Advances in next-generation sequencing have enabled the widespread measurement of microbiome composition across systems and over the course of microbiome assembly. Despite substantial progress in understanding the deterministic drivers of community composition, the role of historical contingency remains poorly understood. The establishment of new species in a community can depend on the order and/or timing of their arrival, a phenomenon known as a priority effect. Here, we review the mechanisms of priority effects and evidence for their importance in microbial communities inhabiting a range of environments, including the mammalian gut, the plant phyllosphere and rhizosphere, soil, freshwaters and oceans. We describe approaches for the direct testing and prediction of priority effects in complex microbial communities and illustrate these with re-analysis of publicly available plant and animal microbiome datasets. Finally, we discuss the shared principles that emerge across study systems, focusing on eco-evolutionary dynamics and the importance of scale. Overall, we argue that predicting when and how current community state impacts the success of newly arriving microbial taxa is crucial for the management of microbiomes to sustain ecological function and host health. We conclude by discussing outstanding conceptual and practical challenges that are faced when measuring priority effects in microbiomes.
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Connell, J. H. & Slatyer, R. O. Mechanisms of succession in natural communities and their role in community stability and organization. Am. Naturalist 111, 1119–1144 (1977).
Shulman, M. J. et al. Priority effects in the recruitment of juvenile coral reef fishes. Ecology 64, 1508–1513 (1983).
Alford, R. A. & Wilbur, H. M. Priority effects in experimental pond communities: competition between Bufo and Rana. Ecology 66, 1097–1105 (1985).
Grman, E. & Suding, K. N. Within-year soil legacies contribute to strong priority effects of exotics on native California grassland communities. Restor. Ecol. 18, 664–670 (2010).
Almany, G. R. Priority effects in coral reef fish communities. Ecology 84, 1920–1935 (2003).
Fukami, T. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu. Rev. Ecol. Evol. Syst. 46, 1–23 (2015). This study defines mechanisms by which early-arriving species affect late-arriving species (niche pre-emption and niche modification) and describes how and when they are expected to influence community assembly outcomes.
Mariotte, P. et al. Plant-soil feedback: bridging natural and agricultural sciences. Trends Ecol. Evol. 33, 129–142 (2018).
Suding, K. N., Gross, K. L. & Houseman, G. R. Alternative states and positive feedbacks in restoration ecology. Trends Ecol. Evol. 19, 46–53 (2004).
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).
Chng, K. R. et al. Metagenome-wide association analysis identifies microbial determinants of post-antibiotic ecological recovery in the gut. Nat. Ecol. Evol. 4, 1256–1267 (2020).
Lee, S. M. et al. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501, 426–429 (2013). Uncovered the molecular mechanism underlying priority effects between strains of Bacteroides in the mouse gut microbiota.
Martínez, I. et al. Experimental evaluation of the importance of colonization history in early-life gut microbiota assembly. eLife 7, e36521 (2018). Inoculated mice with donor communities at different time points; the mature communities most resembled whichever donor community was inoculated first.
Furman, O. et al. Stochasticity constrained by deterministic effects of diet and age drive rumen microbiome assembly dynamics. Nat. Commun. 11, 1904 (2020). This study showed that the effects of delivery mode on the assembly of the cow rumen microbiome extend beyond initial exposure to different microbiota and they continue to affect bacterial species that arrive throughout the first few years of life.
Cheong, J. Z. A. et al. Priority effects dictate community structure and alter virulence of fungal-bacterial biofilms. ISME J. https://doi.org/10.1038/s41396-021-00901-5 (2021).
Seybold, H. et al. A fungal pathogen induces systemic susceptibility and systemic shifts in wheat metabolome and microbiome composition. Nat. Commun. 11, 1910 (2020).
Carlström, C. I. et al. Synthetic microbiota reveal priority effects and keystone strains in the Arabidopsis phyllosphere. Nat Ecol. Evol. 3, 1445–1454 (2019). This study experimentally manipulated the assembly sequence of strains in a complex synthetic community in the plant phyllosphere.
Halliday, F. W. et al. Facilitative priority effects drive parasite assembly under coinfection. Nat. Ecol. Evol. 4, 1510–1521 (2020).
Peay, K. G., Belisle, M. & Fukami, T. Phylogenetic relatedness predicts priority effects in nectar yeast communities. Proc. Biol. Sci. 279, 749–758 (2012).
Wei, Z. et al. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat. Commun. 6, 8413 (2015). Showed that priority effects between commensal and pathogenic bacteria in the plant rhizosphere can be predicted based on overlap in resource consumption in vitro.
