in

The microbiome extends host evolutionary potential

  • 1.

    Blaser, M. J. & Falkow, S. What are the consequences of the disappearing human microbiota? Nat. Rev. Microbiol. 7, 887–894 (2009).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 2.

    Friesen, M. L. et al. Microbially mediated plant functional traits. Annu. Rev. Ecol. Evol. Syst. 42, 23–46 (2011).

    Article 

    Google Scholar 

  • 3.

    McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. 110, 3229–3236 (2013).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 4.

    Douglas, A. E. Symbiosis as a general principle in eukaryotic evolution. Cold Spring Harb. Perspect. Biol. 6, a016113 (2014).

  • 5.

    Stappenbeck, T. S. & Virgin, H. W. Accounting for reciprocal host-microbiome interactions in experimental science. Nature 534, 191–199 (2016).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 6.

    Moran, N. A. & Sloan, D. B. The hologenome concept: helpful or hollow? PLoS Biol. 13, e1002311 (2015).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 7.

    Douglas, A. E. & Werren, J. H. Holes in the hologenome: why host-microbe symbioses are not holobionts. MBio 7, e02099 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 8.

    Koskella, B., Hall, L. J. & Metcalf, C. J. E. The microbiome beyond the horizon of ecological and evolutionary theory. Nat. Ecol. Evol. 1, 1606–1615 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 9.

    Morimoto, J. & Baltrus, D. A. The extended genotype: to what extent? A comment on Carthey et al. Trends Ecol. Evol. 34, 186–187 (2019).

  • 10.

    Scheuring, I. & Yu, D. W. How to assemble a beneficial microbiome in three easy steps. Ecol. Lett. 15, 1300–1307 (2012).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 11.

    Dawkins, R. The Extended Phenotype: The Long Reach of the Gene. (Oxford University Press, USA, 1982).

  • 12.

    Whitham, T. G. et al. A framework for community and ecosystem genetics: from genes to ecosystems. Nat. Rev. Genet. 7, 510–523 (2006).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 13.

    Mueller, U. G. & Sachs, J. L. Engineering Microbiomes to Improve Plant and Animal Health. Trends Microbiol 23, 606–617 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 14.

    Zilber-Rosenberg, I. & Rosenberg, E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32, 723–735 (2008).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 15.

    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 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 16.

    Alberdi, A., Aizpurua, O., Bohmann, K., Zepeda-Mendoza, M. L. & Gilbert, M. T. P. Do vertebrate gut metagenomes confer rapid ecological adaptation? Trends Ecol. Evol. 31, 689–699 (2016).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 17.

    Shapira, M. Gut Microbiotas and host evolution: scaling up symbiosis. Trends Ecol. Evol. 31, 539–549 (2016).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 18.

    Carrier, T. J. & Reitzel, A. M. The hologenome across environments and the implications of a host-associated microbial repertoire. Front. Microbiol. 8, 802 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 19.

    Hurst, G. D. D. Extended genomes: symbiosis and evolution. Interface Focus 7, 20170001 (2017).

  • 20.

    Sudakaran, S., Kost, C. & Kaltenpoth, M. Symbiont acquisition and replacement as a source of ecological innovation. Trends Microbiol 25, 375–390 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 21.

    Carthey, A. J. R., Gillings, M. R. & Blumstein, D. T. The extended genotype: microbially mediated olfactory communication. Trends Ecol. Evol. 33, 885–894 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 22.

    Rosenberg, E. & Zilber-Rosenberg, I. The hologenome concept of evolution after 10 years. Microbiome 6, 78 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 23.

    Futuyma, D. J. & Moreno, G. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19, 207–233 (1988).

    Article 

    Google Scholar 

  • 24.

    Piersma, T. & Drent, J. Phenotypic flexibility and the evolution of organismal design. Trends Ecol. Evol. 18, 228–233 (2003).

