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Bacteriophage experimental evolution/Bibliography

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A list of key readings about Bacteriophage experimental evolution.
Please sort and annotate in a user-friendly manner. For formatting, consider using automated reference wikification.


Laboratory phylogenetics

  • Hahn, M. W., M. D. Rausher, and C. W. Cunningham, 2002. Distinguishing between selection and population expansion in an experimental lineage of bacteriophage T7. Genetics 161:11-20.
  • Oakley, T. H., and C. W. Cunningham, 2000. Independent contrasts succeed where ancestor reconstruction fails in a known bacteriophage phylogeny. Evolution 54:397-405.
  • Cunningham, C.W., K. Jeng, J. Husti, M. Badgett, I.J. Molineux, D.M. Hillis and J.J. Bull, 1997. Parallel molecular evolution of deletions and nonsense mutations in bacteriophage T7. Mol. Biol. Evol. 14:113-116.
  • Bull, J. J., C. W. Cunningham, I. J. Molineux, M. R. Badgett, and D. M. Hills, 1993. Experimental molecular evolution of bacteriophage T7. Evolution 47:993-1007.
  • Hillis, D.M., J.J. Bull, M.E. White, M.R. Badgett and I.J. Molineux, 1992. Experimental phylogenetics: generation of a known phylogeny. Science. 255:589-592.
  • Studier, F. W., 1980. The last of the T phages, p. 72-78. In N. H. Horowitz and E. Hutchings, Jr. (eds.), Genes, Cells, and Behavior: A View of Biology Fifty Years Later.
  • Studier, F. W., 1979. Relationships among different strains of T7 and among T7-related bacteriophages. Virology 95:70-84.


  • Burch, C.L., and L. Chao. 2004. Epistasis and its relationships to canalization in the RNA virus _6. Genetics. 167:559-567.
  • You, L., and J. Yin. 2002. Dependence of epistasis on environment and mutation severity as revealed by in silico mutagenesis of phage T7. Genetics. 160:1273-1281.
  • Schuppli, D., J. Georgijevic, and H. Weber. 2000. Synergism of mutations in bacteriophage Q_ RNA affecting host factor dependence of Q_ replicase. J. Mol. Biol. 295:149-154.

The phage literature provides many examples of epistasis which are not studied under the context of experimental evolution nor necessarily described as examples of epistasis.

Experimental adaptation

  • Bull, J. J., J. Millstein, J. Orcutt and H.A. Wichman. 2006. Evolutionary feedback mediated through population density, illustrated with viruses in chemostats. Am. Nat. 167:E39-E51.
  • Bull, J. J., M. R. Badgett, R. Springman, and I. J. Molineux. 2004. Genome properties
  • Bull, J. J., M. R. Badgett, D. Rokyta, and I. J. Molineux. 2003. Experimental evolution yields hundreds of mutations in a functional viral genome. J. Mol. Evol. 57:241-248.
  • Bull, J. J., M.R. Badgett, H.A. Wichman, J.P. Hulsenbeck, D.M. Hillis, A. Gulati, C. Ho and I.J. Molineux. 1997. Exceptional convergent evolution in a virus. Genetics. 147:1497-1507.

The reader should be aware that numerous phage experimental adaptations were performed in the early decades of phage study.

Adaptation to usual hosts.

  • Wichman, H. A., J. Wichman, and J. J. Bull. 2005. Adaptive molecular evolution for 13,000 phage generations: A possible arms race. Genetics 170:19-31.
  • Rokyta, D., M. R. Badgett, I. J. Molineux, and J. J. Bull. 2002. Experimental genomic evolution: extensive compensation for loss of DNA ligase activity in a virus. Mol. Biol. Evol. 19:230-238.
  • Burch, C. L., and L. Chao. 2000. Evolvability of an RNA virus is determined by its mutational neighbourhood. Nature 406:625-628.
  • Wichman, H. A., L. A. Scott, C. D. Yarber, and J. J. Bull. 2000. Experimental evolution
  • Wichman, H. A., M. R. Badgett, L. A. Scott, C. M. Boulianne, and J. J. Bull. 1999. Different trajectories of parallel evolution during viral adaptation. Science 285:422-424.

Adaptation to new or modified hosts.

