huttenhower C, Gevers D, Knight R, Abubucker S, Badger JH et al. 2012. Structure, function and diversity of the healthy human microbiome. Nature 486:7402207–14
    [Google Scholar]
  3. 3. 
    Peixoto RS, Harkins DM, Nelson KE. 2021. Advances in microbiome research for animal health. Annu. Rev. Anim. Biosci. 9:289–311
    [Google Scholar]
  4. 4. 
    Ezenwa VO, Gerardo NM, Inouye DW, Medina M, Xavier JB. 2012. Animal behavior and the microbiome. Science 338:6104198–99
    [Google Scholar]
  5. 5. 
    Moeller AH, Sanders JG. 2020. Roles of the gut microbiota in the adaptive evolution of mammalian species. Philos. Trans. R. Soc. B 375:180820190597
    [Google Scholar]
  6. 6. 
    Sender R, Fuchs S, Milo R. 2016. Revised estimates for the number of human and bacteria cells in the body. PLOS Biol. 14:8e1002533
    [Google Scholar]
  7. 7. 
    Waite DW, Taylor M. 2015. Exploring the avian gut microbiota: current trends and future directions. Front. Microbiol. 6:673
    [Google Scholar]
  8. 8. 
    Colman DR, Toolson EC, Takacs-Vesbach CD. 2012. Do diet and taxonomy influence insect gut bacterial communities?. Mol. Ecol. 21:205124–37
    [Google Scholar]
  9. 9. 
    Engel P, Moran NA. 2013. The gut microbiota of insects—diversity in structure and function. FEMS Microbiol. Rev. 37:5699–735
    [Google Scholar]
  10. 10. 
    Grond K, Sandercock BK, Jumpponen A, Zeglin LH 2018. The avian gut microbiota: community, physiology and function in wild birds. J. Avian Biol. 49:11e01788
    [Google Scholar]
  11. 11. 
    Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR et al. 2008. Evolution of mammals and their gut microbes. Science 320:58831647–51
    [Google Scholar]
  12. 12. 
    Youngblut ND, Reischer GH, Walters W, Schuster N, Walzer C et al. 2019. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat. Commun. 10:2200
    [Google Scholar]
  13. 13. 
    Levin D, Raab N, Pinto Y, Rothschild D, Zanir G et al. 2021. Diversity and functional landscapes in the microbiota of animals in the wild. Science 372:6539eabb5352
    [Google Scholar]
  14. 14. 
    McFall-Ngai MJ, Ruby EG. 1991. Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science 254:50371491–94
    [Google Scholar]
  15. 15. 
    Ainsworth TD, Krause L, Bridge T, Torda G, Raina J-B et al. 2015. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J 9:102261–74
    [Google Scholar]
  16. 16. 
    Wong AC-N, Chaston JM, Douglas AE 2013. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J. 7:101922–32
    [Google Scholar]
  17. 17. 
    Song SJ, Sanders JG, Delsuc F, Metcalf J, Amato K et al. 2020. Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats. mBio 11:1e02901-19
    [Google Scholar]
  18. 18. 
    Hammer TJ, Sanders JG, Fierer N. 2019. Not all animals need a microbiome. FEMS Microbiol. Lett. 366:10fnz117
    [Google Scholar]
  19. 19. 
    Muegge BD, Kuczynski J, Knights D, Clemente JC, González A et al. 2011. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:6032970–74
    [Google Scholar]
  20. 20. 
    Singh RK, Chang H-W, Yan D, Lee KM, Ucmak D et al. 2017. Influence of diet on the gut microbiome and implications for human health. J. Transl. Med. 15:73
    [Google Scholar]
  21. 21. 
    Sarkar A, Harty S, Johnson KV-A, Moeller AH, Archie EA et al. 2020. Microbial transmission in animal social networks and the social microbiome. Nat. Ecol. Evol. 4:81020–35
    [Google Scholar]
  22. 22. 
    Trinh P, Zaneveld JR, Safranek S, Rabinowitz PM 2018. One Health relationships between human, animal, and environmental microbiomes: a mini-review. Front. Public Health 6:235
    [Google Scholar]
  23. 23. 
    Noller HF, Woese CR. 1981. Secondary structure of 16S ribosomal RNA. Science 212:4493403–11
    [Google Scholar]
  24. 24. 
    Cai L, Ye L, Tong AHY, Lok S, Zhang T. 2013. Biased diversity metrics revealed by bacterial 16S pyrotags derived from different primer sets. PLOS ONE 8:1e53649
    [Google Scholar]
  25. 25. 