    Article 

    Google Scholar 

  • 25.

    Lande, R. Natural selection and random genetic drift in phenotypic. Evolution. Evolution 30, 314–334 (1976).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 26.

    West-Eberhard, M. J. Phenotypic plasticity and the origins of diversity. Annu. Rev. Ecol. Syst. 20, 249–278 (1989).

    Article 

    Google Scholar 

  • 27.

    Ghalambor, C. K., McKay, J. K., Carroll, S. P. & Reznick, D. N. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21, 394–407 (2007).

    Article 

    Google Scholar 

  • 28.

    Bolnick, D. I. et al. Why intraspecific trait variation matters in community ecology. Trends Ecol. Evol. 26, 183–192 (2011).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 29.

    Metcalf, C. J. E. & Koskella, B. Protective microbiomes can limit the evolution of host pathogen defense. Evol. Lett. 3, 534–543 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 30.

    Rosenberg, E., Koren, O., Reshef, L., Efrony, R. & Zilber-Rosenberg, I. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5, 355–362 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 31.

    Theis, K. R. et al. Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1, e00028 (2016).

  • 32.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 33.

    Salem, H., Florez, L., Gerardo, N. & Kaltenpoth, M. An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects. Proc. R. Soc. Lond. B. 282, 20142957 (2015).

  • 34.

    Vacher, C. et al. The phyllosphere: microbial jungle at the plant–climate interface. Annu. Rev. Ecol. Evol. Syst. 47, 1–24 (2016).

    Article 

    Google Scholar 

  • 35.

    Rothschild, D. et al. Environment dominates over host genetics in shaping human gut microbiota. Nature 555, 210–215 (2018).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 36.

    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: Biol. Sci. 286, 20190431 (2019).

    Article 

    Google Scholar 

  • 37.

    McKenney, E. A., Koelle, K., Dunn, R. R. & Yoder, A. D. The ecosystem services of animal microbiomes. Mol. Ecol. 27, 2164–2172 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 38.

    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 
    Article 
    PubMed Central 

    Google Scholar 

  • 39.

    Uhr, G. T., Dohnalová, L. & Thaiss, C. A. The dimension of time in host-microbiome interactions. mSystems 4, e00216–18 (2019).

  • 40.

    van Vliet, S. & Doebeli, M. The role of multilevel selection in host microbiome evolution. Proc. Natl Acad. Sci. U.S.A. 116, 20591–20597 (2019).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 41.

    Benson, A. K. The gut microbiome—an emerging complex trait. Nat. Genet. 48, 1301 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 42.

    van Opstal, E. J. & Bordenstein, S. R. Rethinking heritability of the microbiome. Science 349, 1172–1173 (2015).

    ADS 
    PubMed 
    Article 

    Google Scholar 

  • 43.

    Beilsmith, K. et al. Genome-wide association studies on the phyllosphere microbiome: embracing complexity in host–microbe interactions. Plant J. 97, 164–181 (2019).

  • 44.

    Goodrich, J. K. et al. Human genetics shape the gut microbiome. Cell 159, 789–799 (2014).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 45.

    Goodrich, J. K. et al. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe 19, 731–743 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 46.

    Early, A. M., Shanmugarajah, N., Buchon, N. & Clark, A. G. Drosophila genotype influences commensal bacterial levels. PLoS ONE 12, e0170332 (2017).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 47.

    Walters, W. A. et al. Large-scale replicated field study of maize rhizosphere identifies heritable microbes. Proc. Natl Acad. Sci. U. S. A. 115, 7368–7373 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 48.

    Camarinha-Silva, A. et al. Host genome influence on gut microbial composition and microbial prediction of complex traits in pigs. Genetics 206, 1637–1644 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 49.

    Difford, G. F. et al. Host genetics and the rumen microbiome jointly associate with methane emissions in dairy cows. PLoS Genet 14, e1007580 (2018).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 50.