  • Duffy, S., P. E. Turner, and C. L. Burch. 2006. Pleiotropic Costs of Niche Expansion in the RNA Bacteriophage _6. Genetics 172:751-757.
  • Pepin, K. M., M. A. Samuel, and H. A. Wichman. 2006. Variable Pleiotropic Effects From Mutations at the Same Locus Hamper Prediction of Fitness From a Fitness Component. Genetics 172:2047-2056.
  • Crill, W. D., H. A. Wichman, and J. J. Bull. 2000. Evolutionary reversals during viral adaptation to alternating hosts. Genetics 154:27-37.
  • Bull, J. J., A. Jacoboson, M. R. Badgett, and I. J. Molineux. 1998. Viral escape from antisense RNA. Mol. Microbiol. 28:835-846.
  • Hibma, A. M., S. A. Jassim, and M. W. Griffiths. 1997. Infection and removal of L-forms of Listeria monocytogenes with bred bacteriophage. Int. J. Food Microbiol. 34:197-207.
  • Jassim, S. A. A., S. P. Denyer, and G. S. A. B. Stewart. 1995. Virus breeding. International Patent Application. WO 9523848. (under tab labeled "documents")
  • Schuppli, D., G. Miranda, H. C. T. Tsui, M. E. Winkler, J. M. Sogo, and H. Weber. 1997. Altered 3'-terminal RNA structure in phage Q_ adapted to host factor-less Escherichia coli. Proc. Natl. Acad. Sci. USA 94:10239-10242.
  • Hashemolhosseini, S., Z. Holmes, B. Mutschler, and U. Henning. 1994. Alterations of receptor specificities of coliphages of the T2 family. J. Mol. Biol. 240:105-110.

The older phage literature, e.g., pre-1950s, contains numerous examples of phage adaptations to different hosts.

Adaptation to modified conditions

  • Bacher, J. M., J. J. Bull, and A. D. Ellington. 2003. Evolution of phage with chemically ambiguous proteomes. BMC Evol. Biol. 3:24
  • Bull, J. J., A. Jacoboson, M. R. Badgett, and I. J. Molineux. 1998. Viral escape from
  • Merril, C. R., B. Biswas, R. Carlton, N. C. Jensen, G. J. Creed, S. Zullo, and S. Adhya. 1996. Long-circulating bacteriophage as antibacterial agents. Proc. Natl. Acad. Sci. USA 93:3188-3192.
  • Gupta, K., Y. Lee and J. Yin. 1995. Extremo-phage: in vitro selection of tolerance to a hostile environment. J. Mol. Evol. 41:113-114.

The older phage literature, e.g., pre-1950s, also contains examples of phage adaptations to different culture conditions, such as phage T2 adaptation to low salt conditions.

Adaptation to high temperatures.

  • Knies, J.L., R. Izem, K.L. Supler. J.G. Kingsolver, and C.L. Burch. 2006. The genetic basis of thermal reaction norm evolution in lab and natural phage population. PLoS Biology. 4:e201.
  • Poon, A., and L. Chao. 2005. The rate of compensatory mutation in the DNA bacteriophage _X174. Genetics. 170:989-999.
  • Poon, A., and L. Chao. 2004. Drift increases the advantage of sex in RNA bacteriophage _6. Genetics 166:19-24.
  • Holder, K. K., and J. J. Bull. 2001. Profiles of adaptation in two similar viruses. Genetics 159:1393-1404.
  • Bull, J. J., M. R. Badgett, and H. A. Wichman. 2000. Big-benefit mutations in a bacteriophage inhibited with heat. Mol. Biol. Evol. 17:942-950.

Adaptation as compensation for deleterious mutations.

  • Poon, A., and L. Chao. 2005. The rate of compensatory mutation in the DNA bacteriophage _X174. Genetics. 170:989-999.
  • Heineman, R. H., I. J. Molineux, and J. J. Bull. 2005. Evolutionary robustness of an optimal phenotype: re-evolution of lysis in a bacteriophage deleted for its lysin gene. J. Mol. Evol. 61:181-191.
  • Hayashi, Y., H. Sakata, Y. Makino, I. Urabe, and T. Yomo. 2003. Can an arbitrary sequence evolve towards acquiring a biological function? J. Mol. Evol. 56:162-168.
  • Rokyta, D., M. R. Badgett, I. J. Molineux, and J. J. Bull. 2002. Experimental genomic evolution: extensive compensation for loss of DNA ligase activity in a virus. Mol. Biol. Evol. 19:230-238.
  • Burch, C. L., and L. Chao. 1999. Evolution by small steps and rugged landscapes in the RNA virus _6. Genetics 151:921-927.
  • Klovins, J., N. A. Tsareva, M. H. de Smit, V. Berzins, and D. Van. 1997. Rapid evolution of translational control mechanisms in RNA genomes. J. Mol. Biol. 265:372-384. &
  • Olsthoorn, R. C., and J. van Duin. 1996. Evolutionary reconstruction of a hairpin deleted from the genome of an RNA virus. Proc. Natl. Acad. Sci. USA 93:12256-12261.
  • Nelson, M. A., M. Ericson, L. Gold, and J. F. Pulitzer. 1982. The isolation and characterization of TabR bacteria: Hosts that restrict bacteriophage T4 rII mutants Mol. Gen. Genet. 188:60-68.
  • Nelson, M.A. and L. Gold. 1982. The isolation and characterization of bacterial strains (Tab32) that restrict bacteriophage T4 gene 32 mutants Mol. Gen. Genet. 188:69-76.

