Coevolution with Bacteriophages Drives Genome-Wide Host Evolution and Constrains the Acquisition of Abiotic-Beneficial Mutations
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Studies of antagonistic coevolution between hosts and parasites typically focus on resistance and infectivity traits. However, coevolution could also have genome-wide effects on the hosts due to pleiotropy, epistasis, or selection for evolvability. Here, we investigate these effects in the bacterium Pseudomonas fluorescens SBW25 during approximately 400 generations of evolution in the presence or absence of bacteriophage (coevolution or evolution treatments, respectively). Coevolution resulted in variable phage resistance, lower competitive fitness in the absence of phages, and greater genome-wide divergence both from the ancestor and between replicates, in part due to the evolution of increased mutation rates. Hosts from coevolution and evolution treatments had different suites of mutations. A high proportion of mutations observed in coevolved hosts were associated with a known phage target binding site, the lipopolysaccharide (LPS), and correlated with altered LPS length and phage resistance. Mutations in evolved bacteria were correlated with higher fitness in the absence of phages. However, the benefits of these growth-promoting mutations were completely lost when these bacteria were subsequently coevolved with phages, indicating that they were not beneficial in the presence of resistance mutations (consistent with negative epistasis). Our results show that in addition to affecting genome-wide evolution in loci not obviously linked to parasite resistance, coevolution can also constrain the acquisition of mutations beneficial for growth in the abiotic environment.
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The traditional fitness assay (competition assay) is a more efficient tool than the Luria-Delbrück protocol for measuring bacterial fitness.
“The traditional fitness assay (also known as the competition assay) is a more efficient tool, which has been increasingly conducted in tandem with fluctuation assays in recent studies (Scanlan et al. 2015).”
From rSalvador: An R Package for the Fluctuation Experiment (2017) · cites this paper as Scanlan et al. 2015
Cites
The neighbor-joining method: a new method for reconstructing phylogenetic trees.
Saitou, N., & Nei, M. (1987) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040454 · Cited by 59,962 · see citing works
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607 · see citing works
Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992) · Genetics · doi:10.1093/genetics/131.2.479 · Cited by 13,929 · see citing works
A new method for non-parametric multivariate analysis of variance
Anderson, M. J. (2001) · Austral Ecology · doi:10.1111/j.1442-9993.2001.01070.pp.x · Cited by 13,828 · see citing works
Molecular Evolution and Phylogenetics
Nei, M., & Kumar, S. (2000) · doi:10.1093/oso/9780195135848.001.0001 · Cited by 8,012 · see citing works
VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencingPreprint
Koboldt, D. C., Zhang, Q., Larson, D. E., Shen, D., McLellan, M. D., Lin, L., Miller, C. A., Mardis, E. R., Ding, L., & Wilson, R. K. (2012) · Genome Research · doi:10.1101/gr.129684.111 · Cited by 4,822 · see citing works
Valen, L. V. (1973) · Medical Entomology and Zoology · Cited by 2,468 · see citing works
THE EVOLUTIONARY ADVANTAGE OF RECOMBINATION
Felsenstein, J. (1974) · Genetics · doi:10.1093/genetics/78.2.737 · Cited by 1,711 · see citing works
Darwinian Evolution Can Follow Only Very Few Mutational Paths to Fitter Proteins
Weinreich, D. M., Delaney, N. F., DePristo, M. A., & Hartl, D. L. (2006) · Science · doi:10.1126/science.1123539 · Cited by 1,418 · see citing works
Sexual reproduction as an adaptation to resist parasites (a review).
Hamilton, W. D. O., Axelrod, R., & Tanese, R. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.9.3566 · Cited by 1,277 · see citing works
Koskella, B. L., & Brockhurst, M. A. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12072 · Cited by 894 · see citing works
Biological and biomedical implications of the co-evolution of pathogens and their hosts
Woolhouse, M. E. J., Webster, J. P., Domingo, E., Charlesworth, B., & Levin, B. R. (2002) · Nature Genetics · doi:10.1038/ng1202-569 · Cited by 869 · see citing works
The fate of competing beneficial mutations in an asexual population
Gerrish, P. J., & Lenski, R. E. (1998) · Genetica · doi:10.1023/a:1017067816551 · Cited by 783 · see citing works
The fate of competing beneficial mutations in an asexual population
Gerrish, P. J., & Lenski, R. E. (1998) · Contemporary issues in genetics and evolution · doi:10.1007/978-94-011-5210-5_12 · Cited by 721 · see citing works
PERSPECTIVE:SIGN EPISTASIS AND GENETIC CONSTRAINT ON EVOLUTIONARY TRAJECTORIES
Weinreich, D. M., Watson, R. A. R., & Chao, L. (2005) · Evolution · doi:10.1554/04-272 · Cited by 640 · see citing works
Negative Epistasis Between Beneficial Mutations in an Evolving Bacterial Population
Khan, A., Dinh, D. M., Schneider, D., Lenski, R. E., & Cooper, T. F. (2011) · Science · doi:10.1126/science.1203801 · Cited by 581 · see citing works
Ryjenkov, D. A., Tarutina, M. G., Moskvin, O. V., & Gomelsky, M. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.5.1792-1798.2005 · Cited by 577 · see citing works
Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage
Bohannan, B. J. M., & Lenski, R. E. (2000) · Ecology Letters · doi:10.1046/j.1461-0248.2000.00161.x · Cited by 560 · see citing works
Antagonistic coevolution accelerates molecular evolution
Paterson, S., Vogwill, T., Buckling, A. G. J., Benmayor, R., Spiers, A. J., Thomson, N. R., Quail, M. A., Smith, F., Walker, D., Libberton, B., et al. (2010) · Nature · doi:10.1038/nature08798 · Cited by 547 · see citing works
The fate of competing beneficial mutations in an asexual population.
