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Mutualism-enhancing mutations dominate early adaptation in a two-species microbial community

  • Agostini, S. et al. Ocean acidification drives community shifts towards simplified non-calcified habitats in a subtropical–temperate transition zone. Sci. Rep. 8, 11354 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Walther, G.-R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Gilbert, B. & Levine, J. M. Ecological drift and the distribution of species diversity. Proc. Biol. Sci. 284, 20170507 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • White, E. P. et al. A comparison of the species–time relationship across ecosystems and taxonomic groups. Oikos 112, 185–195 (2006).

    Article 

    Google Scholar 

  • Sax, D. F. & Gaines, S. D. Species invasions and extinction: the future of native biodiversity on islands. Proc. Natl Acad. Sci. USA 105, 11490–11497 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Thompson, J. N. Rapid evolution as an ecological process. Trends Ecol. Evol. 13, 329–332 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Post, D. M. & Palkovacs, E. P. Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play. Philos. Trans. R. Soc. Lond. B 364, 1629–1640 (2009).

    Article 

    Google Scholar 

  • Reznick, D. N. & Travis, J. Experimental studies of evolution and eco-evo dynamics in guppies (Poecilia reticulata). Annu. Rev. Ecol. Evol. Syst. https://doi.org/10.1146/annurev-ecolsys-110218-024926 (2019).

  • Hendry, A. P. Eco-evolutionary Dynamics (Princeton Univ. Press, 2020).

  • Schoener, T. W. The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science 331, 426–429 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Yoshida, T., Jones, L. E., Ellner, S. P., Fussmann, G. F. & Hairston, N. G. Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424, 303–306 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hansen, S. K., Rainey, P. B., Haagensen, J. A. J. & Molin, S. Evolution of species interactions in a biofilm community. Nature 445, 533–536 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hillesland, K. L. & Stahl, D. A. Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc. Natl Acad. Sci. USA 107, 2124–2129 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Turcotte, M. M., Reznick, D. N. & Hare, J. D. The impact of rapid evolution on population dynamics in the wild: experimental test of eco-evolutionary dynamics. Ecol. Lett. 14, 1084–1092 (2011).

    Article 
    PubMed 

    Google Scholar 

  • Lawrence, D. et al. Species interactions alter evolutionary responses to a novel environment. PLoS Biol. 10, e1001330 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Celiker, H. & Gore, J. Clustering in community structure across replicate ecosystems following a long-term bacterial evolution experiment. Nat. Commun. 5, 4643 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Andrade-Domínguez, A. et al. Eco-evolutionary feedbacks drive species interactions. ISME J. 8, 1041–1054 (2014).

    Article 
    PubMed 

    Google Scholar 

  • Reznick, D. Hard and soft selection revisited: how evolution by natural selection works in the real world. J. Hered. 107, 3–14 (2016).

    Article 
    PubMed 

    Google Scholar 

  • Matthews, B., Aebischer, T., Sullam, K. E., Lundsgaard-Hansen, B. & Seehausen, O. Experimental evidence of an eco-evolutionary feedback during adaptive divergence. Curr. Biol. 26, 483–489 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Harcombe, W. R., Chacón, J. M., Adamowicz, E. M., Chubiz, L. M. & Marx, C. J. Evolution of bidirectional costly mutualism from byproduct consumption. Proc. Natl Acad. Sci. USA 115, 12000–12004 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Preussger, D., Giri, S., Muhsal, L. K., Oña, L. & Kost, C. Reciprocal fitness feedbacks promote the evolution of mutualistic cooperation. Curr. Biol. https://doi.org/10.1016/j.cub.2020.06.100 (2020).

  • Adamowicz, E. M., Muza, M., Chacón, J. M. & Harcombe, W. R. Cross-feeding modulates the rate and mechanism of antibiotic resistance evolution in a model microbial community of Escherichia coli and Salmonella enterica. PLoS Pathog. 16, e1008700 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Rodríguez-Verdugo, A. & Ackermann, M. Rapid evolution destabilizes species interactions in a fluctuating environment. ISME J. 15, 450–460 (2021).

    Article 
    PubMed 

    Google Scholar 

  • Barber, J. N. et al. The evolution of coexistence from competition in experimental co-cultures of Escherichia coli and Saccharomyces cerevisiae. ISME J. 15, 746–761 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hart, S. F. M., Chen, C.-C. & Shou, W. Pleiotropic mutations can rapidly evolve to directly benefit self and cooperative partner despite unfavorable conditions. eLife 10, e57838 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kokko, H. et al. Can evolution supply what ecology demands? Trends Ecol. Evol. 32, 187–197 (2017).

    Article 
    PubMed 

    Google Scholar 

  • Nuismer, S. Introduction to Coevolutionary Theory (Macmillan Learning, 2017).