Kennedy, P. G., Peay, K. G. & Bruns, T. D. Root tip competition among ectomycorrhizal fungi: Are priority effects a rule or an exception? Ecology 90, 2098–2107 (2009).
Fukami, T. et al. Assembly history dictates ecosystem functioning: evidence from wood decomposer communities. Ecol. Lett. 13, 675–684 (2010).
Enke, T. N. et al. Modular assembly of polysaccharide-degrading marine microbial communities. Curr. Biol. 29, 1528–1535 (2019).
Svoboda, P., Lindström, E. S., Ahmed Osman, O. & Langenheder, S. Dispersal timing determines the importance of priority effects in bacterial communities. ISME J. 12, 644–646 (2018). Demonstrated that the strength of priority effects in an aquatic community was a product of how well each community was adapted to the habitat and the amount of time between their dispersal events.
Trivedi, P., Leach, J. E., Tringe, S. G., Sa, T. & Singh, B. K. Plant-microbiome interactions: from community assembly to plant health. Nat. Rev. Microbiol. 18, 607–621 (2020).
Shreiner, A. B., Kao, J. Y. & Young, V. B. The gut microbiome in health and disease. Curr. Opin. Gastroenterol. 31, 69–75 (2015).
Long, Z. T. & Karel, I. Resource specialization determines whether history influences community structure. Oikos 96, 62–69 (2002).
Tan, J., Pu, Z., Ryberg, W. A. & Jiang, L. Species phylogenetic relatedness, priority effects, and ecosystem functioning. Ecology 93, 1164–1172 (2012).
Maignien, L., DeForce, E. A., Chafee, M. E., Eren, A. M. & Simmons, S. L. Ecological succession and stochastic variation in the assembly of Arabidopsis thaliana phyllosphere communities. mBio 5, e00682–13 (2014).
Yassour, M. et al. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci. Transl Med. 8, 343ra81 (2016).
Tilman, D. Resource competition between plankton algae: an experimental and theoretical approach. Ecology 58, 338–348 (1977).
Tucker, C. M. & Fukami, T. Environmental variability counteracts priority effects to facilitate species coexistence: evidence from nectar microbes. Proc. Biol. Sci. 281, 20132637 (2014).
Poza-Carrion, C., Suslow, T. & Lindow, S. Resident bacteria on leaves enhance survival of immigrant cells of Salmonella enterica. Phytopathology 103, 341–351 (2013).
Monier, J.-M. & Lindow, S. E. Aggregates of resident bacteria facilitate survival of immigrant bacteria on leaf surfaces. Microb. Ecol. 49, 343–352 (2005).
Piccardi, P., Vessman, B. & Mitri, S. Toxicity drives facilitation between 4 bacterial species. Proc. Natl Acad. Sci. USA 116, 15979–15984 (2019).
Potnis, N. et al. Xanthomonas perforans colonization influences Salmonella enterica in the tomato phyllosphere. Appl. Environ. Microbiol. 80, 3173–3180 (2014).
Zhang, Y., Kastman, E. K., Guasto, J. S. & Wolfe, B. E. Fungal networks shape dynamics of bacterial dispersal and community assembly in cheese rind microbiomes. Nat. Commun. 9, 336 (2018).
Chang, P. V. Chemical mechanisms of colonization resistance by the gut microbial metabolome. ACS Chem. Biol. 15, 1119–1126 (2020).
Borton, M. A. et al. Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome. Microbiome 5, 47 (2017).
Snelders, N. C. et al. Microbiome manipulation by a soil-borne fungal plant pathogen using effector proteins. Nat. Plants 6, 1365–1374 (2020).
Foster, J. L. & Fogleman, J. C. Bacterial succession in necrotic tissue of agria cactus (Stenocereus gummosus). Appl. Environ. Microbiol. 60, 619–625 (1994).
O’Keeffe, K. R., Halliday, F. W., Jones, C. D., Carbone, I. & Mitchell, C. E. Parasites, niche modification, and the host microbiome: a field survey of multiple parasites. Mol. Ecol. 30, 2404–2416 (2021).
Joo, J. et al. Bacteriophage-mediated competition in Bordetella bacteria. Proc. Biol. Sci. 273, 1843–1848 (2006).
Fernández, L., Rodríguez, A. & García, P. Phage or foe: an insight into the impact of viral predation on microbial communities. ISME J. 12, 1171–1179 (2018).
