Ecophylogenetics Clarifies the Evolutionary Association between Mammals and Their Gut Microbiota
Open accessAbstract
Our understanding of mammalian evolution has become microbiome-aware. While emerging research links mammalian biodiversity and the gut microbiome, we lack insight into which microbes potentially impact mammalian evolution. Microbes common to diverse mammalian species may be strong candidates, as their absence in the gut may affect how the microbiome functionally contributes to mammalian physiology to adversely affect fitness. Identifying such conserved gut microbes is thus important to ultimately assessing the microbiome’s potential role in mammalian evolution. To advance their discovery, we developed an approach that identifies ancestrally related groups of microbes that distribute across mammals in a way that indicates their collective conservation. These conserved clades are presumed to have evolved a trait in their ancestor that matters to their distribution across mammals and which has been retained among clade members. We found not only that such clades do exist among mammals but also that they appear to be subject to natural selection and characterize human evolution.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Over time the microbiota has co-evolved with host organisms, becoming mutually co-dependent for survival.
“Over time the microbiota has co-evolved with host organisms, becoming mutually co-dependent for survival (Bordenstein and Theis, 2015;Gaulke et al., 2018).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Gaulke et al., 2018
The Results (page unavailable) report that some gut bacterial clades show evolutionary patterns linked to their mammalian hosts. But the Discussion (page unavailable) says coevolution remains an unclear explanation for that association and describes host dependence on gut microbiota as a hypothesis. It does not establish that hosts and microbiota have become mutually dependent for survival. (LLM, conf=0.87)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Human Genetics Shape the Gut Microbiome
Goodrich, J. K., Waters, J. L., Poole, A. C., Sutter, J. L., Koren, O., Blekhman, R., Beaumont, M., Van Treuren, W., Knight, R., Bell, J. T., et al. (2014) · Cell · doi:10.1016/j.cell.2014.09.053 · Cited by 3,164 · see citing works
Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans
Muegge, B. D., Kuczynski, J., Knights, D., Clemente, J. C., González, A., Fontana, L., Henrissat, B., Knight, R., & Gordon, J. I. (2011) · Science · doi:10.1126/science.1198719 · Cited by 1,988 · see citing works
Nayfach, S., Rodriguez-Mueller, B., Garud, N., & Pollard, K. S. (2016) · Genome Research · doi:10.1101/gr.201863.115 · Cited by 470 · see citing works
The convergence of carbohydrate active gene repertoires in human gut microbes
Lozupone, C. A., Hamady, M., Cantarel, B. L., Coutinho, P. M., Henrissat, B., Gordon, J. I., & Knight, R. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807339105 · Cited by 139 · see citing works
Flagged first, then by citations
Research works printed but not linked: 57
- [1]Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI 2008 Evolution of mammals and their gut microbes. Science 320: 1647– 1651. doi: 10.1126/science.1155725. 18497261 PMC2649005 · DOI · Paper page
- [2]Moeller AH, Degnan PH, Pusey AE, Wilson ML, Hahn BH, Ochman H 2012 Chimpanzees and humans harbour compositionally similar gut enterotypes. Nat Commun 3: 1179. doi: 10.1038/ncomms2159. 23149725 PMC3520023 · DOI