Gerrish, P. J., & Lenski, R. E. (1998) · PubMed · Cited by 520 · see citing works
Diminishing Returns Epistasis Among Beneficial Mutations Decelerates Adaptation
Chou, H.-H. D., Chiu, H.-C., Delaney, N. F., Segrè, D., & Marx, C. J. (2011) · Science · doi:10.1126/science.1203799 · Cited by 510 · see citing works
Determining Mutation Rates in Bacterial Populations
Rosche, W. A., & Foster, P. L. (2000) · Methods · doi:10.1006/meth.1999.0901 · Cited by 482 · see citing works
Running with the Red Queen: Host-Parasite Coevolution Selects for Biparental Sex
Morran, L. T., Schmidt, O. G., Gelarden, I. A., Parrish, R. C., & Lively, C. M. (2011) · Science · doi:10.1126/science.1206360 · Cited by 434 · see citing works
Hall, B. M., Ma, C.-X., Liang, P., & Singh, K. K. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp253 · Cited by 375 · cited 2× · see citing works
“Mutation rate, as indicated, is displayed per 107 mutations/generation (Hall et al. 2009).”
BackgroundMethodThe role of parasites in sympatric and allopatric host diversification
Buckling, A. G. J., & Rainey, P. B. (2002) · Nature · doi:10.1038/nature01164 · Cited by 351 · see citing works
Coevolution with viruses drives the evolution of bacterial mutation rates
Pál, C., Macia, M. D., Oliver, A., Schachar, I. H., & Buckling, A. G. J. (2007) · Nature · doi:10.1038/nature06350 · Cited by 324 · see citing works
Natural Selection Drives Extremely Rapid Evolution in Antiviral RNAi Genes
Obbard, D. J., Jiggins, F. M., Halligan, D. L., & Little, T. J. (2006) · Current Biology · doi:10.1016/j.cub.2006.01.065 · Cited by 311 · see citing works
Host-parasite coevolutionary arms races give way to fluctuating selection
Hall, A. R., Scanlan, P. D., Morgan, A. D., & Buckling, A. G. J. (2011) · Ecology Letters · doi:10.1111/j.1461-0248.2011.01624.x · Cited by 307 · see citing works
The Phage Therapy Paradigm: Prêt-à-Porter or Sur-mesure?
Pirnay, J., Vos, D. D., Verbeken, G., Merabishvili, M., Чанішвілі, Н., Vaneechoutte, M., Zizi, M., Laire, G., Lavigne, R., Huys, I., et al. (2010) · Pharmaceutical Research · doi:10.1007/s11095-010-0313-5 · Cited by 298 · see citing works
Zapala, M. A., & Schork, N. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609333103 · Cited by 292 · see citing works
Maisnier‐Patin, S., & Andersson, D. I. (2004) · Research in Microbiology · doi:10.1016/j.resmic.2004.01.019 · Cited by 259 · see citing works
Lenski, R. E. (1988) · Evolution · doi:10.1111/j.1558-5646.1988.tb04149.x · Cited by 258 · see citing works
Evolutionary Genetics of the Major Histocompatibility Complex
Hedrick, P. W. (1994) · The American Naturalist · doi:10.1086/285643 · Cited by 247 · see citing works
Diverse virulence traits underlying different clinical outcomes of Salmonella infection
Fierer, J., & Guiney, D. G. (2001) · Journal of Clinical Investigation · doi:10.1172/jci12561 · Cited by 245 · see citing works
Tamaki, S., Sato, T., & Matsuhashi, M. (1971) · Journal of Bacteriology · doi:10.1128/jb.105.3.968-975.1971 · Cited by 230 · see citing works
Coevolution: The Geographic Mosaic of Coevolutionary Arms Races
Thompson, J. N. (2005) · Current Biology · doi:10.1016/j.cub.2005.11.046 · Cited by 218 · see citing works
Rapid diversification of coevolving marine Synechococcus and a virus
Marston, M. F., Pierciey, F. J., Shepard, A., Gearin, G., Qi, J., Yandava, C., Schuster, S. C., Henn, M. R., & Martiny, J. B. H. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1120310109 · Cited by 204 · see citing works
Genomewide screens for Escherichia coli genes affecting growth of T7 bacteriophage
Qimron, U., Marintcheva, B., Tabor, S., & Richardson, C. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609428103 · Cited by 201 · see citing works
Molecular evolution as predicted by natural selection
Valen, L. M. V. (1974) · Journal of Molecular Evolution · doi:10.1007/bf01796554 · Cited by 165 · see citing works
Michael R. Davis, Jr., & Goldberg, J. B. (2012) · Journal of Visualized Experiments · doi:10.3791/3916 · Cited by 163 · see citing works
Lenski, R. E. (1988) · Evolution · doi:10.2307/2409028 · Cited by 153 · see citing works
The effect of spatial heterogeneity and parasites on the evolution of host diversity
Brockhurst, M. A., Rainey, P. B., & Buckling, A. G. J. (2004) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2003.2556 · Cited by 151 · see citing works