Sweere, J. M. et al. Bacteriophage trigger antiviral immunity and prevent clearance of bacterial infection. Science 363, eaat9691 (2019).
Veiga, P. et al. Bifidobacterium animalis subsp. lactis fermented milk product reduces inflammation by altering a niche for colitogenic microbes. Proc. Natl Acad. Sci. USA 107, 18132–18137 (2010).
Topisirovic, L. et al. Potential of lactic acid bacteria isolated from specific natural niches in food production and preservation. Int. J. Food Microbiol. 112, 230–235 (2006).
De Vuyst, L. & Leroy, F. Bacteriocins from lactic acid bacteria: production, purification, and food applications. J. Mol. Microbiol. Biotechnol. 13, 194–199 (2007).
ten Cate, J. M. Biofilms, a new approach to the microbiology of dental plaque. Odontology 94, 1–9 (2006).
Gibbons, S. M., Kearney, S. M., Smillie, C. S. & Alm, E. J. Two dynamic regimes in the human gut microbiome. PLoS Comput. Biol. 13, e1005364 (2017).
Mouillot, D. et al. Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs. Proc. Natl Acad. Sci. USA 111, 13757–13762 (2014).
Louca, S. et al. Function and functional redundancy in microbial systems. Nat. Ecol. Evol. 2, 936–943 (2018).
The Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012).
Zhang, Q.-G. & Zhang, D.-Y. Colonization sequence influences selection and complementarity effects on biomass production in experimental algal microcosms. Oikos 116, 1748–1758 (2007).
Dickie, I. A., Fukami, T., Wilkie, J. P., Allen, R. B. & Buchanan, P. K. Do assembly history effects attenuate from species to ecosystem properties? A field test with wood-inhabiting fungi. Ecol. Lett. 15, 133–141 (2012).
Bittleston, L. S., Gralka, M., Leventhal, G. E., Mizrahi, I. & Cordero, O. X. Context-dependent dynamics lead to the assembly of functionally distinct microbial communities. Nat. Commun. 11, 1440 (2020).
Boyle, J. A., Simonsen, A. K., Frederickson, M. E. & Stinchcombe, J. R. Priority effects alter interaction outcomes in a legume-rhizobium mutualism. Proc. Biol. Sci. 288, 20202753 (2021).
Fukami, T. & Morin, P. J. Productivity–biodiversity relationships depend on the history of community assembly. Nature 424, 423–426 (2003).
Medini, D., Donati, C., Tettelin, H., Masignani, V. & Rappuoli, R. The microbial pan-genome. Curr. Opin. Genet. Dev. 15, 589–594 (2005).
Wagg, C., Schlaeppi, K., Banerjee, S., Juramae, E. E. & van der Heijden, M. G. A. Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nat. Commun. 10, 4841 (2019).
Rummens, K., De Meester, L. & Souffreau, C. Inoculation history affects community composition in experimental freshwater bacterioplankton communities. Environ. Microbiol. 20, 1120–1133 (2018).
Steen, A. D. et al. High proportions of bacteria and archaea across most biomes remain uncultured. ISME J. 13, 3126–3130 (2019).
Imachi, H. et al. Isolation of an archaeon at the prokaryote–eukaryote interface. Nature 577, 519–525 (2020).
D’Onofrio, A. et al. Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem. Biol. 17, 254–264 (2010).
Maldonado-Gómez, M. X. et al. Stable engraftment of Bifidobacterium longum AH1206 in the human gut depends on individualized features of the resident microbiome. Cell Host Microbe 20, 515–526 (2016). This study identified features of the resident microbiome (bacterial taxa and genes) that predicted variation in the persistence of a probiotic among subjects in a clinical trial.
Christian, N., Herre, E. A., Mejia, L. C. & Clay, K. Exposure to the leaf litter microbiome of healthy adults protects seedlings from pathogen damage. Proc. Biol. Sci. 284, 20170641 (2017).
Alavi, S. et al. Interpersonal gut microbiome variation drives susceptibility and resistance to cholera infection. Cell 181, 1533–1546 (2020).
Hiscox, J. et al. Priority effects during fungal community establishment in beech wood. ISME J. 9, 2246–2260 (2015).
Losos, J. B. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279, 2115–2118 (1998).
Glitzenstein, J. S., Harcombe, P. A. & Streng, D. R. Disturbance, succession, and maintenance of species diversity in an east texas forest. Ecol. Monogr. 56, 243–258 (1986).
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).
Bäckhed, F. et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17, 852 (2015).