- [3]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. doi: 10.1371/journal.pbio.2000225. 27861590 PMC5115861 · DOI
- [4]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. doi: 10.1038/ncomms14319. 28230052 PMC5331214 · DOI
- [5]Sharpton TJ 2018 Role of the gut microbiome in vertebrate evolution. mSystems 3: e00174-17. doi: 10.1128/mSystems.00174-17. 29629413 PMC5881020 · DOI
- [6]Bäckhed F 2012 Host responses to the human microbiome. Nutr Rev 70: S14– S17. doi: 10.1111/j.1753-4887.2012.00496.x. 22861802 · DOI
- [7]Claus SP, Guillou H, Ellero-Simatos S 2016 The gut microbiota: a major player in the toxicity of environmental pollutants? NPJ Biofilms Microbiomes 2: 16003. doi: 10.1038/npjbiofilms.2016.3. 28721242 PMC5515271 · DOI · Paper page
- [8]Kohl KD, Weiss RB, Cox J, Dale C, Dearing MD 2014 Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol Lett 17: 1238– 1246. doi: 10.1111/ele.12329. 25040855 · DOI
- [9]Hooper LV, Littman DR, Macpherson AJ 2012 Interactions between the microbiota and the immune system. Science 336: 1268– 1273. doi: 10.1126/science.1223490. 22674334 PMC4420145 · DOI · Paper page
- [10]Cho I, Blaser MJ 2012 The human microbiome: at the interface of health and disease. Nat Rev Genet 13: 260– 270. doi: 10.1038/nrg3182. 22411464 PMC3418802 · DOI · Paper page
- [11]Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L, Henrissat B, Knight R, Gordon JI 2011 Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332: 970– 974. 21596990 PMC3303602
- [12]Clayton JB, Vangay P, Huang H, Ward T, Hillmann BM, Al-Ghalith GA, Travis DA, Long HT, Tuan BV, Minh VV, Cabana F, Nadler T, Toddes B, Murphy T, Glander KE, Johnson TJ, Knights D 2016 Captivity humanizes the primate microbiome. Proc Natl Acad Sci U S A 113: 10376– 10381. doi: 10.1073/pnas.1521835113. 27573830 PMC5027417 · DOI
- [13]O’Dwyer JP, Kembel SW, Green JL 2012 Phylogenetic diversity theory sheds light on the structure of microbial communities. PLoS Comput Biol 8: e1002832. doi: 10.1371/journal.pcbi.1002832. 23284280 PMC3527210 · DOI
- [14]Moeller AH, Caro-Quintero A, Mjungu D, Georgiev AV, Lonsdorf EV, Muller MN, Pusey AE, Peeters M, Hahn BH, Ochman H 2016 Cospeciation of gut microbiota with hominids. Science 353: 380– 382. doi: 10.1126/science.aaf3951. 27463672 PMC4995445 · DOI
- [16]Beaumont M, Goodrich JK, Jackson MA, Yet I, Davenport ER, Vieira-Silva S, Debelius J, Pallister T, Mangino M, Raes J, Knight R, Clark AG, Ley RE, Spector TD, Bell JT 2016 Heritable components of the human fecal microbiome are associated with visceral fat. Genome Biol 17: 189. doi: 10.1186/s13059-016-1052-7. 27666579 PMC5036307 · DOI
- [17]Blekhman R, Goodrich JK, Huang K, Sun Q, Bukowski R, Bell JT, Spector TD, Keinan A, Ley RE, Gevers D, Clark AG 2015 Host genetic variation impacts microbiome composition across human body sites. Genome Biol 16: 191. doi: 10.1186/s13059-015-0759-1. 26374288 PMC4570153 · DOI · Paper page
- [18]Shade A, Handelsman J 2012 Beyond the Venn diagram: the hunt for a core microbiome. Environ Microbiol 14: 4– 12. doi: 10.1111/j.1462-2920.2011.02585.x. 22004523 · DOI
- [19]Martiny AC, Treseder K, Pusch G 2013 Phylogenetic conservatism of functional traits in microorganisms. ISME J 7: 830– 838. doi: 10.1038/ismej.2012.160. 23235290 PMC3603392 · DOI
- [20]Philippot L, Andersson SGE, Battin TJ, Prosser JI, Schimel JP, Whitman WB, Hallin S 2010 The ecological coherence of high bacterial taxonomic ranks. Nat Rev Microbiol 8: 523– 529. doi: 10.1038/nrmicro2367. 20531276 · DOI