Garrett, E. S., Perlegas, D., & Wozniak, D. J. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.23.7401-7404.1999 · Cited by 144 · see citing works
Epistasis and Allele Specificity in the Emergence of a Stable Polymorphism in Escherichia coli
Plucain, J., Hindré, T., Gac, M. L., Tenaillon, O., Cruveiller, S., Médigue, C., Leiby, N., Harcombe, W. R., Marx, C. J., Lenski, R. E., et al. (2014) · Science · doi:10.1126/science.1248688 · Cited by 128 · see citing works
Bacteria‐Phage Coevolution and the Emergence of Generalist Pathogens
Hall, A. R., Scanlan, P. D., & Buckling, A. (2010) · The American Naturalist · doi:10.1086/657441 · Cited by 126 · see citing works
Septal Localization of FtsQ, an Essential Cell Division Protein in Escherichia coli
Chen Joseph, C., Weiss, D. S., Ghigo, J., & Beckwith, J. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.2.521-530.1999 · Cited by 126 · see citing works
Chromosomal DNA deletion confers phage resistance to Pseudomonas aeruginosa
Le, S., Yao, X., Lu, S., Tan, Y., Rao, X., Li, M., Jin, X., Wang, J., Zhao, Y., Wu, N. C., et al. (2014) · Scientific Reports · doi:10.1038/srep04738 · Cited by 115 · see citing works
Co-evolution with lytic phage selects for the mucoid phenotype of Pseudomonas fluorescens SBW25
Scanlan, P. D., & Buckling, A. G. J. (2011) · The ISME Journal · doi:10.1038/ismej.2011.174 · Cited by 114 · see citing works
Quantifying Fitness and Gene Stability in Microorganisms
Lenski, R. E. (1991) · Elsevier eBooks · doi:10.1016/b978-0-409-90199-3.50015-2 · Cited by 112 · see citing works
Genetic basis of infectivity evolution in a bacteriophage
Scanlan, P. D., Hall, A. R., LOPEZ‐PASCUA, L. D. C., & Buckling, A. G. J. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2010.04903.x · Cited by 107 · see citing works
Antagonistic coevolution with parasites increases the cost of host deleterious mutations
Buckling, A. G. J., Wei, Y., Massey, R. C., Brockhurst, M. A., & Hochberg, M. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2005.3279 · Cited by 107 · see citing works
Schurr, M. J., Yu, H. D., Boucher, J. C., Hibler, N. S., & Deretic, V. P. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.19.5670-5679.1995 · Cited by 105 · see citing works
The Coupon Collector and the Suppressor Mutation
Poon, A. F. Y., Davis, B., & Chao, L. (2005) · Genetics · doi:10.1534/genetics.104.037259 · Cited by 99 · see citing works
Banemann, A., Deppisch, H., & Gross, R. (1998) · Infection and Immunity · doi:10.1128/iai.66.12.5607-5612.1998 · Cited by 97 · see citing works
Franco, A. V., Liu, D., & Reeves, P. R. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.10.2670-2675.1998 · Cited by 96 · see citing works
Evolution of Pseudomonas aeruginosa Virulence as a Result of Phage Predation
Hosseinidoust, Z., van de Ven, T. G. M., & Tufenkji, N. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.01421-13 · Cited by 71 · see citing works
Meyer, J. R., Agrawal, A. A., Quick, R. T., Dobias, D. T., Schneider, D., & Lenski, R. E. (2010) · Evolution · doi:10.1111/j.1558-5646.2010.01049.x · Cited by 63 · see citing works
Zhang, Q., & Buckling, A. (2011) · Ecology Letters · doi:10.1111/j.1461-0248.2010.01586.x · Cited by 60 · see citing works
Lasocki, K., Bartosik, A. A., Mierzejewska, J., Thomas, C. M., & Jagura‐Burdzy, G. (2007) · Journal of Bacteriology · doi:10.1128/jb.00371-07 · Cited by 60 · see citing works
Selection on non‐social traits limits the invasion of social cheats
Morgan, A. D., Quigley, B. J. Z., Brown, S. P., & Buckling, A. G. J. (2012) · Ecology Letters · doi:10.1111/j.1461-0248.2012.01805.x · Cited by 59 · see citing works
Kashiwagi, A., & Yomo, T. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002188 · Cited by 54 · see citing works
Wang, Y., Xu, J., Chen, A., Wang, Y., Zhu, J., Yu, G., Xu, L., & Luo, L. (2010) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmq034 · Cited by 33 · see citing works
Davis, M. R., & Goldberg, J. B. (2012) · Journal of Visualized Experiments · doi:10.3791/3916-v · Cited by 31 · see citing works
Czyż, A., Zielke, R. A., & Węgrzyn, G. (2001) · Archives of Virology · doi:10.1007/s007050170073 · Cited by 10 · see citing works
Flagged first, then by citations
2 of the 66 references couldn’t be matched to a known paper.