    Knight R, Vrbanac A, Taylor BC, Aksenov A, Callewaert C et al. 2018. Best practices for analysing microbiomes. Nat. Rev. Microbiol. 16:7410–22
    [Google Scholar]
  26. 26. 
    Youngblut ND, de la Cuesta-Zuluaga J, Reischer GH, Dauser S, Schuster N et al. 2020. Large-scale metagenome assembly reveals novel animal-associated microbial genomes, biosynthetic gene clusters, and other genetic diversity. mSystems 5:6e01045-20
    [Google Scholar]
  27. 27. 
    Goodrich JK, Di Rienzi SC, Poole AC, Koren O, Walters WA et al. 2014. Conducting a microbiome study. Cell 158:2250–62
    [Google Scholar]
  28. 28. 
    Baumann P. 2005. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59:155–89
    [Google Scholar]
  29. 29. 
    Milani C, Mancabelli L, Lugli GA, Duranti S, Turroni F et al. 2015. Exploring vertical transmission of Bifidobacteria from mother to child. Appl. Environ. Microbiol. 81:207078–87
    [Google Scholar]
  30. 30. 
    Zoetendal EG, Akkermans ADL, Akkermans-van Vliet WM, de Visser JAGM, de Vos WM. 2001. The host genotype affects the bacterial community in the human gastrointestinal tract. Microb. Ecol. Health Dis. 13:129–34
    [Google Scholar]
  31. 31. 
    Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O et al. 2014. Human genetics shape the gut microbiome. Cell 159:4789–99
    [Google Scholar]
  32. 32. 
    Goodrich JK, Davenport ER, Beaumont M, Jackson MA, Knight R et al. 2016. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe 19:5731–43
    [Google Scholar]
  33. 33. 
    Khachatryan ZA, Ktsoyan ZA, Manukyan GP, Kelly D, Ghazaryan KA, Aminov RI. 2008. Predominant role of host genetics in controlling the composition of gut microbiota. PLOS ONE 3:8e3064
    [Google Scholar]
  34. 34. 
    Altshuler D, Daly MJ, Lander ES. 2008. Genetic mapping in human disease. Science 322:5903881–88
    [Google Scholar]
  35. 35. 
    Ahlqvist E, Hultqvist M, Holmdahl R. 2009. The value of animal models in predicting genetic susceptibility to complex diseases such as rheumatoid arthritis. Arthritis Res. Ther. 11:226
    [Google Scholar]
  36. 36. 
    Visscher PM, Brown MA, McCarthy MI, Yang J. 2012. Five years of GWAS discovery. Am. J. Hum. Genet. 90:17–24
    [Google Scholar]
  37. 37. 
    Visscher PM, Wray NR, Zhang Q, Sklar P, McCarthy MI et al. 2017. 10 years of GWAS discovery: biology, function, and translation. Am. J. Hum. Genet. 101:15–22
    [Google Scholar]
  38. 38. 
    Buniello A, MacArthur JAL, Cerezo M, Harris LW, Hayhurst J et al. 2019. The NHGRI-EBI GWAS catalog of published genome-wide association studies, targeted arrays and summary statistics 2019. Nucleic Acids Res 47:D1D1005–12
    [Google Scholar]
  39. 39. 
    Lim MY, You HJ, Yoon HS, Kwon B, Lee JY et al. 2017. The effect of heritability and host genetics on the gut microbiota and metabolic syndrome. Gut 66:61031–38
    [Google Scholar]
  40. 40. 
    Turpin W, Espin-Garcia O, Xu W, Silverberg MS, Kevans D et al. 2016. Association of host genome with intestinal microbial composition in a large healthy cohort. Nat. Genet. 48:1413–17
    [Google Scholar]
  41. 41. 
    Blekhman R, Goodrich JK, Huang K, Sun Q, Bukowski R et al. 2015. Host genetic variation impacts microbiome composition across human body sites. Genome Biol 16:191
    [Google Scholar]
  42. 42. 
    Kolde R, Franzosa EA, Rahnavard G, Hall AB, Vlamakis H et al. 2018. Host genetic variation and its microbiome interactions within the Human Microbiome Project. Genome Med 10:6
    [Google Scholar]
  43. 43. 
    Davenport ER, Cusanovich DA, Michelini K, Barreiro LB, Ober C, Gilad Y. 2015. Genome-wide association studies of the human gut microbiota. PLOS ONE 10:11e0140301
    [Google Scholar]
  44. 44. 
    Wang J, Thingholm LB, Skiecevičienė J, Rausch P, Kummen M et al. 2016. Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota. Nat. Genet. 48:111396–406
    [Google Scholar]
  45. 45. 