- [21]Barberán A, Caceres Velazquez H, Jones S, Fierer N 2017 Hiding in plain sight: mining bacterial species records for phenotypic trait information. mSphere 2: e00237-17. doi: 10.1128/mSphere.00237-17. 28776041 PMC5541158 · DOI
- [22]Mouquet N, Devictor V, Meynard CN, Munoz F, Bersier LF, Chave J, Couteron P, Dalecky A, Fontaine C, Gravel D, Hardy OJ, Jabot F, Lavergne S, Leibold M, Mouillot D, Münkemüller T, Pavoine S, Prinzing A, Rodrigues ASL, Rohr RP, Thébault E, Thuiller W 2012 Ecophylogenetics: advances and perspectives. Biol Rev Camb Philos Soc 87: 769– 785. doi: 10.1111/j.1469-185X.2012.00224.x. 22432924 · DOI
- [24]Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA 2008 Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6: 121– 131. doi: 10.1038/nrmicro1817. 18180751 · DOI
- [25]Heinken A, Khan MT, Paglia G, Rodionov DA, Harmsen HJM, Thiele I 2014 Functional metabolic map of Faecalibacterium prausnitzii, a beneficial human gut microbe. J Bacteriol 196: 3289– 3302. doi: 10.1128/JB.01780-14. 25002542 PMC4135701 · DOI
- [26]Miquel S, Martín R, Rossi O, Bermúdez-Humarán LG, Chatel JM, Sokol H, Thomas M, Wells JM, Langella P 2013 Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol 16: 255– 261. doi: 10.1016/j.mib.2013.06.003. 23831042 · DOI
- [27]Goodrich JK, Davenport ER, Beaumont M, Jackson MA, Knight R, Ober C, Spector TD, Bell JT, Clark AG, Ley RE 2016 Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe 19: 731– 743. doi: 10.1016/j.chom.2016.04.017. 27173935 PMC4915943 · DOI · Paper page
- [28]Horner-Devine MC, Bohannan BJM 2006 Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87: S100– S108. doi: 10.1890/0012-9658(2006)87[100:PCAOIB]2.0.CO;2. 16922306 · DOI
- [29]Legendre P, Desdevises Y, Bazin E 2002 A statistical test for host-parasite coevolution. Syst Biol 51: 217– 234. doi: 10.1080/10635150252899734. 12028729 · DOI
- [30]Solden LM, Hoyt DW, Collins WB, Plank JE, Daly RA, Hildebrand E, Beavers TJ, Wolfe R, Nicora CD, Purvine SO, Carstensen M, Lipton MS, Spalinger DE, Firkins JL, Wolfe BA, Wrighton KC 2017 New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11. ISME J 11: 691– 703. doi: 10.1038/ismej.2016.150. 27959345 PMC5322302 · DOI
- [31]Stewart CS, Duncan SH, Cave DR 2004 Oxalobacter formigenes and its role in oxalate metabolism in the human gut. FEMS Microbiol Lett 230: 1– 7. doi: 10.1016/S0378-1097(03)00864-4. 14734158 · DOI
- [32]Schnorr SL, Sankaranarayanan K, Lewis CM, Warinner C 2016 Insights into human evolution from ancient and contemporary microbiome studies. Curr Opin Genet Dev 41: 14– 26. doi: 10.1016/j.gde.2016.07.003. 27507098 PMC5534492 · DOI
- [33]Moeller AH, Li Y, Mpoudi Ngole E, Ahuka-Mundeke S, Lonsdorf EV, Pusey AE, Peeters M, Hahn BH, Ochman H 2014 Rapid changes in the gut microbiome during human evolution. Proc Natl Acad Sci U S A 111: 16431– 16435. doi: 10.1073/pnas.1419136111. 25368157 PMC4246287 · DOI
- [34]Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI 2012 Human gut microbiome viewed across age and geography. Nature 486: 222– 227. doi: 10.1038/nature11053. 22699611 PMC3376388 · DOI · Paper page
- [35]Meehan CJ, Beiko RG 2014 A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol 6: 703– 713. doi: 10.1093/gbe/evu050. 24625961 PMC3971600 · DOI
- [36]Clavel T, Lepage P, Charrier C 2014 The family Coriobacteriaceae, p 201– 238. In The prokaryotes. Springer, Berlin, Germany.