Cited by
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Oechslin, F., Piccardi, P., Mancini, S., Gabard, J., Moreillon, P., Entenza, J. M., Resch, G., & Que, Y. (2016) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiw632 · Cited by 327 · see citing works
Pleiotropy complicates a trade-off between phage resistance and antibiotic resistance
Burmeister, A. R., Fortier, A. V., Roush, C., Lessing, A. J., Bender, R. G., Barahman, R., Grant, R. S., Chan, B. K., & Turner, P. E. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1919888117 · Cited by 288 · see citing works
The Human Gut Phage Community and Its Implications for Health and Disease
Manrique, P., Dills, M., & Young, M. (2017) · Viruses · doi:10.3390/v9060141 · Cited by 253 · see citing works
Framing the Future with Bacteriophages in Agriculture
Svircev, A. M., Roach, D. R., & Castle, A. J. (2018) · Viruses · doi:10.3390/v10050218 · Cited by 252 · see citing works
Evolutionary Ecology of Prokaryotic Immune Mechanisms
van Houte, S., Buckling, A., & Westra, E. R. (2016) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00011-16 · Cited by 243 · see citing works
The Significance of Mutualistic Phages for Bacterial Ecology and Evolution
Obeng, N., Pratama, A. A., & van Elsas, J. D. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2015.12.009 · Cited by 209 · see citing works
Pseudomonas predators: understanding and exploiting phage–host interactions
Smet, J. D., Hendrix, H., Blasdel, B. G., Danis-Wlodarczyk, K. M., & Lavigne, R. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.61 · Cited by 202 · see citing works
Experimental Design, Population Dynamics, and Diversity in Microbial Experimental Evolution
den Bergh, B. V., Swings, T., Fauvart, M., & Michiels, J. J. (2018) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00008-18 · Cited by 180 · see citing works
Microbial Experimental Evolution – a proving ground for evolutionary theory and a tool for discovery
McDonald, M. J. (2019) · EMBO Reports · doi:10.15252/embr.201846992 · Cited by 165 · see citing works
Huang, D., Yu, P., Ye, M., Schwarz, C., Jiang, X., & Alvarez, P. J. J. (2021) · Microbiome · doi:10.1186/s40168-021-01074-1 · Cited by 167 · see citing works
Resistance Evolution against Phage Combinations Depends on the Timing and Order of Exposure
Wright, R. C. T., Friman, V., Smith, M. C. M., & Brockhurst, M. A. (2019) · mBio · doi:10.1128/mbio.01652-19 · Cited by 152 · see citing works
Hasan, M., & Ahn, J. (2022) · Antibiotics · doi:10.3390/antibiotics11070915 · Cited by 144 · see citing works
Cross-resistance is modular in bacteria–phage interactions
Wright, R. C. T., Friman, V., Smith, M. C. M., & Brockhurst, M. A. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2006057 · Cited by 139 · see citing works
rSalvador: An R Package for the Fluctuation Experiment
Zheng, Q. (2017) · G3 Genes|Genomes|Genetics · doi:10.1534/g3.117.300120 · Cited by 98 · see citing works
“The traditional fi tness assay (also known as the competition assay) is a more ef fi cient tool, which has been increasingly conducted in tandem with fl uctuation assays in recent studies (Scanlan et al. 2015).”
MethodScanlan, P. D. (2017) · Trends in Microbiology · doi:10.1016/j.tim.2017.02.012 · Cited by 115 · see citing works
Hesse, S. E., & Adhya, S. L. (2019) · Annual Review of Microbiology · doi:10.1146/annurev-micro-090817-062535 · Cited by 110 · see citing works
Friman, V., Soanes‐Brown, D., Sierocinski, P., Molin, S., Johansen, H. K., Merabishvili, M., Pirnay, J., Vos, D. D., & Buckling, A. G. J. (2015) · Journal of Evolutionary Biology · doi:10.1111/jeb.12774 · Cited by 106 · see citing works
Effects of single and combined use of bacteriophages and antibiotics to inactivate Escherichia coli
Valério, N., Oliveira, C., Jesus, V. I. R., Branco, T. M., Pereira, C., Moreirinha, C., & Almeida, A. (2017) · Virus Research · doi:10.1016/j.virusres.2017.07.015 · Cited by 105 · see citing works
Majkowska-Skrobek, G., Markwitz, P., Sosnowska, E., Lood, C., Lavigne, R., & Drulis‐Kawa, Z. (2021) · Environmental Microbiology · doi:10.1111/1462-2920.15476 · Cited by 92 · see citing works
Functions of the Microbiota for the Physiology of Animal Metaorganisms
Esser, D., Lange, J., Μαρίνος, Γ., Sieber, M., Best, L., Prasse, D., Bathia, J., Rühlemann, M. C., Boersch, K., Jaspers, C., et al. (2018) · Journal of Innate Immunity · doi:10.1159/000495115 · Cited by 90 · see citing works
Recent progress toward the implementation of phage therapy in Western medicine