    Hughes DA, Bacigalupe R, Wang J, Rühlemann MC, Tito RY et al. 2020. Genome-wide associations of human gut microbiome variation and implications for causal inference analyses. Nat. Microbiol. 5:91079–87
    [Google Scholar]
  46. 46. 
    Kurilshikov A, Medina-Gomez C, Bacigalupe R, Radjabzadeh D, Wang J et al. 2021. Large-scale association analyses identify host factors influencing human gut microbiome composition. Nat. Genet. 53:2156–65
    [Google Scholar]
  47. 47. 
    Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T et al. 2018. Environment dominates over host genetics in shaping human gut microbiota. Nature 555:7695210–15
    [Google Scholar]
  48. 48. 
    Davenport ER. 2016. Elucidating the role of the host genome in shaping microbiome composition. Gut Microbes 7:2178–84
    [Google Scholar]
  49. 49. 
    Goodrich JK, Davenport ER, Waters JL, Clark AG, Ley RE. 2016. Cross-species comparisons of host genetic associations with the microbiome. Science 352:6285532–35
    [Google Scholar]
  50. 50. 
    Goodrich JK, Davenport ER, Clark AG, Ley RE. 2017. The relationship between the human genome and microbiome comes into view. Annu. Rev. Genet. 51:413–33
    [Google Scholar]
  51. 51. 
    Weissbrod O, Rothschild D, Barkan E, Segal E 2018. Host genetics and microbiome associations through the lens of genome wide association studies. Curr. Opin. Microbiol. 44:9–19
    [Google Scholar]
  52. 52. 
    Bonder MJ, Kurilshikov A, Tigchelaar EF, Mujagic Z, Imhann F et al. 2016. The effect of host genetics on the gut microbiome. Nat. Genet. 48:111407–12
    [Google Scholar]
  53. 53. 
    Kostic AD, Howitt MR, Garrett WS. 2013. Exploring host-microbiota interactions in animal models and humans. Genes Dev 27:7701–18
    [Google Scholar]
  54. 54. 
    Korach-Rechtman H, Freilich S, Gerassy-Vainberg S, Buhnik-Rosenblau K, Danin-Poleg Y et al. 2019. Murine genetic background has a stronger impact on the composition of the gut microbiota than maternal inoculation or exposure to unlike exogenous microbiota. Appl. Environ. Microbiol. 85:18e00826-19
    [Google Scholar]
  55. 55. 
    Kovacs A, Ben-Jacob N, Tayem H, Halperin E, Iraqi FA, Gophna U. 2011. Genotype is a stronger determinant than sex of the mouse gut microbiota. Microb. Ecol. 61:2423–28
    [Google Scholar]
  56. 56. 
    Hoy YE, Bik EM, Lawley TD, Holmes SP, Monack DM et al. 2015. Variation in taxonomic composition of the fecal microbiota in an inbred mouse strain across individuals and time. PLOS ONE 10:11e0142825
    [Google Scholar]
  57. 57. 
    Ericsson AC, Davis JW, Spollen W, Bivens N, Givan S et al. 2015. Effects of vendor and genetic background on the composition of the fecal microbiota of inbred mice. PLOS ONE 10:2e0116704
    [Google Scholar]
  58. 58. 
    Leamy LJ, Kelly SA, Nietfeldt J, Legge RM, Ma F et al. 2014. Host genetics and diet, but not immunoglobulin A expression, converge to shape compositional features of the gut microbiome in an advanced intercross population of mice. Genome Biol 15:12552
    [Google Scholar]
  59. 59. 
    Campbell JH, Foster CM, Vishnivetskaya T, Campbell AG, Yang ZK et al. 2012. Host genetic and environmental effects on mouse intestinal microbiota. ISME J 6:112033–44
    [Google Scholar]
  60. 60. 
    Benson AK, Kelly SA, Legge R, Ma F, Low SJ et al. 2010. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. PNAS 107:4418933–38
    [Google Scholar]
  61. 61. 
    Zhang C, Zhang M, Wang S, Han R, Cao Y et al. 2010. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J. 4:2232–41
    [Google Scholar]
  62. 62. 
    Carmody RN, Gerber GK, Luevano JM, Gatti DM, Somes L et al. 2015. Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17:172–84
    [Google Scholar]
  63. 63. 
    O'Connor A, Quizon PM, Albright JE, Lin FT, Bennett BJ 2014. Responsiveness of cardiometabolic-related microbiota to diet is influenced by host genetics. Mamm. Genome 25:11583–99
    [Google Scholar]
  64. 64. 