Edwards, J. A. et al. Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice. PLoS Biol. 16, e2003862 (2018).
Chappell, C. R. & Fukami, T. Nectar yeasts: a natural microcosm for ecology. Yeast 35, 417–423 (2018).
Loeuille, N. & Leibold, M. A. Evolution in metacommunities: on the relative importance of species sorting and monopolization in structuring communities. Am. Nat. 171, 788–799 (2008).
Vallespir Lowery, N. & Ursell, T. Structured environments fundamentally alter dynamics and stability of ecological communities. Proc. Natl Acad. Sci. USA 116, 379–388 (2019).
Wittmann, M. J. & Fukami, T. Eco-evolutionary buffering: rapid evolution facilitates regional species coexistence despite local priority effects. Am. Nat. 191, E171–E184 (2018).
Eitam, A., Blaustein, L. & Mangel, M. Density and intercohort priority effects on larval Salamandra salamandra in temporary pools. Oecologia 146, 36–42 (2005).
Woody, S. T., Ives, A. R., Nordheim, E. V. & Andrews, J. H. Dispersal, density dependence, and population dynamics of a fungal microbe on leaf surfaces. Ecology 88, 1513–1524 (2007).
Wein, T. et al. Carrying capacity and colonization dynamics of Curvibacter in the hydra host habitat. Front. Microbiol. 9, 443 (2018).
Remus-Emsermann, M. N. P. et al. Spatial distribution analyses of natural phyllosphere-colonizing bacteria on Arabidopsis thaliana revealed by fluorescence in situ hybridization. Environ. Microbiol. 16, 2329–2340 (2014).
Tewksbury, J. J. & Lloyd, J. D. Positive interactions under nurse-plants: spatial scale, stress gradients and benefactor size. Oecologia 127, 425–434 (2001).
Monier, J.-M. & Lindow, S. E. Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces. Proc. Natl Acad. Sci. USA 100, 15977–15982 (2003).
LaSarre, B., McCully, A. L., Lennon, J. T. & McKinlay, J. B. Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients. ISME J. 11, 337–348 (2017).
McCully, A. L., LaSarre, B. & McKinlay, J. B. Growth-independent cross-feeding modifies boundaries for coexistence in a bacterial mutualism. Environ. Microbiol. 19, 3538–3550 (2017).
Nuñez, M. A., Horton, T. R. & Simberloff, D. Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90, 2352–2359 (2009).
Fürst, U. et al. Perception of Agrobacterium tumefaciens flagellin by FLS2XL confers resistance to crown gall disease. Nat. Plants 6, 22–27 (2020).
Lu, P., Bian, G., Pan, X. & Xi, Z. Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl. Trop. Dis. 6, e1754 (2012).
Vannette, R. L. & Fukami, T. Historical contingency in species interactions: towards niche-based predictions. Ecol. Lett. 17, 115–124 (2014).
Onoda, Y. et al. Trade-off between light interception efficiency and light use efficiency: implications for species coexistence in one-sided light competition. J. Ecol. 102, 167–175 (2014).
Burson, A., Stomp, M., Greenwell, E., Grosse, J. & Huisman, J. Competition for nutrients and light: testing advances in resource competition with a natural phytoplankton community. Ecology 99, 1108–1118 (2018).
Malerba, M. E., Palacios, M. M., Palacios Delgado, Y. M., Beardall, J. & Marshall, D. J. Cell size, photosynthesis and the package effect: an artificial selection approach. N. Phytol. 219, 449–461 (2018).
Hajishengallis, G. et al. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 10, 497–506 (2011).
Herren, C. M. & McMahon, K. D. Keystone taxa predict compositional change in microbial communities. Environ. Microbiol. 20, 2207–2217 (2018).
Battin, T. J., Kaplan, L. A., Newbold, J. D., Cheng, X. & Hansen, C. Effects of current velocity on the nascent architecture of stream microbial biofilms. Appl. Environ. Microbiol. 69, 5443–5452 (2003).
Tecon, R., Ebrahimi, A., Kleyer, H., Erev Levi, S. & Or, D. Cell-to-cell bacterial interactions promoted by drier conditions on soil surfaces. Proc. Natl Acad. Sci. USA 115, 9791–9796 (2018).
van der Wal, A., Tecon, R., Kreft, J.-U., Mooij, W. M. & Leveau, J. H. J. Explaining bacterial dispersion on leaf surfaces with an individual-based model (PHYLLOSIM). PLoS ONE 8, e75633 (2013).