There are many examples in the early phage literature of phage adapting and compensating for deleterious mutations.

Adaptation as toward change in phage virulence

  • Kerr, B., C. Neuhauser, B. J. M. Bohannan, and A. M. Dean. 2006. Local migration promotes competitive restraint in a host–pathogen 'tragedy of the commons'. Nature 442:75-78.
  • Wang, I.-N. 2006. Lysis timing and bacteriophage fitness. Genetics 172:17-26.
  • Abedon, S. T., P. Hyman, and C. Thomas. 2003. Experimental examination of bacteriophage latent-period evolution as a response to bacterial availability. Appl. Environ. Microbiol. 69:7499-7506.
  • Messenger, S. L., I. J. Molineux, and J. J. Bull. 1999. Virulence evolution in a virus obeys a trade-off. Proc. R. Soc. Lond. B Biol. Sci. 266:397-404.
  • Bull, J. J., and I. J. Molineux. 1992. Molecular genetics of adaptation in an experimental model of cooperation. Evolution 46:882-895.
  • Bull, J. J., I. J. Molineux, and W. R. Rice. 1991. Selection for benevolence in a host-parasite system. Evolution 45:875-882.

The older phage literature contains numerous references to phage virulence, and phage virulence evolution. However, the reader should be warned that virulence is often used as a synonym for "not temperature", a usage which is neither employed here nor to be encouraged generally.

Impact of sex/coinfection

  • Froissart, R., C. O. Wilke, R. Montville, S. K. Remold, L. Chao, and P. E. Turner. 2004. Co-infection weakens selection against epistatic mutations in RNA viruses. Genetics
  • Montville, R., R. Froissart, S. K. Remold, O. Tenaillon, and P. E. Turner. 2005. Evolution of mutational robustness in an RNA virus. PLoS Biology 3:e381
  • Sachs, J.L. and J. J. Bull. 2005. Experimental evolution of conflict mediation between genomes. Proc. Natl. Acad. Sci. 102:390-395.
  • Poon, A., and L. Chao. 2004. Drift increases the advantage of sex in RNA bacteriophage
  • Turner, P. E., and L. Chao. 1998. Sex and the evolution of intrahost competition in RNA virus _6. Genetics 150:523-532.
  • L. Chao, T. T. Tran, and T. T. Tran. 1997. The advantage of sex in the RNA virus _6. Genetics 147:953-959.
  • Malmberg, R. L. 1977. The evolution of epistasis and the advantage of recombination in populations of bacteriophage T4. Genetics 86:607-621.

Muller’s ratchet

  • de la Peña, M., S. F. Elena, and A. Moya. 2000. Effect of deleterious mutation-accumulation on the fitness of RNA bacteriophage MS2. Evolution 54:686-691.
  • L. Chao. 1990. Fitness of RNA virus decreased by Muller's ratchet. Nature 348:454-455.

Prisoner’s dilemma

  • Turner, P. E., and L. Chao. 2003. Escape from Prisoner's Dilemma in RNA phage _phi6. Am. Nat. 161:497-505.
  • Turner, P. E., and L. Chao. 1999. Prisoner's dilemma in an RNA virus. Nature 398:441-443.


  • Buckling, A., Y. Wei, R. C. Massey, M. A. Brockhurst, and M. E. Hochberg. 2006. Antagonistic coevolution with parasites increases the cost of host deleterious mutations. Proc. R. Soc. Lond. B Biol. Sci. 273:45-49.
  • Morgan, A. D., S. Gandon, and A. Buckling. 2005. The effect of migration on local adaptation in a coevolving host-parasite system. Nature 437:253-256.
  • Forde, S. E., J. N. Thompson, and B. J. M. Bohannan. 2004. Adaptation varies through space and time in a coevolving host–parasitoid interaction. Nature 431:841-844.
  • Mizoguchi, K., M. Morita, C. R. Fischer, M. Yoichi, Y. Tanji, and H. Unno. 2003. Coevolution of bacteriophage PP01 and Escherichia coli O157:H7 in continuous culture. Appl. Environ. Microbiol. 69:170-176.
  • Buckling, A., and P. B. Rainey. 2002. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. R. Soc. Lond. B Biol. Sci. 269:931-936.
  • Buckling, A., and P. B. Rainey. 2002. The role of parasites in sympatric and allopatric host diversification. Nature 420:496-499.
  • Lenski, R.E. and B.R. Levin. 1985. Constraints on the coevolution of bacteria and virulent phage – a model, some experiments and predictions for natural communities. Am. Nat. 125:585-602.
  • Chao, L., B.R. Levin, and F.M. Stewart. 1977. A complex community in a simple habitat: an experimental study with bacteria and phage. Ecology. 58:369-378.
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