    Parks BW, Nam E, Org E, Kostem E, Norheim F et al. 2013. Genetic control of obesity and gut microbiota composition in response to high-fat, high-sucrose diet in mice. Cell Metab 17:1141–52
    [Google Scholar]
  65. 65. 
    Adair KL, Wilson M, Bost A, Douglas AE. 2018. Microbial community assembly in wild populations of the fruit fly Drosophila melanogaster. ISME J 12:4959–72
    [Google Scholar]
  66. 66. 
    Douglas AE. 2018. The Drosophila model for microbiome research. Lab. Anim. 47:6157–64
    [Google Scholar]
  67. 67. 
    Blum JE, Fischer CN, Miles J, Handelsman J 2013. Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster. mBio 4:6e00860-13
    [Google Scholar]
  68. 68. 
    Mistry R, Kounatidis I, Ligoxygakis P 2017. Interaction between familial transmission and a constitutively active immune system shapes gut microbiota in Drosophila melanogaster. Genetics 206:2889–904
    [Google Scholar]
  69. 69. 
    Vázquez-Arreguín K, Bensard C, Schell JC, Swanson E, Chen X et al. 2019. Oct1/Pou2f1 is selectively required for colon regeneration and regulates colon malignancy. PLOS Genet 15:5e1007687
    [Google Scholar]
  70. 70. 
    Dantoft W, Davis MM, Lindvall JM, Tang X, Uvell H et al. 2013. The Oct1 homolog Nubbin is a repressor of NF-κB-dependent immune gene expression that increases the tolerance to gut microbiota. BMC Biol 11:99
    [Google Scholar]
  71. 71. 
    Ryu J-H, Kim S-H, Lee H-Y, Bai JY, Nam Y-D et al. 2008. Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila. Science 319:5864777–82
    [Google Scholar]
  72. 72. 
    Early AM, Shanmugarajah N, Buchon N, Clark AG. 2017. Drosophila genotype influences commensal bacterial levels. PLOS ONE 12:1e0170332
    [Google Scholar]
  73. 73. 
    Chaston JM, Dobson AJ, Newell PD, Douglas AE. 2016. Host genetic control of the microbiota mediates the Drosophila nutritional phenotype. Appl. Environ. Microbiol. 82:2671–79
    [Google Scholar]
  74. 74. 
    Zhang F, Berg M, Dierking K, Félix M-A, Shapira M et al. 2017. Caenorhabditis elegans as a model for microbiome research. Front. Microbiol. 8:485
    [Google Scholar]
  75. 75. 
    Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:171–94
    [Google Scholar]
  76. 76. 
    Kaletta T, Hengartner MO. 2006. Finding function in novel targets: C. elegans as a model organism. Nat. Rev. Drug Discov. 5:5387–99
    [Google Scholar]
  77. 77. 
    Berg M, Zhou XY, Shapira M. 2016. Host-specific functional significance of Caenorhabditis gut commensals. Front. Microbiol. 7:1622
    [Google Scholar]
  78. 78. 
    Berg M, Monnin D, Cho J, Nelson L, Crits-Christoph A, Shapira M 2019. TGFβ/BMP immune signaling affects abundance and function of C. elegans gut commensals. Nat. Commun. 10:604
    [Google Scholar]
  79. 79. 
    Taylor M, Vega NM 2021. Host immunity alters community ecology and stability of the microbiome in a Caenorhabditis elegans model. mSystems 6:2e00608-20
    [Google Scholar]
  80. 80. 
    Dirksen P, Assié A, Zimmermann J, Zhang F, Tietje A-M et al. 2020. CeMbio—the Caenorhabditis elegans microbiome resource. G3 10:93025–39
    [Google Scholar]
  81. 81. 
    Zhang F, Weckhorst JL, Assié A, Hosea C, Ayoub CA et al. 2021. Natural genetic variation drives microbiome selection in the Caenorhabditis elegans gut. Curr. Biol. 31:122603–18
    [Google Scholar]
  82. 82. 
    Chandler JA, Lang JM, Bhatnagar S, Eisen JA, Kopp A. 2011. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLOS Genet. 7:9e1002272
    [Google Scholar]
  83. 83. 
    Berg M, Stenuit B, Ho J, Wang A, Parke C et al. 2016. Assembly of the Caenorhabditis elegans gut microbiota from diverse soil microbial environments. ISME J 10:81998–2009
    [Google Scholar]
  84. 84. 