Pirnay, J., Ferry, T., & Resch, G. (2021) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuab040 · Cited by 87 · see citing works
Gómez, P., Paterson, S., Meester, L. D., Liu, X., Lenzi, L., Sharma, M. D., McElroy, K., & Buckling, A. G. J. (2016) · Nature Communications · doi:10.1038/ncomms12453 · Cited by 82 · see citing works
Sequential Combined Effect of Phages and Antibiotics on the Inactivation of Escherichia coli
Lopes, A. S., Pereira, C., & Almeida, A. (2018) · Microorganisms · doi:10.3390/microorganisms6040125 · Cited by 81 · see citing works
Competitive species interactions constrain abiotic adaptation in a bacterial soil community
Hall, J. P. J., Harrison, E., & Brockhurst, M. A. (2018) · Evolution Letters · doi:10.1002/evl3.83 · Cited by 79 · see citing works
Yoshimura, D., Kajitani, R., Gotoh, Y., Katahira, K., Okuno, M., Ogura, Y., Hayashi, T., & Itoh, T. (2019) · Microbial Genomics · doi:10.1099/mgen.0.000261 · Cited by 71 · see citing works
Bonilla‐Rosso, G., Steiner, T., Wichmann, F., Bexkens, E., & Engel, P. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2000228117 · Cited by 68 · see citing works
The interaction of phages and bacteria: the co-evolutionary arms race
Safari, F., Sharifi, M., Farajnia, S., Akbari, B., Ahmadi, M. K. B., Negahdaripour, M., & Ghasemi, Y. (2019) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2019.1674774 · Cited by 69 · see citing works
Multistep diversification in spatiotemporal bacterial-phage coevolution
Tamar, E. S., & Kishony, R. (2022) · Nature Communications · doi:10.1038/s41467-022-35351-w · Cited by 68 · see citing works
Latino, L., Midoux, C., Hauck, Y., Vergnaud, G., & Pourcel, C. (2016) · Microbiology · doi:10.1099/mic.0.000263 · Cited by 68 · see citing works
Parasites and competitors suppress bacterial pathogen synergistically due to evolutionary trade-offs
Wang, X., Wei, Z., Li, M., Wang, X., Shan, A., Mei, X., Jousset, A., Shen, Q., Xu, Y., & Friman, V. (2016) · Evolution · doi:10.1111/evo.13143 · Cited by 56 · see citing works
Microbial evolution and ecological opportunity in the gut environment
Scanlan, P. D. (2019) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.1964 · Cited by 54 · see citing works
A role for bacterial experimental evolution in coral bleaching mitigation?
Maire, J., & van Oppen, M. J. H. (2021) · Trends in Microbiology · doi:10.1016/j.tim.2021.07.006 · Cited by 54 · see citing works
Scanlan, P. D., Buckling, A. G. J., & Hall, A. R. (2015) · Bacteriophage · doi:10.1080/21597081.2015.1050153 · Cited by 54 · see citing works
Barceló, C. T., Franzon, B., Vasse, M., & Hochberg, M. (2016) · Evolutionary Applications · doi:10.1111/eva.12364 · Cited by 54 · see citing works
Core Genes Evolve Rapidly in the Long-Term Evolution Experiment with Escherichia coli
Maddamsetti, R., Hatcher, P. J., Green, A. G., Williams, B. L., Marks, D. S., & Lenski, R. E. (2017) · Genome Biology and Evolution · doi:10.1093/gbe/evx064 · Cited by 53 · see citing works
Coevolutionary dynamics shape the structure of bacteria‐phage infection networks
Fortuna, M. A., Barbour, M. A., Zaman, L., Hall, A. R., Buckling, A. G. J., & Bascompte, J. (2019) · Evolution · doi:10.1111/evo.13731 · Cited by 52 · see citing works
Braga, L. P. P., Soucy, S. M., Amgarten, D., da Silva, A. M., & Setúbal, J. C. (2018) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2018.00006 · Cited by 49 · see citing works
A phage tail–like bacteriocin suppresses competitors in metapopulations of pathogenic bacteria
Backman, T., Latorre, S. M., Symeonidi, E., Muszyński, A., Bleak, E., Eads, L., Martinez-Koury, P. I., Som, S., Hawks, A., Gloss, A. D., et al. (2024) · Science · doi:10.1126/science.ado0713 · Cited by 48 · see citing works
Dissecting the genetic architecture of a stepwise infection process
Hall, M. D., Routtu, J., & Ebert, D. (2019) · Molecular Ecology · doi:10.1111/mec.15166 · Cited by 46 · see citing works
Sublethal streptomycin concentrations and lytic bacteriophage together promote resistance evolution
Cairns, J., Becks, L., Jalasvuori, M., & Hiltunen, T. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0040 · Cited by 46 · see citing works
Network structure and local adaptation in co‐evolving bacteria–phage interactions
Gurney, J., Aldakak, L., Betts, A., Gougat‐Barbera, C., Poisot, T., Kaltz, O., & Hochberg, M. (2017) · Molecular Ecology · doi:10.1111/mec.14008 · Cited by 43 · see citing works