    Koga, R., Meng, X.-Y., Tsuchida, T. & Fukatsu, T. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte–embryo interface. Proc. Natl Acad. Sci. U.S.A. 109, E1230–E1237 (2012).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 51.

    Nyholm, S. V. & McFall-Ngai, M. The winnowing: establishing the squid–vibrio symbiosis. Nat. Rev. Microbiol. 2, 632–642 (2004).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 52.

    Kaltenpoth, M., Göttler, W., Herzner, G. & Strohm, E. Symbiotic bacteria protect wasp larvae from fungal infestation. Curr. Biol. 15, 475–479 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 53.

    Clark, R. I. et al. Distinct shifts in microbiota composition during Drosophila aging impair intestinal function and drive mortality. Cell Rep. 12, 1656–1667 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 54.

    Franzosa, E. A. et al. Identifying personal microbiomes using metagenomic codes. Proc. Natl Acad. Sci. U.S.A. 112, E2930–E2938 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 55.

    Lokmer, A. et al. Spatial and temporal dynamics of pacific oyster hemolymph microbiota across multiple scales. Front. Microbiol. 7, 1367 (2016).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 56.

    Elena, S. F. & Lenski, R. E. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4, 457–469 (2003).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 57.

    Lapierre, P. & Gogarten, J. P. Estimating the size of the bacterial pan-genome. Trends Genet 25, 107–110 (2009).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 58.

    Koonin, E. V. & Wolf, Y. I. Evolution of microbes and viruses: a paradigm shift in evolutionary biology? Front. Cell. Infect. Microbiol. 2, 119 (2012).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 59.

    Ferreiro, A., Crook, N., Gasparrini, A. J. & Dantas, G. Multiscale evolutionary dynamics of host-associated microbiomes. Cell 172, 1216–1227 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 60.

    Kikuchi, Y., Hosokawa, T. & Fukatsu, T. Specific developmental window for establishment of an insect-microbe gut symbiosis. Appl. Environ. Microbiol. 77, 4075–4081 (2011).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 61.

    Kikuchi, Y. et al. Symbiont-mediated insecticide resistance. Proc. Natl Acad. Sci. U.S.A. 109, 8618–8622 (2012).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 62.

    Itoh, H. et al. Infection dynamics of insecticide-degrading symbionts from soil to insects in response to insecticide spraying. ISME J. 12, 909–920 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 63.

    Kohl, K. D. & Dearing, M. D. The woodrat gut microbiota as an experimental system for understanding microbial metabolism of dietary toxins. Front. Microbiol. 7, 1165 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 64.

    Kohl, K. D., Weiss, R. B., Cox, J., Dale, C. & Dearing, M. D. Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol. Lett. 17, 1238–1246 (2014).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 65.

    Miller, A. W., Kohl, K. D. & Dearing, M. D. The gastrointestinal tract of the white-throated Woodrat (Neotoma albigula) harbors distinct consortia of oxalate-degrading bacteria. Appl. Environ. Microbiol. 80, 1595–1601 (2014).

    ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 66.

    Miller, A. W., Oakeson, K. F., Dale, C. & Dearing, M. D. Effect of dietary oxalate on the gut microbiota of the mammalian herbivore Neotoma albigula. Appl. Environ. Microbiol. 82, 2669–2675 (2016).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 67.

    Kohl, K. D., Stengel, A. & Dearing, M. D. Inoculation of tannin-degrading bacteria into novel hosts increases performance on tannin-rich diets. Environ. Microbiol. 18, 1720–1729 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 68.

    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 

  • 69.

    Redman, R. S., Sheehan, K. B., Stout, R. G., Rodriguez, R. J. & Henson, J. M. Thermotolerance generated by plant/fungal symbiosis. Science 298, 1581 (2002).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 70.

    Rodriguez, R. J. et al. Stress tolerance in plants via habitat-adapted symbiosis. ISME J. 2, 404–416 (2008).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 71.