    Huggins MA, Sjaastad FV, Pierson M, Kucaba TA, Swanson W et al. 2019. Microbial exposure enhances immunity to pathogens recognized by TLR2 but increases susceptibility to cytokine storm through TLR4 sensitization. Cell Rep 28:71729–43.e5
    [Google Scholar]
  85. 85. 
    Parker KD, Albeke SE, Gigley JP, Goldstein AM, Ward NL. 2018. Microbiome composition in both wild-type and disease model mice is heavily influenced by mouse facility. Front. Microbiol. 9:1598
    [Google Scholar]
  86. 86. 
    Tuttle AH, Philip VM, Chesler EJ, Mogil JS. 2018. Comparing phenotypic variation between inbred and outbred mice. Nat. Methods 15:12994–96
    [Google Scholar]
  87. 87. 
    Hildebrand F, Nguyen TLA, Brinkman B, Yunta RG, Cauwe B et al. 2013. Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome Biol. 14:R4
    [Google Scholar]
  88. 88. 
    Andersson L. 2001. Genetic dissection of phenotypic diversity in farm animals. Nat. Rev. Genet. 2:2130–38
    [Google Scholar]
  89. 89. 
    Meuwissen T, Hayes B, Goddard M 2016. Genomic selection: a paradigm shift in animal breeding. Anim. Front. 6:16–14
    [Google Scholar]
  90. 90. 
    de Freitas AS, de David DB, Takagaki BM, Roesch LFW 2020. Microbial patterns in rumen are associated with gain of weight in beef cattle. Antonie van Leeuwenhoek 113:91299–312
    [Google Scholar]
  91. 91. 
    Guan LL, Nkrumah JD, Basarab JA, Moore SS. 2008. Linkage of microbial ecology to phenotype: correlation of rumen microbial ecology to cattle's feed efficiency. FEMS Microbiol. Lett. 288:185–91
    [Google Scholar]
  92. 92. 
    Maltecca C, Bergamaschi M, Tiezzi F. 2020. The interaction between microbiome and pig efficiency: a review. J. Anim. Breed. Genet. 137:14–13
    [Google Scholar]
  93. 93. 
    Xue M-Y, Sun H-Z, Wu X-H, Liu J-X, Guan LL. 2020. Multi-omics reveals that the rumen microbiome and its metabolome together with the host metabolome contribute to individualized dairy cow performance. Microbiome 8:64
    [Google Scholar]
  94. 94. 
    Elokil AA, Magdy M, Melak S, Ishfaq H, Bhuiyan A et al. 2020. Faecal microbiome sequences in relation to the egg-laying performance of hens using amplicon-based metagenomic association analysis. Animal 14:4706–15
    [Google Scholar]
  95. 95. 
    O'Hara E, Neves ALA, Song Y, Guan LL 2020. The role of the gut microbiome in cattle production and health: Driver or passenger?. Annu. Rev. Anim. Biosci. 8:199–220
    [Google Scholar]
  96. 96. 
    Li F, Li C, Chen Y, Liu J, Zhang C et al. 2019. Host genetics influence the rumen microbiota and heritable rumen microbial features associate with feed efficiency in cattle. Microbiome 7:92
    [Google Scholar]
  97. 97. 
    La Reau AJ, Meier-Kolthoff JP, Suen G 2016. Sequence-based analysis of the genus Ruminococcus resolves its phylogeny and reveals strong host association. Microb. Genom. 2:12e000099
    [Google Scholar]
  98. 98. 
    Roehe R, Dewhurst RJ, Duthie C-A, Rooke JA, McKain N et al. 2016. Bovine host genetic variation influences rumen microbial methane production with best selection criterion for low methane emitting and efficiently feed converting hosts based on metagenomic gene abundance. PLOS Genet. 12:2e1005846
    [Google Scholar]
  99. 99. 
    Difford GF, Plichta DR, Løvendahl P, Lassen J, Noel SJ et al. 2018. Host genetics and the rumen microbiome jointly associate with methane emissions in dairy cows. PLOS Genet. 14:10e1007580
    [Google Scholar]
  100. 100. 
    Golder HM, Thomson JM, Denman SE, McSweeney CS, Lean IJ. 2018. Genetic markers are associated with the ruminal microbiome and metabolome in grain and sugar challenged dairy heifers. Front. Genet. 9:62
    [Google Scholar]
  101. 101. 
    Wallace RJ, Sasson G, Garnsworthy PC, Tapio I, Gregson E et al. 2019. A heritable subset of the core rumen microbiome dictates dairy cow productivity and emissions. Sci. Adv. 5:7eaav8391
    [Google Scholar]
  102. 102. 