Genetic hurdles limit the arms race betweenProchlorococcusand the T7-like podoviruses infecting them
Schwartz, D. A., & Lindell, D. (2017) · The ISME Journal · doi:10.1038/ismej.2017.47 · Cited by 42 · see citing works
Näpflin, K., O'Connor, E., Becks, L., Bensch, S., Ellis, V. A., Hafer-Hahmann, N., Harding, K., Lindén, S. K., Olsen, M. T., Roved, J., et al. (2019) · PeerJ · doi:10.7717/peerj.8013 · Cited by 30 · see citing works
How to Train Your Phage: The Recent Efforts in Phage Training
Abdelsattar, A. S., Dawoud, A., Rezk, N., Makky, S., Safwat, A., Richards, P., & El‐Shibiny, A. (2021) · Biologics · doi:10.3390/biologics1020005 · Cited by 42 · see citing works
Ecological conditions determine extinction risk in co-evolving bacteria-phage populations
Wright, R. C. T., Brockhurst, M. A., & Harrison, E. (2016) · BMC Evolutionary Biology · doi:10.1186/s12862-016-0808-8 · Cited by 41 · see citing works
Zhao, X., Buckling, A. G. J., Zhang, Q., & Hesse, E. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2018.0007 · Cited by 36 · see citing works
Bacteriocins and the assembly of natural Pseudomonas fluorescens populations
Bruce, J. B., West, S. A., & Griffin, A. S. (2016) · Journal of Evolutionary Biology · doi:10.1111/jeb.13010 · Cited by 35 · see citing works
Mutalik, V. K., & Arkin, A. P. (2022) · iScience · doi:10.1016/j.isci.2022.104121 · Cited by 32 · see citing works
A new practical guide to the Luria–Delbrück protocol
Zheng, Q. (2015) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2015.08.005 · Cited by 34 · see citing works
Adaptation to Parasites and Costs of Parasite Resistance in Mutator and Nonmutator Bacteria
Wielgoss, S., Bergmiller, T., Bischofberger, A. M., & Hall, A. R. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv270 · Cited by 33 · see citing works
Resistance gained, resistance lost: An explanation for host–parasite coexistence
Koskella, B. L. (2018) · PLoS Biology · doi:10.1371/journal.pbio.3000013 · Cited by 31 · see citing works
Evolutionary contribution to coexistence of competitors in microbial food webs
Hiltunen, T., Kaitala, V., Laakso, J., & Becks, L. (2017) · Proceedings of the Royal Society of London. Biological Sciences · doi:10.1098/rspb.2017.0415 · Cited by 32 · see citing works
Smith, C. H., Pfeiffer, J. M., & Johnson, N. A. (2020) · Cladistics · doi:10.1111/cla.12423 · Cited by 26 · see citing works
Host Resistance, Genomics and Population Dynamics in a Salmonella Enteritidis and Phage System
Holguín, A. V., Cárdenas, P., Prada-Peñaranda, C., Leite, L. R., Buitrago, C. A., Clavijo, V., Oliveira, G., Leekitcharoenphon, P., Aarestrup, F. M., & Vives, M. J. (2019) · Viruses · doi:10.3390/v11020188 · Cited by 26 · see citing works
Experimental evolution can unravel the complex causes of natural selection in clinical infections
Brockhurst, M. A. (2015) · Microbiology · doi:10.1099/mic.0.000107 · Cited by 25 · see citing works
Harrison, E., Hall, J. P. J., Paterson, S., Spiers, A. J., & Brockhurst, M. A. (2017) · Molecular Ecology · doi:10.1111/mec.14080 · Cited by 25 · see citing works
Scanlan, J., Hall, A. R., & Scanlan, P. D. (2019) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2019.05.021 · Cited by 25 · see citing works
Genomic evolution of bacterial populations under coselection by antibiotics and phage
Cairns, J., Frickel, J., Jalasvuori, M., Hiltunen, T., & Becks, L. (2016) · Molecular Ecology · doi:10.1111/mec.13950 · Cited by 25 · see citing works
McClean, D., Friman, V., Finn, A., Salzberg, L. I., & Donohue, I. (2019) · Oikos · doi:10.1111/oik.06586 · Cited by 24 · see citing works
Quinn, A., Bottery, M. J., Thompson, H., & Friman, V. (2022) · The ISME Journal · doi:10.1038/s41396-022-01285-w · Cited by 25 · see citing works
Plasmid carriage can limit bacteria–phage coevolution
Harrison, E., Truman, J., Wright, R. C. T., Spiers, A. J., Paterson, S., & Brockhurst, M. A. (2015) · Biology Letters · doi:10.1098/rsbl.2015.0361 · Cited by 23 · see citing works
Phage resistance-mediated trade-offs with antibiotic resistance in Salmonella Typhimurium
Laure, N. N., & Ahn, J. (2022) · Microbial Pathogenesis · doi:10.1016/j.micpath.2022.105732 · Cited by 22 · see citing works
Klimenko, A. I., Matushkin, Y. G., Kolchanov, N. A., & Lashin, S. A. (2016) · BMC Microbiology · doi:10.1186/s12866-015-0620-4 · Cited by 22 · see citing works
Genotype‐by‐genotype interactions between an insect and its pathogen
Hudson, A. I., Fleming-Davies, A. E., Páez, D. J., & Dwyer, G. (2016) · Journal of Evolutionary Biology · doi:10.1111/jeb.12977 · Cited by 22 · see citing works