  • Stoltzfus, A. & McCandlish, D. M. Mutational biases influence parallel adaptation. Mol. Biol. Evol. 34, 2163–2172 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Payne, J. L. et al. Transition bias influences the evolution of antibiotic resistance in Mycobacterium tuberculosis. PLoS Biol. 17, e3000265 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Storz, J. F. et al. The role of mutation bias in adaptive molecular evolution: insights from convergent changes in protein function. Philos. Trans. R. Soc. Lond. B 374, 20180238 (2019).

    Article 
    CAS 

    Google Scholar 

  • Gomez, K., Bertram, J. & Masel, J. Mutation bias can shape adaptation in large asexual populations experiencing clonal interference. Proc. Biol. Sci. 287, 20201503 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Venkataram, S., Monasky, R., Sikaroodi, S. H., Kryazhimskiy, S. & Kacar, B. Evolutionary stalling and a limit on the power of natural selection to improve a cellular module. Proc. Natl Acad. Sci. USA 117, 18582–18590 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hom, E. F. Y. & Murray, A. W. Niche engineering demonstrates a latent capacity for fungal–algal mutualism. Science 345, 94–98 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wolfe, B. E. & Dutton, R. J. Fermented foods as experimentally tractable microbial ecosystems. Cell 161, 49–55 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Chacón, J. M., Hammarlund, S. P., Martinson, J. N. V., Smith, L. B. & Harcombe, W. R. The ecology and evolution of model microbial mutualisms. Annu. Rev. Ecol. Evol. Syst. 52, 363–384 (2021).

    Article 

    Google Scholar 

  • Blasche, S., Kim, Y., Oliveira, A. P. & Patil, K. R. Model microbial communities for ecosystems biology. Curr. Opin. Syst. Biol. 6, 51–57 (2017).

    Article 

    Google Scholar 

  • Levy, S. F. et al. Quantitative evolutionary dynamics using high-resolution lineage tracking. Nature 519, 181–186 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Venkataram, S. et al. Development of a comprehensive genotype-to-fitness map of adaptation-driving mutations in yeast. Cell 166, 1585–1596.e22 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jones, E. I., Bronstein, J. L. & Ferrière, R. The fundamental role of competition in the ecology and evolution of mutualisms. Ann. N. Y. Acad. Sci. 1256, 66–88 (2012).

    Article 
    PubMed 

    Google Scholar 

  • Boyer, S., Hérissant, L. & Sherlock, G. Adaptation is influenced by the complexity of environmental change during evolution in a dynamic environment. PLoS Genet. 17, e1009314 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Blundell, J. R. et al. The dynamics of adaptive genetic diversity during the early stages of clonal evolution. Nat. Ecol. Evol. 3, 293–301 (2019).

    Article 
    PubMed 

    Google Scholar 

  • Good, B. H., Rouzine, I. M., Balick, D. J., Hallatschek, O. & Desai, M. M. Distribution of fixed beneficial mutations and the rate of adaptation in asexual populations. Proc. Natl Acad. Sci. USA 109, 4950–4955 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Good, B. H., Martis, S. & Hallatschek, O. Adaptation limits ecological diversification and promotes ecological tinkering during the competition for substitutable resources. Proc. Natl Acad. Sci. USA 115, E10407–E10416 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhu, Y. O., Siegal, M. L., Hall, D. W. & Petrov, D. A. Precise estimates of mutation rate and spectrum in yeast. Proc. Natl Acad. Sci. USA 111, E2310–E2318 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dunham, M. J. et al. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 99, 16144–16149 (2002).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yona, A. H. et al. Chromosomal duplication is a transient evolutionary solution to stress. Proc. Natl Acad. Sci. USA 109, 21010–21015 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sunshine, A. B. et al. The fitness consequences of aneuploidy are driven by condition-dependent gene effects. PLoS Biol. 13, e1002155 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gerrish, P. J. & Lenski, R. E. The fate of competing beneficial mutations in an asexual population. Genetica 102-103, 127–144 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Desai, M. M. & Fisher, D. S. Beneficial mutation–selection balance and the effect of linkage on positive selection. Genetics 176, 1759–1798 (2007).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Schiffels, S., Szöllosi, G. J., Mustonen, V. & Lässig, M. Emergent neutrality in adaptive asexual evolution. Genetics 189, 1361–1375 (2011).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nguyen, Ba,A. N. et al. High-resolution lineage tracking reveals travelling wave of adaptation in laboratory yeast. Nature 575, 494–499 (2019).

    Article 

    Google Scholar 

  • Foster, K. R., Shaulsky, G., Strassmann, J. E., Queller, D. C. & Thompson, C. R. L. Pleiotropy as a mechanism to stabilize cooperation. Nature 431, 693–696 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Sachs, J. L., Mueller, U. G., Wilcox, T. P. & Bull, J. J. The evolution of cooperation. Q. Rev. Biol. 79, 135–160 (2004).