    Miller, E. T., Svanbäck, R. & Bohannan, B. J. M. Microbiomes as Metacommunities: Understanding Host-Associated Microbes through Metacommunity Ecology. Trends Ecol. Evol. 33, 926–935 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 72.

    Newell, P. D. & Douglas, A. E. Interspecies interactions determine the impact of the gut microbiota on nutrient allocation in Drosophila melanogaster. Appl. Environ. Microbiol. 80, 788–796 (2014).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 73.

    Keebaugh, E. S., Yamada, R., Obadia, B., Ludington, W. B. & Ja, W. W. Microbial quantity impacts drosophila nutrition, development, and lifespan. Science 4, 247–259 (2018).

    CAS 

    Google Scholar 

  • 74.

    Gould, A. L. et al. Microbiome interactions shape host fitness. Proc. Natl Acad. Sci. U.S.A. 115, E11951–E11960 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 75.

    Mushegian, A. A., Walser, J.-C., Sullam, K. E. & Ebert, D. The microbiota of diapause: How host-microbe associations are formed after dormancy in an aquatic crustacean. J. Anim. Ecol. 87, 400–413 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 76.

    Panke-Buisse, K., Poole, A. C., Goodrich, J. K., Ley, R. E. & Kao-Kniffin, J. Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J. 9, 980–989 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 77.

    Rolig, A. S., Parthasarathy, R., Burns, A. R., Bohannan, B. J. M. & Guillemin, K. Individual members of the microbiota disproportionately modulate host innate immune responses. Cell Host Microbe 18, 613–620 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 78.

    Webster, N. S. & Reusch, T. B. H. Microbial contributions to the persistence of coral reefs. ISME J. 11, 2167–2174 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 79.

    Bourne, D. G., Morrow, K. M. & Webster, N. S. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70, 317–340 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 80.

    Ainsworth, T. D., Thurber, R. V. & Gates, R. D. The future of coral reefs: a microbial perspective. Trends Ecol. Evol. 25, 233–240 (2010).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 81.

    Sommer, F. et al. The gut microbiota modulates energy metabolism in the hibernating brown bear Ursus arctos. Cell Rep. 14, 1655–1661 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 82.

    Metcalf, C. J. E., Henry, L. P., Rebolleda-Gómez, M. & Koskella, B. Why evolve reliance on the microbiome for timing of ontogeny? MBio 10, e01496-19 (2019).

  • 83.

    Gilbert, S. F., Bosch, T. C. G. & Ledón-Rettig, C. Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents. Nat. Rev. Genet. 16, 611–622 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 84.

    Philippi, T. & Seger, J. Hedging one’s evolutionary bets, revisited. Trends Ecol. Evol. 4, 41–44 (1989).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 85.

    Storelli, G. et al. Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab. 14, 403–414 (2011).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 86.

    Bruijning, M., Henry, L. P., Forsberg, S. K. G., Metcalf, C. J. E. & Ayroles, J. F. When the microbiome defines the host phenotype: selection on vertical transmission in varying environments. bioRxiv 2020.09.02.280040 (2020) https://doi.org/10.1101/2020.09.02.280040.

  • 87.

    Boone, C. K. et al. Bacteria associated with a tree-killing insect reduce concentrations of plant defense compounds. J. Chem. Ecol. 39, 1003–1006 (2013).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 88.

    Berasategui, A. et al. Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness. Mol. Ecol. 26, 4099–4110 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 89.

    Ceja-Navarro, J. A. et al. Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat. Commun. 6, 7618 (2015).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 90.

    Berasategui, A. et al. The gut microbiota of the pine weevil is similar across Europe and resembles that of other conifer-feeding beetles. Mol. Ecol. 25, 4014–4031 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 91.