Xu, Z., Ding, Z., Shi, L., Xie, Y., Zhang, Y., Wang, Z., & Liu, Q. (2023) · The ISME Journal · doi:10.1038/s41396-023-01529-3 · Cited by 21 · see citing works
Zhao, Y., Shu, M., Zhang, L., Zhong, C., Liao, N., & Wu, G. (2024) · ISME Communications · doi:10.1093/ismeco/ycae039 · Cited by 20 · see citing works
Halawa, E. M. (2023) · Journal of Genetic Engineering and Biotechnology · doi:10.1186/s43141-023-00549-y · Cited by 19 · see citing works
Multiyear Time-Shift Study of Bacteria and Phage Dynamics in the Phyllosphere
Dewald-Wang, E. A., Parr, N., Tiley, K., Lee, A., & Koskella, B. L. (2021) · The American Naturalist · doi:10.1086/717181 · Cited by 19 · see citing works
Bischofberger, A. M., Pfrunder‐Cardozo, K. R., Baumgartner, M., & Hall, A. R. (2021) · Evolutionary Applications · doi:10.1111/eva.13200 · Cited by 17 · see citing works
Long-read powered viral metagenomics in the oligotrophic Sargasso Sea
Warwick-Dugdale, J., Tian, F., Michelsen, M. L., Cronin, D. R., Moore, K., Farbos, A., Chittick, L., Bell, A. G., Zayed, A. A., Buchholz, H. H., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-48300-6 · Cited by 15 · see citing works
Baumgartner, M., Roffler, S., Wicker, T., & Pernthaler, J. (2017) · The ISME Journal · doi:10.1038/ismej.2017.87 · Cited by 15 · see citing works
Parasite host range and the evolution of host resistance
Gorter, F. A., Hall, A. R., Buckling, A. G. J., & Scanlan, P. D. (2015) · Journal of Evolutionary Biology · doi:10.1111/jeb.12639 · Cited by 13 · see citing works
Resource‐dependent antagonistic coevolution leads to a new paradox of enrichment
Zhang, Q., & Buckling, A. G. J. (2016) · Ecology · doi:10.1890/15-1408.1 · Cited by 12 · see citing works
Baumgartner, M., Neu, T. R., Blom, J. F., & Pernthaler, J. (2016) · Journal of Evolutionary Biology · doi:10.1111/jeb.12957 · Cited by 11 · see citing works
Parasite genetic distance and local adaptation in co‐evolving bacteria–bacteriophage populations
Scanlan, P. D., Hall, A. R., & Buckling, A. G. J. (2016) · Molecular Ecology · doi:10.1111/mec.13897 · Cited by 9 · see citing works
Jia, R. F., Xiao, C., Zhang, Y., Hu, L.-Y., Jun-jun, Y., Zuo, R., Hu, Y., Xie, Y.-H., Ma, X., Li, Q., et al. (2025) · Drug Resistance Updates · doi:10.1016/j.drup.2025.101311 · Cited by 8 · see citing works
Hidden paths to endless forms most wonderful: parasite-blind diversification of host quality
Freund, L., Vasse, M., & Velicer, G. J. (2021) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2021.0456 · Cited by 7 · see citing works
Ecological partitioning enables phage–antibiotic cooperation in a human Pseudomonas infection
Luong, T., Kharrat, L., Champagne-Jorgensen, K. P., Melendez, J. A., Pride, D. T., Conrad, D. J., & Roach, D. R. (2026) · Nature Communications · doi:10.1038/s41467-026-69247-w · Cited by 9 · see citing works
Dip-a-Dee-Doo-Dah: Bacteriophage-Mediated Rescoring of a Harmoniously Orchestrated RNA Metabolism
Dendooven, T., & Lavigne, R. (2019) · Annual Review of Virology · doi:10.1146/annurev-virology-092818-015644 · Cited by 7 · see citing works
Localised genetic heterogeneity provides a novel mode of evolution in dsDNA phages
Magill, D., Kucher, P. A., Krylov, V. N., Pleteneva, E. A., Quinn, J. P., & Kulakov, L. A. (2017) · Scientific Reports · doi:10.1038/s41598-017-14285-0 · Cited by 7 · see citing works
Zhou, W., Li, Y., Li, Z., Ma, B., Jiang, X., Hu, C., Ai, Y., & Luo, P. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.710262 · Cited by 5 · see citing works
Fight Not Flight: Parasites Drive the Bacterial Evolution of Resistance, Not Escape
Blazanin, M., Moore, J. P., Olsen, S., & Travisano, M. (2024) · The American Naturalist · doi:10.1086/733414 · Cited by 5 · see citing works
Burmeister, A. R., Bender, R. G., Fortier, A. V., Lessing, A. J., Chan, B. K., & Turner, P. E. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/397695 · Cited by 5 · see citing works
Synergistic coevolution accelerates genome evolutionPreprint
Preußger, D., Herbig, A., & Kost, C. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.19.444833 · Cited by 5 · see citing works
Phylogeny-agnostic strain-level prediction of phage-host interactions from genomesPreprint
Noonan, A. J. C., Morinière, L., Rivera-Lopez, E. O., Patel, K., Pena, M., Svab, M., Kazakov, A. E., Deutschbauer, A. M., Dudley, E. G., Mutalik, V. K., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.15.688630 · Cited by 5 · see citing works