    Article 
    PubMed 

    Google Scholar 

  • Harcombe, W. Novel cooperation experimentally evolved between species. Evolution 64, 2166–2172 (2010).

    PubMed 

    Google Scholar 

  • Vasi, F., Travisano, M. & Lenski, R. E. Long-term experimental evolution in Escherichia coli. II. Changes in life-history traits during adaptation to a seasonal environment. Am. Nat. 144, 432–456 (1994).

    Article 

    Google Scholar 

  • MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, 2001).

  • Reznick, D., Bryant, M. J. & Bashey, F. r– and K-selection revisited: the role of population regulation in life-history evolution. Ecology 83, 1509–1520 (2002).

    Article 

    Google Scholar 

  • Mueller, L. D. & Ayala, F. J. Trade-off between r-selection and K-selection in Drosophila populations. Proc. Natl Acad. Sci. USA 78, 1303–1305 (1981).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Novak, M., Pfeiffer, T., Lenski, R. E., Sauer, U. & Bonhoeffer, S. Experimental tests for an evolutionary trade-off between growth rate and yield in E. coli. Am. Nat. 168, 242–251 (2006).

    Article 
    PubMed 

    Google Scholar 

  • Bachmann, H. et al. Availability of public goods shapes the evolution of competing metabolic strategies. Proc. Natl Acad. Sci. USA 110, 14302–14307 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lipson, D. A. The complex relationship between microbial growth rate and yield and its implications for ecosystem processes. Front. Microbiol. 6, 615 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Orivel, J. et al. Trade-offs in an ant–plant–fungus mutualism. Proc. Biol. Sci. 284, 20161679 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Fritts, R. K. et al. Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community. ISME J. 14, 2816–2828 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wortel, M. T., Noor, E., Ferris, M., Bruggeman, F. J. & Liebermeister, W. Metabolic enzyme cost explains variable trade-offs between microbial growth rate and yield. PLoS Comput. Biol. 14, e1006010 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cheng, C. et al. Laboratory evolution reveals a two-dimensional rate-yield tradeoff in microbial metabolism. PLoS Comput. Biol. 15, e1007066 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Luckinbill, L. S. r and K selection in experimental populations of Escherichia coli. Science 202, 1201–1203 (1978).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Oxman, E., Alon, U. & Dekel, E. Defined order of evolutionary adaptations: experimental evidence. Evolution 62, 1547–1554 (2008).

    Article 
    PubMed 

    Google Scholar 

  • Jasmin, J.-N., Dillon, M. M. & Zeyl, C. The yield of experimental yeast populations declines during selection. Proc. Biol. Sci. 279, 4382–4388 (2012).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Laan, L., Koschwanez, J. H. & Murray, A. W. Evolutionary adaptation after crippling cell polarization follows reproducible trajectories. eLife 4, e09638 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Blount, Z. D., Lenski, R. E. & Losos, J. B. Contingency and determinism in evolution: replaying life’s tape. Science 362, eaam5979 (2018).

    Article 
    PubMed 

    Google Scholar 

  • Fukami, T. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu. Rev. Ecol. Evol. Syst. 46, 1–23 (2015).

    Article 

    Google Scholar 

  • Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Meyer, J. R. et al. Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 335, 428–432 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Herron, M. D. & Doebeli, M. Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biol. 11, e1001490 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hillesland, K. L. et al. Erosion of functional independence early in the evolution of a microbial mutualism. Proc. Natl Acad. Sci. USA 111, 14822–14827 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Meroz, N., Tovi, N., Sorokin, Y. & Friedman, J. Community composition of microbial microcosms follows simple assembly rules at evolutionary timescales. Nat. Commun. 12, 2891 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • MacLean, R. C. The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies. Heredity 100, 471–477 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Dunn, B. et al. Recurrent rearrangement during adaptive evolution in an interspecific yeast hybrid suggests a model for rapid introgression. PLoS Genet. 9, e1003366 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Barillot, E., Lacroix, B. & Cohen, D. Theoretical analysis of library screening using a N-dimensional pooling strategy. Nucleic Acids Res. 19, 6241–6247 (1991).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Baym, M., Shaket, L., Anzai, I. A., Adesina, O. & Barstow, B. Rapid construction of a whole-genome transposon insertion collection for Shewanella oneidensis by Knockout Sudoku. Nat. Commun. 7, 13270 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Baym, M. et al. Inexpensive multiplexed library preparation for megabase-sized genomes. PLoS ONE 10, e0128036 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Venkataram, S., Kuo, H., Hom, E., Kryazhimskiy, S. Early adaptation in a microbial community is dominated by mutualism-enhancing mutations. Dryad https://doi.org/10.6076/D14K5X (2022).

  • Plant–pollinator network change across a century in the subarctic

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