    Zhang Q, Difford G, Sahana G, Løvendahl P, Lassen J et al. 2020. Bayesian modeling reveals host genetics associated with rumen microbiota jointly influence methane emission in dairy cows. ISME J 14:82019–33
    [Google Scholar]
  103. 103. 
    Fan P, Nelson CD, Driver JD, Elzo MA, Peñagaricano F, Jeong KC 2021. Host genetics exerts lifelong effects upon hindgut microbiota and its association with bovine growth and immunity. ISME J. 15:2306–21
    [Google Scholar]
  104. 104. 
    Fan P, Bian B, Teng L, Nelson CD, Driver J et al. 2020. Host genetic effects upon the early gut microbiota in a bovine model with graduated spectrum of genetic variation. ISME J. 14:302–17
    [Google Scholar]
  105. 105. 
    Sasson G, Ben-Shabat SK, Seroussi E, Doron-Faigenboim A, Shterzer N et al. 2017. Heritable bovine rumen bacteria are phylogenetically related and correlated with the cow's capacity to harvest energy from its feed. mBio 8:4e00703-17
    [Google Scholar]
  106. 106. 
    Estellé J, Mach N, Ramayo-Caldas Y, Levenez F, Lemonnier G et al. 2014. The influence of host's genetics on the gut microbiota composition in pigs and its links with immunity traits. Proceedings of the 10th World Congress of Genetics Applied to Livestock Production, Vancouver, BC, Aug. 17–22 Champaign, IL: Am. Soc. Anim. Sci.
    [Google Scholar]
  107. 107. 
    Camarinha-Silva A, Maushammer M, Wellmann R, Vital M, Preuss S, Bennewitz J. 2017. Host genome influence on gut microbial composition and microbial prediction of complex traits in pigs. Genetics 206:31637–44
    [Google Scholar]
  108. 108. 
    Bergamaschi M, Maltecca C, Schillebeeckx C, McNulty NP, Schwab C et al. 2020. Heritability and genome-wide association of swine gut microbiome features with growth and fatness parameters. Sci. Rep. 10:10134
    [Google Scholar]
  109. 109. 
    Reverter A, Ballester M, Alexandre PA, Mármol-Sánchez E, Dalmau A et al. 2021. A gene co-association network regulating gut microbial communities in a Duroc pig population. Microbiome 9:52
    [Google Scholar]
  110. 110. 
    Clark SA, van der Werf J. 2013. Genomic best linear unbiased prediction (gBLUP) for the estimation of genomic breeding values. Methods Mol. Biol. 1019:321–30
    [Google Scholar]
  111. 111. 
    Jost T, Lacroix C, Braegger CP, Rochat F, Chassard C 2014. Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ. Microbiol. 16:92891–904
    [Google Scholar]
  112. 112. 
    Pannaraj PS, Li F, Cerini C, Bender JM, Yang S et al. 2017. Association between breast milk bacterial communities and establishment and development of the infant gut microbiome. JAMA Pediatr 171:7647–54
    [Google Scholar]
  113. 113. 
    Bian G, Ma S, Zhu Z, Su Y, Zoetendal EG et al. 2016. Age, introduction of solid feed and weaning are more important determinants of gut bacterial succession in piglets than breed and nursing mother as revealed by a reciprocal cross-fostering model. Environ. Microbiol. 18:51566–77
    [Google Scholar]
  114. 114. 
    Zhao L, Wang G, Siegel P, He C, Wang H et al. 2013. Quantitative genetic background of the host influences gut microbiomes in chickens. Sci. Rep. 3:1163
    [Google Scholar]
  115. 115. 
    Meng H, Zhang Y, Zhao L, Zhao W, He C et al. 2014. Body weight selection affects quantitative genetic correlated responses in gut microbiota. PLOS ONE 9:3e89862
    [Google Scholar]
  116. 116. 
    Ji J, Luo CL, Zou X, Lv XH, Xu YB et al. 2019. Association of host genetics with intestinal microbial relevant to body weight in a chicken F2 resource population. Poultry Sci 98:94084–93
    [Google Scholar]
  117. 117. 
    Ji J, Xu Y, Luo C, He Y, Xu X et al. 2020. Effects of the DMRT1 genotype on the body weight and gut microbiota in the broiler chicken. Poultry Sci. 99:84044–51
    [Google Scholar]
  118. 118. 
    Wen C, Yan W, Sun C, Ji C, Zhou Q et al. 2019. The gut microbiota is largely independent of host genetics in regulating fat deposition in chickens. ISME J. 13:61422–36
    [Google Scholar]
  119. 119. 
    Felsenstein J. 1985. Phylogenies and the comparative method. Am. Nat. 125:11–15
    [Google Scholar]
  120. 120. 