Ambutsi, M., Reva, O., & OKOTH, P. K. (2021) · Scientific African · doi:10.1016/j.sciaf.2021.e00910 · Cited by 4 · see citing works
Molecular Detection and Identification of Pathogens, Pathotypes, and Genes
Saharan, G. S., Mehta, N. K., & Meena, P. D. (2023) · Springer eBooks · doi:10.1007/978-981-19-3812-2_4 · Cited by 4 · see citing works
Source-sink migration of natural enemies drives maladaptation of victim populations in sink habitats
Chu, X., Buckling, A. G. J., & Zhang, Q. (2023) · Evolution · doi:10.1093/evolut/qpad099 · Cited by 2 · see citing works
Deery, J., Carmody, M., Flavin, R., Tomanek, M., O'Keeffe, M., McGlacken, G. P., & Reen, F. J. (2024) · Microbial Genomics · doi:10.1099/mgen.0.001205 · Cited by 2 · see citing works
Phage therapy for One Health approach: current status, challenges and opportunities
Wei, Z., Wang, X., Ma, Y., Mao, Y. E., Xu, Y., Shen, Q., & Zhu, Y. (2022) · Scientia Sinica Vitae · doi:10.1360/ssv-2021-0402 · Cited by 2 · see citing works
Lew, B. Y. X., Njondimackal, N. L., Ravisankar, V., & Ayuni, N. N. (2023) · Springer eBooks · doi:10.1007/978-981-99-8369-8_24 · Cited by 2 · see citing works
Pleiotropic Costs of Phage Resistance
Abedon, S. T. (2022) · Springer eBooks · doi:10.1007/978-3-030-94309-7_22 · Cited by 2 · see citing works
Chen, L., Middelboe, M., & Svenningsen, S. L. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.12.28.630609 · Cited by 2 · see citing works
Noonan, A. J. C., Morinière, L., Rivera-Lopez, E. O., Patel, K., Pena, M., Svab, M., Kazakov, A. E., Deutschbauer, A. M., Dudley, E. G., Mutalik, V. K., et al. (2026) · Nature Microbiology · doi:10.1038/s41564-026-02482-5 · Cited by 1 · see citing works
Biofilm and Chronic Typhoid Carriers with Special Reference to Bacteriophage Therapy
Nath, G., Yadav, V. B., & Singh, S. K. (2022) · JOURNAL OF GASTROINTESTINAL INFECTIONS · doi:10.5005/jp-journals-10068-3053 · Cited by 1 · see citing works
Prokaryotic Viruses: Intriguing Players in the Aquatic Realm
Schweichhart, J. S. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819166-8.00106-7 · Cited by 1 · see citing works
Chu, X., Buckling, A. G. J., & Zhang, Q. (2022) · doi:10.22541/au.165123938.89441744/v1 · Cited by 1 · see citing works
Lungu, T. S., Badruna, L., & Rendueles, O. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.17.694638 · Cited by 1 · see citing works
Molecular basis of cyanphage resistance in marine Synechococcus
Perez-Sepulveda, B. M. (2015)
Understanding the structure and dynamics of bacteria-phage infection networks
Wright, R. C. T. (2018) · White Rose eTheses Online (University of Leeds, The University of Sheffield, University of York)
- Authors
- Scanlan, P. D., Hall, A. R., Blackshields, G., Friman, V.-P., Davis, M. R., Goldberg, J. B., & Buckling, A.
- Affiliations
- University of Oxford (GB)
- Trinity College Dublin (IE)
- University of Virginia Health System (US)
- Corresponding author
- Scanlan, Pauline D.
- ORCID
- Venue
- Molecular Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2015-02-12
- Volume
- 32
- Issue
- 6
- Pages
- 1425-1435
- ISSN
- 0737-4038 (ISSN-L)
- 1537-1719
- PMC
- PMC6281048
- OpenAlex
- W2156066664
- Cited by
- 111
- References
- 66
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 7 · 2023: 5 · 2022: 9 · 2021: 14 · 2020: 3 · 2019: 13 · 2018: 13 · 2017: 12 · 2016: 17 · 2015: 9
- FWCI
- 11.62
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Molecular Biology and Evolution (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Open Research Exeter (University of Exeter) (acceptedVersion)
- Figshare (submittedVersion)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, other-oa)
- ETH Zürich Research Collection
- Funders
- Natural Environment Research Council (NE/J021806/1)
- National Institute of Allergy and Infectious Diseases (T32AI007046)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Physical Sciences › Environmental Science › Ecology › Bacteriophages and microbial interactions
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- host-parasite coevolution, phage resistance, Pseudomonas fluorescens SBW25, lipopolysaccharide, epistasis, negative epistasis, mutation rate evolution, competitive fitness, evolvability
- MeSH terms
- DNA, Bacterial, DNA, Viral, Genotype, Phenotype, Pseudomonas fluorescens, Genetic Variation, Genome, Bacterial, Pseudomonas Phages, Sequence Analysis, DNA, Evolution, Molecular, Genetic Association Studies
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