    Sachs, J. L., Skophammer, R. G. & Regus, J. U. Evolutionary transitions in bacterial symbiosis. Proc. Natl Acad. Sci. U.S.A 108, 10800–10807 (2011).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 92.

    Ohbayashi, T. et al. Insect’s intestinal organ for symbiont sorting. Proc. Natl Acad. Sci. U.S.A 112, E5179–E5188 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 93.

    Itoh, H. et al. Host–symbiont specificity determined by microbe–microbe competition in an insect gut. Proc. Natl Acad. Sci. U.S.A. 116, 22673–22682 (2019).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 94.

    Bennett, G. M. & Moran, N. A. Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. Proc. Natl Acad. Sci. 112, 10169–10176 (2015).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 95.

    Knight, R. et al. Best practices for analysing microbiomes. Nat. Rev. Microbiol. 16, 410–422 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 96.

    Klassen, J. L. Defining microbiome function. Nat. Microbiol 3, 864–869 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 97.

    Lau, J. A. & Lennon, J. T. Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc. Natl Acad. Sci. U.S.A. 109, 14058–14062 (2012).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 98.

    Xu, L. et al. Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proc. Natl Acad. Sci. U.S.A 115, E4284–E4293 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 99.

    Cho, I. & Blaser, M. J. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13, 260–270 (2012).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 100.

    Raymann, K., Bobay, L.-M. & Moran, N. A. Antibiotics reduce genetic diversity of core species in the honeybee gut microbiome. Mol. Ecol. 27, 2057–2066 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 101.

    David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 (2014).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 102.

    Ziegler, M., Seneca, F. O., Yum, L. K., Palumbi, S. R. & Voolstra, C. R. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat. Commun. 8, 14213 (2017).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 103.

    Pollock, J., Glendinning, L., Wisedchanwet, T. & Watson, M. The madness of microbiome: attempting to find consensus ‘best practice’ for 16S microbiome studies. Appl. Environ. Microbiol. 84, e02627–17 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 104.

    Roth-Schulze, A. J. et al. Functional biogeography and host specificity of bacterial communities associated with the Marine Green Alga Ulva spp. Mol. Ecol. 27, 1952–1965 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 105.

    Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230 (2012).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 106.

    Meaden, S., Metcalf, C. J. E. & Koskella, B. The effects of host age and spatial location on bacterial community composition in the English Oak tree (Quercus robur). Environ. Microbiol. Rep. 8, 649–658 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 107.

    Lambais, M. R., Barrera, S. E., Santos, E. C., Crowley, D. E. & Jumpponen, A. Phyllosphere metaproteomes of trees from the Brazilian atlantic forest show high levels of functional redundancy. Microb. Ecol. 73, 123–134 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 108.

    Kwong, W. K. & Moran, N. A. Gut microbial communities of social bees. Nat. Rev. Microbiol. 14, 374–384 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 109.

    Oh, J. et al. Temporal stability of the human skin microbiome. Cell 165, 854–866 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 110.

    Garud, N. R., Good, B. H., Hallatschek, O. & Pollard, K. S. Evolutionary dynamics of bacteria in the gut microbiome within and across hosts. PLoS Biol. 17, e3000102 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 111.

    Asnicar, F. et al. Studying vertical microbiome transmission from mothers to infants by strain-level metagenomic profiling. mSystems 2, e00164–16 (2017).

  • 112.

    Yassour, M. et al. Strain-level analysis of mother-to-child bacterial transmission during the first few months of life. Cell Host Microbe 24, 146–154.e4 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 113.

    Fierer, N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 15, 579–590 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 114.

    Gilbert, J. A. et al. Current understanding of the human microbiome. Nat. Med. 24, 392–400 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 115.

    Abubucker, S. et al. Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput. Biol. 8, e1002358 (2012).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 116.

    Jorth, P. et al. Metatranscriptomics of the human oral microbiome during health and disease. MBio 5, e01012–e01014 (2014).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 117.