    Clayton JB, Vangay P, Huang H, Ward T, Hillmann BM et al. 2016. Captivity humanizes the primate microbiome. PNAS 113:3710376–81
    [Google Scholar]
  121. 121. 
    Reese AT, Chadaideh KS, Diggins CE, Schell LD, Beckel M et al. 2021. Effects of domestication on the gut microbiota parallel those of human industrialization. eLife 10:e60197
    [Google Scholar]
  122. 122. 
    Tung J, Barreiro LB, Burns MB, Grenier J-C, Lynch J et al. 2015. Social networks predict gut microbiome composition in wild baboons. eLife 4:e05224
    [Google Scholar]
  123. 123. 
    Moeller AH, Foerster S, Wilson ML, Pusey AE, Hahn BH, Ochman H. 2016. Social behavior shapes the chimpanzee pan-microbiome. Sci. Adv. 2:1e1500997
    [Google Scholar]
  124. 124. 
    Grieneisen L, Dasari M, Gould TJ, Björk JR, Grenier J-C et al. 2021. Gut microbiome heritability is nearly universal but environmentally contingent. Science 373:6551181–86
    [Google Scholar]
  125. 125. 
    Gevers D, Kugathasan S, Denson LA, Vázquez-Baeza Y, Van Treuren W et al. 2014. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 15:3382–92
    [Google Scholar]
  126. 126. 
    Iwasaki A, Medzhitov R. 2015. Control of adaptive immunity by the innate immune system. Nat. Immunol. 16:4343–53
    [Google Scholar]
  127. 127. 
    Dunne A, O'Neill LAJ 2003. The interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense. Sci. STKE 2003:171re3
    [Google Scholar]
  128. 128. 
    Kawai T, Akira S. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11:5373–84
    [Google Scholar]
  129. 129. 
    Lamas B, Richard ML, Leducq V, Pham H-P, Michel M-L et al. 2016. CARD9 impacts colitis by altering gut microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands. Nat. Med. 22:6598–605
    [Google Scholar]
  130. 130. 
    Crespo-Piazuelo D, Migura-Garcia L, Estellé J, Criado-Mesas L, Revilla M et al. 2019. Association between the pig genome and its gut microbiota composition. Sci. Rep. 9:8791
    [Google Scholar]
  131. 131. 
    Mignon-Grasteau S, Narcy A, Rideau N, Chantry-Darmon C, Boscher M-Y et al. 2015. Impact of selection for digestive efficiency on microbiota composition in the chicken. PLOS ONE 10:8e0135488
    [Google Scholar]
  132. 132. 
    Abbas W, Howard JT, Paz HA, Hales KE, Wells JE et al. 2020. Influence of host genetics in shaping the rumen bacterial community in beef cattle. Sci. Rep. 10:15101
    [Google Scholar]
  133. 133. 
    Parks OB, Pociask DA, Hodzic Z, Kolls JK, Good M. 2016. Interleukin-22 signaling in the regulation of intestinal health and disease. Front. Cell Dev. Biol. 3:85
    [Google Scholar]
  134. 134. 
    Kubiczkova L, Sedlarikova L, Hajek R, Sevcikova S. 2012. TGF-β—an excellent servant but a bad master. J. Transl. Med. 10:183
    [Google Scholar]
  135. 135. 
    McFall-Ngai M. 2007. Care for the community. Nature 445:7124153
    [Google Scholar]
  136. 136. 
    Wieczorek M, Abualrous ET, Sticht J, Álvaro-Benito M, Stolzenberg S et al. 2017. Major histocompatibility complex (MHC) class I and MHC class II proteins: conformational plasticity in antigen presentation. Front. Immunol. 8:292
    [Google Scholar]
  137. 137. 
    Khan AA, Yurkovetskiy L, O'Grady K, Pickard JM, de Pooter R et al. 2019. Polymorphic immune mechanisms regulate commensal repertoire. Cell Rep 29:3541–50.e4
    [Google Scholar]
  138. 138. 
    Kubinak JL, Stephens WZ, Soto R, Petersen C, Chiaro T et al. 2015. MHC variation sculpts individualized microbial communities that control susceptibility to enteric infection. Nat. Commun. 6:8642
    [Google Scholar]
  139. 139. 
    Bryant MP. 1979. Microbial methane production—theoretical aspects. J. Anim. Sci. 48:1193–201
    [Google Scholar]
  140. 140. 
    VanderWeele TJ. 2016. Mediation analysis: a practitioner's guide. Annu. Rev. Public Health 37:17–32
    [Google Scholar]
  141. 141. 