- [37]David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ 2014 Diet rapidly and reproducibly alters the human gut microbiome. Nature 505: 559– 563. doi: 10.1038/nature12820. 24336217 PMC3957428 · DOI · Paper page
- [38]Ruiz-Calderon JF, Cavallin H, Song SJ, Novoselac A, Pericchi LR, Hernandez JN, Rios R, Branch OH, Pereira H, Paulino LC, Blaser MJ, Knight R, Dominguez-Bello MG 2016 Walls talk: microbial biogeography of homes spanning urbanization. Sci Adv 2: e1501061. doi: 10.1126/sciadv.1501061. 26933683 PMC4758746 · DOI
- [39]Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R 2011 UniFrac: an effective distance metric for microbial community comparison. ISME J 5: 169– 172. doi: 10.1038/ismej.2010.133. 20827291 PMC3105689 · DOI · Paper page
- [40]Matsen FA, Evans SN 2013 Edge principal components and squash clustering: using the special structure of phylogenetic placement data for sample comparison. PLoS One 8: e56859. doi: 10.1371/journal.pone.0056859. 23505415 PMC3594297 · DOI
- [41]Amend AS, Martiny AC, Allison SD, Berlemont R, Goulden ML, Lu Y, Treseder KK, Weihe C, Martiny JBH 2016 Microbial response to simulated global change is phylogenetically conserved and linked with functional potential. ISME J 10: 109– 118. doi: 10.1038/ismej.2015.96. 26046258 PMC4681869 · DOI
- [42]Washburne AD, Silverman JD, Leff JW, Bennett DJ, Darcy JL, Mukherjee S, Fierer N, David LA 2017 Phylogenetic factorization of compositional data yields lineage-level associations in microbiome datasets. PeerJ 5: e2969. doi: 10.7717/peerj.2969. 28289558 PMC5345826 · DOI
- [43]Vergin KL, Beszteri B, Monier A, Thrash JC, Temperton B, Treusch AH, Kilpert F, Worden AZ, Giovannoni SJ 2013 High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences. ISME J 7: 1322– 1332. doi: 10.1038/ismej.2013.32. 23466704 PMC3695298 · DOI
- [44]Martin AP 2002 Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl Environ Microbiol 68: 3673– 3682. doi: 10.1128/AEM.68.8.3673-3682.2002. 12147459 PMC124012 · DOI
- [45]Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer KH, Whitman WB, Euzéby J, Amann R, Rosselló-Móra R 2014 Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12: 635– 645. doi: 10.1038/nrmicro3330. 25118885 · DOI
- [47]Amato KR 2013 Co-evolution in context: the importance of studying gut microbiomes in wild animals. De Gruyter Online 1. doi: 10.2478/micsm-2013-0002. · DOI
- [48]Ronquist F 1997 Phylogenetic approaches in coevolution and biogeography. Zool Scr 26: 313– 322. doi: 10.1111/j.1463-6409.1997.tb00421.x. · DOI
- [49]Ochman H, Elwyn S, Moran NA 1999 Calibrating bacterial evolution. Proc Natl Acad Sci U S A 96: 12638– 12643. doi: 10.1073/pnas.96.22.12638. 10535975 PMC23026 · DOI
- [50]Kuo CH, Ochman H 2009 Inferring clocks when lacking rocks: the variable rates of molecular evolution in bacteria. Biol Direct 4: 35. doi: 10.1186/1745-6150-4-35. 19788732 PMC2760517 · DOI
- [51]Riesenfeld SJ, Pollard KS 2013 Beyond classification: gene-family phylogenies from shotgun metagenomic reads enable accurate community analysis. BMC Genomics 14: 419. doi: 10.1186/1471-2164-14-419. 23799973 PMC3701559 · DOI
- [53]Duchêne S, Holt KE, Weill FX, Le Hello S, Hawkey J, Edwards DJ, Fourment M, Holmes EC 2016 Genome-scale rates of evolutionary change in bacteria. Microb Genomics 2: e000094. doi: 10.1099/mgen.0.000094. PMC5320706 28348834 · DOI