    Bashiardes, S., Zilberman-Schapira, G. & Elinav, E. Use of metatranscriptomics in microbiome research. Bioinform. Biol. Insights 10, 19–25 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 118.

    Franzosa, E. A. et al. Relating the metatranscriptome and metagenome of the human gut. Proc. Natl Acad. Sci. U.S.A. 111, E2329–E2338 (2014).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 119.

    Abu-Ali, G. S. et al. Metatranscriptome of human faecal microbial communities in a cohort of adult men. Nat. Microbiol. 3, 356–366 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 120.

    Hoang, K. L., Morran, L. T. & Gerardo, N. M. Experimental evolution as an underutilized tool for studying beneficial animal–microbe interactions. Front. Microbiol. 7, 1444 (2016).

  • 121.

    Martino, M. E. et al. Bacterial adaptation to the host’s diet is a key evolutionary force shaping drosophila-lactobacillus symbiosis. Cell Host Microbe 24, 109–119.e6 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 122.

    Schlötterer, C., Kofler, R., Versace, E., Tobler, R. & Franssen, S. U. Combining experimental evolution with next-generation sequencing: a powerful tool to study adaptation from standing genetic variation. Heredity 114, 431–440 (2015).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 123.

    Henry, L. P. & Ayroles, J. F. Meta-analysis suggests the microbiome responds to Evolve and Resequence experiments in Drosophila melanogaster. BMC Microbiol 21, 108 (2021).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 124.

    Wagner, M. R. et al. Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative. Ecol. Lett. 17, 717–726 (2014).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 125.

    Hendry, A. P. Eco-evolutionary Dynamics. (Princeton University Press, 2017).

  • 126.

    Bang, C. et al. Metaorganisms in extreme environments: do microbes play a role in organismal adaptation? Zoology 127, 1–19 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 127.

    Hoyt, J. R. et al. Bacteria isolated from bats inhibit the growth of Pseudogymnoascus destructans, the causative agent of white-nose syndrome. PLoS ONE 10, e0121329 (2015).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 128.

    Cheng, T. L. et al. Efficacy of a probiotic bacterium to treat bats affected by the disease white-nose syndrome. J. Appl. Ecol. 54, 701–708 (2016).

    Article 

    Google Scholar 

  • 129.

    Woodhams, D. C., Bletz, M., Kueneman, J. & McKenzie, V. Managing amphibian disease with skin microbiota. Trends Microbiol. 24, 161–164 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 130.

    Weiss, B. & Aksoy, S. Microbiome influences on insect host vector competence. Trends Parasitol. 27, 514–522 (2011).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 131.

    Zitvogel, L., Ma, Y., Raoult, D., Kroemer, G. & Gajewski, T. F. The microbiome in cancer immunotherapy: diagnostic tools and therapeutic strategies. Science 359, 1366–1370 (2018).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 132.

    Toju, H. et al. Core microbiomes for sustainable agroecosystems. Nat. Plants 4, 247–257 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 133.

    Costello, E. K., Stagaman, K., Dethlefsen, L., Bohannan, B. J. M. & Relman, D. A. The application of ecological theory toward an understanding of the human microbiome. Science 336, 1255–1262 (2012).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 134.

    Christian, N., Whitaker, B. K. & Clay, K. Microbiomes: unifying animal and plant systems through the lens of community ecology theory. Front. Microbiol. 6, 869 (2015).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 135.

    Trevelline, B. K., Fontaine, S. S., Hartup, B. K. & Kohl, K. D. Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices. Proc. Biol. Sci. 286, 20182448 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 136.

    Mueller, E. A., Wisnoski, N. I., Peralta, A. L. & Lennon, J. T. Microbial rescue effects: how microbiomes can save hosts from extinction. Funct. Ecol. 34, 2055-2064 (2020).

  • 137.

    Hird, S. M. Evolutionary biology needs wild microbiomes. Front. Microbiol. 8, 725 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 138.