    Tiezzi F, Fix J, Schwab C, Shull C, Maltecca C. 2021. Gut microbiome mediates host genomic effects on phenotypes: a case study with fat deposition in pigs. Comput. Struct. Biotechnol. J. 19:530–44
    [Google Scholar]
  142. 142. 
    Jin X, Zhang Y, Celniker SE, Xia Y, Mao J-H et al. 2021. Gut microbiome partially mediates and coordinates the effects of genetics on anxiety-like behavior in Collaborative Cross mice. Sci. Rep. 11:270
    [Google Scholar]
  143. 143. 
    Wade KH, Hall LJ. 2020. Improving causality in microbiome research: can human genetic epidemiology help?. Wellcome Open Res 4:199
    [Google Scholar]
  144. 144. 
    Sanna S, van Zuydam NR, Mahajan A, Kurilshikov A, Vich Vila A et al. 2019. Causal relationships among the gut microbiome, short-chain fatty acids and metabolic diseases. Nat. Genet. 51:4600–5
    [Google Scholar]
  145. 145. 
    Bourne DG, Morrow KM, Webster NS. 2016. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70:317–40
    [Google Scholar]
  146. 146. 
    Avila-Magaña V, Kamel B, DeSalvo M, Gómez-Campo K, Enríquez S et al. 2021. Elucidating gene expression adaptation of phylogenetically divergent coral holobionts under heat stress. Nat. Commun. 12:15731
    [Google Scholar]
  147. 147. 
    Webster NS, Negri AP, Botté ES, Laffy PW, Flores F et al. 2016. Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Sci. Rep. 6:119324
    [Google Scholar]
  148. 148. 
    Glasl B, Smith CE, Bourne DG, Webster NS. 2019. Disentangling the effect of host-genotype and environment on the microbiome of the coral Acropora tenuis. PeerJ 7:e6377
    [Google Scholar]
  149. 149. 
    Kumar S, Stecher G, Suleski M, Hedges SB. 2017. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34:71812–19
    [Google Scholar]
  150. 150. 
    Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. 2018. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36:10996–1004
    [Google Scholar]
  151. 151. 
    Asnicar F, Weingart G, Tickle TL, Huttenhower C, Segata N. 2015. Compact graphical representation of phylogenetic data and metadata with GraPhlAn. PeerJ 3:e1029
    [Google Scholar]
  152. 152. 
    Org E, Parks BW, Joo JWJ, Emert B, Schwartzman W et al. 2015. Genetic and environmental control of host-gut microbiota interactions. Genome Res 25:101558–69
    [Google Scholar]
  153. 153. 
    McKnite AM, Perez-Munoz ME, Lu L, Williams EG, Brewer S et al. 2012. Murine gut microbiota is defined by host genetics and modulates variation of metabolic traits. PLOS ONE 7:6e39191
    [Google Scholar]
  154. 154. 
    Snijders AM, Langley SA, Kim Y-M, Brislawn CJ, Noecker C et al. 2016. Influence of early life exposure, host genetics and diet on the mouse gut microbiome and metabolome. Nat. Microbiol. 2:16221
    [Google Scholar]
  155. 155. 
    Ramayo-Caldas Y, Prenafeta-Boldú F, Zingaretti LM, Gonzalez-Rodriguez O, Dalmau A et al. 2020. Gut eukaryotic communities in pigs: diversity, composition and host genetics contribution. Anim. Microbiome 2:18
    [Google Scholar]
  156. 156. 
    Suzuki TA, Phifer-Rixey M, Mack KL, Sheehan MJ, Lin D et al. 2019. Host genetic determinants of the gut microbiota of wild mice. Mol. Ecol. 28:133197–207
    [Google Scholar]
  157. 157. 
    Griffiths SM, Antwis RE, Lenzi L, Lucaci A, Behringer DC et al. 2019. Host genetics and geography influence microbiome composition in the sponge Ircinia campana. J. Anim. Ecol. 88:111684–95
    [Google Scholar]
  158. 158. 
    Smith CC, Snowberg LK, Caporaso JG, Knight R, Bolnick DI. 2015. Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota. ISME J 9:2515–26
    [Google Scholar]
  159. 159. 
    Steury RA, Currey MC, Cresko WA, Bohannan BJM 2019. Population genetic divergence and environment influence the gut microbiome in Oregon threespine stickleback. Genes 10:7484
    [Google Scholar]
/content/journals/10.1146/annurev-animal-020420-032054
Loading
/content/journals/10.1146/annurev-animal-020420-032054
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error