Pande, S. et al. Privatization of cooperative benefits stabilizes mutualistic cross-feeding interactions in spatially structured environments. ISME J. 10, 1413–1423 (2016).
Momeni, B., Waite, A. J. & Shou, W. Spatial self-organization favors heterotypic cooperation over cheating. eLife 2, e00960 (2013).
Hol, F. J. H., Galajda, P., Woolthuis, R. G., Dekker, C. & Keymer, J. E. The idiosyncrasy of spatial structure in bacterial competition. BMC Res. Notes 8, 245 (2015).
Dal Co, A., van Vliet, S., Kiviet, D. J., Schlegel, S. & Ackermann, M. Short-range interactions govern the dynamics and functions of microbial communities. Nat. Ecol. Evol. 4, 366–375 (2020).
Dang, A. T. & Marsland, B. J. Microbes, metabolites, and the gut–lung axis. Mucosal Immunol. 12, 843–850 (2019).
Morella, N. M., Zhang, X. & Koskella, B. Tomato seed-associated bacteria confer protection of seedlings against foliar disease caused by Pseudomonas syringae. Phytobiomes J. 3, 177–190 (2019).
Scharschmidt, T. C. et al. A wave of regulatory t cells into neonatal skin mediates tolerance to commensal microbes. Immunity 43, 1011–1021 (2015).
Sadd, B. M., Kleinlogel, Y., Schmid-Hempel, R. & Schmid-Hempel, P. Trans-generational immune priming in a social insect. Biol. Lett. 1, 386–388 (2005).
Zhou, J. & Ning, D. Stochastic community assembly: does it matter in microbial ecology? Microbiol. Mol. Biol. Rev. https://doi.org/10.1128/MMBR.00002-17 (2017).
Rillig, M. C. et al. Interchange of entire communities: microbial community coalescence. Trends Ecol. Evol. 30, 470–476 (2015).
Meadow, J. F., Bateman, A. C., Herkert, K. M., O’Connor, T. K. & Green, J. L. Significant changes in the skin microbiome mediated by the sport of roller derby. PeerJ 1, e53 (2013).
Vannette, R. L. The floral microbiome: plant, pollinator, and microbial perspectives. Annu. Rev. Ecol. Evol. Syst. 51, 363–386 (2020).
Pachiadaki, M. G. et al. Charting the complexity of the marine microbiome through single-cell genomics. Cell 179, 1623–1635 (2019).
Watrous, J. D. & Dorrestein, P. C. Imaging mass spectrometry in microbiology. Nat. Rev. Microbiol. 9, 683–694 (2011).
Hungate, B. A. et al. Quantitative microbial ecology through stable isotope probing. Appl. Environ. Microbiol. 81, 7570–7581 (2015).
Tropini, C., Earle, K. A., Huang, K. C. & Sonnenburg, J. L. The gut microbiome: connecting spatial organization to function. Cell Host Microbe 21, 433–442 (2017).
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).
Braga, L. P. P. et al. Impact of phages on soil bacterial communities and nitrogen availability under different assembly scenarios. Microbiome 8, 52 (2020).
Rao, C. et al. Multi-kingdom ecological drivers of microbiota assembly in preterm infants. Nature 591, 633–638 (2021).
Schluter, D., Price, T. D. & Grant, P. R. Ecological character displacement in Darwin’s finches. Science 227, 1056–1059 (1985).
Zee, P. C. & Fukami, T. Priority effects are weakened by a short, but not long, history of sympatric evolution. Proc. R. Soc. Lond. B Biol. Sci. 285, 20171722 (2018).
Gensollen, T., Iyer, S. S., Kasper, D. L. & Blumberg, R. S. How colonization by microbiota in early life shapes the immune system. Science 352, 539–544 (2016).
Suez, J. et al. Post-antibiotic gut mucosal microbiome reconstitution is impaired by probiotics and improved by autologous FMT. Cell 174, 1406–1423 (2018).
Urban, M. C. & De Meester, L. Community monopolization: local adaptation enhances priority effects in an evolving metacommunity. Proc. R. Soc. Lond. B Biol. Sci. 276, 4129–4138 (2009).
De Meester, L., Vanoverbeke, J., Kilsdonk, L. J. & Urban, M. C. Evolving perspectives on monopolization and priority effects. Trends Ecol. Evol. 31, 136–146 (2016). This study describes how evolutionary changes in early-arriving strains or species can limit colonization by later-arriving strains or species.