    Wade, M. J. The co-evolutionary genetics of ecological communities. Nat. Rev. Genet. 8, 185–195 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 139.

    Hammer, T. J., Janzen, D. H., Hallwachs, W., Jaffe, S. P. & Fierer, N. Caterpillars lack a resident gut microbiome. Proc. Natl Acad. Sci. 114, 9641–9646 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 140.

    Hammer, T. J., Sanders, J. G. & Fierer, N. Not all animals need a microbiome. FEMS Microbiol. Lett. 366, fnz117 (2019).

  • 141.

    Heath, K. D. & Stinchcombe, J. R. Explaining mutualism variation: a new evolutionary paradox? Evolution 68, 309–317 (2014).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 142.

    Sandoval-Motta, S., Aldana, M., Martínez-Romero, E. & Frank, A. The human microbiome and the missing heritability problem. Front. Genet. 8, 80 (2017).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 143.

    Wallace, R. J. et al. A heritable subset of the core rumen microbiome dictates dairy cow productivity and emissions. Sci. Adv. 5, eaav8391 (2019).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 144.

    Vollmar, S. et al. The gut microbial architecture of efficiency traits in the domestic poultry model species japanese quail (Coturnix japonica) assessed by mixed linear models. G3 10, 2553–2562 (2020).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 145.

    Hoffmann, A. A., Sgrò, C. M. & Kristensen, T. N. Revisiting adaptive potential, population size, and conservation. Trends Ecol. Evol. 32, 506–517 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 146.

    Bruijning, M., Metcalf, C. J. E., Jongejans, E. & Ayroles, J. F. The evolution of variance control. Trends Ecol. Evol. 35, 22–33 (2020).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 147.

    Douglas, G. M., Bielawski, J. P. & Langille, M. G. I. Re-evaluating the relationship between missing heritability and the microbiome. Microbiome 8, 87 (2020).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 148.

    Johannes, F., Colot, V. & Jansen, R. C. Epigenome dynamics: a quantitative genetics perspective. Nat. Rev. Genet. 9, 883–890 (2008).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 149.

    Slatkin, M. Epigenetic inheritance and the missing heritability problem. Genetics 182, 845–850 (2009).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 150.

    Hernando-Herraez, I., Garcia-Perez, R., Sharp, A. J. & Marques-Bonet, T. DNA methylation: insights into human evolution. PLoS Genet 11, e1005661 (2015).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 151.

    Pujol, B. et al. The missing response to selection in the wild. Trends Ecol. Evol. 33, 337–346 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 152.

    Shaw, R. G. From the past to the future: considering the value and limits of evolutionary prediction. Am. Nat. 193, 1–10 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 153.

    Garud, N. R., Good, B. H., Hallatschek, O. & Pollard, K. S. Evolutionary dynamics of bacteria in the gut microbiome within and across hosts. PLoS Biol.17, e3000102 (2019).

  • 154.

    Truong, D. T., Tett, A., Pasolli, E., Huttenhower, C. & Segata, N. Microbial strain-level population structure and genetic diversity from metagenomes. Genome Res. 27, 626–638 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 155.

    Spor, A., Koren, O. & Ley, R. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat. Rev. Microbiol. 9, 279–290 (2011).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 156.

    Guo, Y. et al. Networks underpinning symbiosis revealed through cross-species eQTL mapping. Genetics 206, 2175–2184 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 157.

    Kohl, K. D. An introductory ‘how-to’ guide for incorporating microbiome research into integrative and comparative biology. Integr. Comp. Biol. 57, 674–681 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 158.

    Marchesi, J. R. & Ravel, J. The vocabulary of microbiome research: a proposal. Microbiome 3, 31 (2015).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 


  • Source: Ecology - nature.com

    The boiling crisis — and how to avoid it

    A statistics-based reconstruction of high-resolution global terrestrial climate for the last 800,000 years