- [54]Martiny JBH, Jones SE, Lennon JT, Martiny AC 2015 Microbiomes in light of traits: a phylogenetic perspective. Science 350: aac9323. doi: 10.1126/science.aac9323. 26542581 · DOI · Paper page
- [55]Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R 2010 QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335– 336. doi: 10.1038/nmeth.f.303. 20383131 PMC3156573 · DOI · Paper page
- [56]Edgar RC 2010 Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460– 2461. doi: 10.1093/bioinformatics/btq461. 20709691 · DOI
- [57]Sharpton TJ, Riesenfeld SJ, Kembel SW, Ladau J, O’Dwyer JP, Green JL, Eisen JA, Pollard KS 2011 PhylOTU: a high-throughput procedure quantifies microbial community diversity and resolves novel taxa from metagenomic data. PLoS Comput Biol 7: e1001061. doi: 10.1371/journal.pcbi.1001061. 21283775 PMC3024254 · DOI
- [58]O’Dwyer JP, Kembel SW, Sharpton TJ 2015 Backbones of evolutionary history test biodiversity theory for microbes. Proc Natl Acad Sci U S A 112: 8356– 8361. doi: 10.1073/pnas.1419341112. 26106159 PMC4500224 · DOI
- [59]Nawrocki EP, Eddy SR 2013 Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29: 2933– 2935. doi: 10.1093/bioinformatics/btt509. 24008419 PMC3810854 · DOI
- [60]Price MN, Dehal PS, Arkin AP 2010 FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS One 5: e9490. doi: 10.1371/journal.pone.0009490. 20224823 PMC2835736 · DOI · Paper page
- [61]Arnold C, Matthews LJ, Nunn CL 2010 The 10kTrees website: a new online resource for primate phylogeny. Evol Anthropol 19: 114– 118. doi: 10.1002/evan.20251. · DOI
Cited by
Sorted by citations
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
You’ve got male: Sex and the microbiota-gut-brain axis across the lifespan
Jaggar, M., Rea, K., Spichak, S., Dinan, T. G., & Cryan, J. F. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100815 · Cited by 200 · see citing works
- Authors
- Gaulke, C. A., Arnold, H. K., Humphreys, I. R., Kembel, S. W., O’Dwyer, J. P., & Sharpton, T. J.
- Affiliations
- Oregon State University (US)
- Université du Québec à Montréal (CA)
- University of Illinois Urbana-Champaign (US)
- Corresponding author
- Sharpton, Thomas J.
- ORCID
- Venue
- mBio
- Publisher
- American Society for Microbiology
- Published
- 2018-11-07
- Volume
- 9
- Issue
- 5
- ISSN
- 2150-7511 (ISSN-L)
- 2161-2129
- PMC
- PMC6134092
- OpenAlex
- W2949791294
- Cited by
- 117
- References
- 4
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 9 · 2023: 36 · 2022: 18 · 2021: 16 · 2020: 12 · 2019: 11 · 2018: 4
- FWCI
- 3.82
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- mBio (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Science Foundation (1557192)
- Oregon State University (Institutional Funds)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- mammalian evolution, host-microbe coevolution, natural selection, human evolution, microbiome
- MeSH terms
- Gastrointestinal Microbiome, Host Microbial Interactions, Algorithms, Animals, Bacteria, Biological Evolution, Mammals, Phylogeny, RNA, Ribosomal, 16S, Computational Biology, Biodiversity
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review