Madi, N., Vos, M., Murall, C. L., Legendre, P. & Shapiro, B. J. Does diversity beget diversity in microbiomes? eLife 9, e58999 (2020).
Castledine, M., Padfield, D. & Buckling, A. Experimental (co)evolution in a multi-species microbial community results in local maladaptation. Ecol. Lett. 23, 1673–1681 (2020).
von Gillhaussen, P. et al. Priority effects of time of arrival of plant functional groups override sowing interval or density effects: a grassland experiment. PLoS ONE 9, e86906 (2014).
Ferrero, A. F. Effect of compaction simulating cattle trampling on soil physical characteristics in woodland. Soil. Tillage Res. 19, 319–329 (1991).
Maron, J. L. & Jefferies, R. L. Bush lupine mortality, altered resource availability, and alternative vegetation states. Ecology 80, 443–454 (1999).
Eng, T. et al. Iron supplementation eliminates antagonistic interactions between root-associated bacteria. Front. Microbiol. 11, 1742 (2020).
Gong, B.-Q. et al. Cross-microbial protection via priming a conserved immune co-receptor through juxtamembrane phosphorylation in plants. Cell Host Microbe 26, 810–822 (2019).
Goldford, J. E. et al. Emergent simplicity in microbial community assembly. Science 361, 469–474 (2018).
Lindemann, J. Competition between ice nucleation-active wild type and ice nucleation-deficient deletion mutant strains of Pseudomonas syringae and P. fluorescens biovar I and biological control of frost injury on strawberry blossoms. Phytopathology 77, 882 (1987).
Guittar, J., Shade, A. & Litchman, E. Trait-based community assembly and succession of the infant gut microbiome. Nat. Commun. 10, 512 (2019).
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K. & Schloss, P. D. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 79, 5112–5120 (2013).
Nyholm, S. V. & McFall-Ngai, M. The winnowing: establishing the squid-Vibrio symbiosis. Nat. Rev. Microbiol. 2, 632–642 (2004).
O’Hanlon, D. E., Moench, T. R. & Cone, R. A. Vaginal pH and microbicidal lactic acid when lactobacilli dominate the microbiota. PLoS ONE 8, e80074 (2013).
Pantel, J. H., Duvivier, C. & Meester, L. D. Rapid local adaptation mediates zooplankton community assembly in experimental mesocosms. Ecol. Lett. 18, 992–1000 (2015).
Fukami, T., Beaumont, H. J. E., Zhang, X.-X. & Rainey, P. B. Immigration history controls diversification in experimental adaptive radiation. Nature 446, 436–439 (2007).
Rigby, M. C., Hechinger, R. F. & Stevens, L. Why should parasite resistance be costly? Trends Parasitol. 18, 116–120 (2002).
Koskella, B. Phage-mediated selection on microbiota of a long-lived host. Curr. Biol. 23, 1256–1260 (2013).
R.D. was supported by the National Science Foundation Graduate Research Fellowship (grant no. 1650114). The authors thank members of the graduate seminar ‘Microbiomes in and as Food Webs’ for helpful discussion.
The authors declare no competing interests.
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- Priority effects
Refers, in the narrowest sense, to instances in which the outcomes of species interactions vary according to the order of arrival but is often broadened (including here) to include instances in which arrival timing and/or the abundances of resident species affect the ability of new species to establish.
A change in the biotic or abiotic environment that affects organisms in an ecological community; considered a pulse perturbation (or disturbance) when it is brief compared with the population timescales of relevant organisms or a press perturbation (stress, regime shift) if it is more prolonged.
- Trophic resources
Any resource that can be metabolized for biomass production.
- Non-trophic resources
Any resource that aids the growth or survival of an organism without being consumed for biomass or energy.
- Exploitative competition
An adverse indirect interaction between consumers caused by depleting a shared limiting resource.
- Interference competition
An adverse direct interaction between species, generally mediated by harmful behaviours or chemicals.
- Apparent competition
An adverse indirect interaction between species that increases the abundance or impact of a common enemy (pathogen, consumer, antibody or predator).
- Keystone taxa
A species or strain whose effect is large and disproportionate to its abundance in a community.
A set of interacting communities that are linked by dispersal.
- Community coalescence
The mixing of multiple ecological communities.
- Ecological character displacement
Evolutionary divergence of species with overlapping ranges to lessen resource competition.
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Debray, R., Herbert, R.A., Jaffe, A.L. et al. Priority effects in microbiome assembly. Nat Rev Microbiol 20, 109–121 (2022). https://doi.org/10.1038/s41579-021-00604-w
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