Bacteria–Virus Coevolution

  • Angus Buckling
  • Michael Brockhurst
Part of the Advances in Experimental Medicine and Biology book series (volume 751)


Phages, viruses of bacteria, are ubiquitous. Many phages require host cell death to successfully complete their life cycle, resulting in reciprocal evolution of bacterial resistance and phage infectivity (antagonistic coevolution). Such coevolution can have profound consequences at all levels of biological organisation. Here, we review genetic and ecological factors that contribute to determining coevolutionary dynamics between bacteria and phages. We also consider some of the consequences of bacteria-phage coevolution, such as determining rates of molecular evolution and structuring communities, and how these in turn feedback into driving coevolutionary dynamics.


Encounter Rate Soil Microcosm CRISPR Locus Phage Population Resistance Range 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We are grateful to our colleagues past and present who we have worked with on these topics. We gratefully acknowledge support from NERC (UK), European Research Council, Wellcome Trust, Royal Society and Leverhulme Trust.


  1. 1.
    Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, ChicagoGoogle Scholar
  2. 2.
    Salathe M, Soyer OS (2008) Parasites lead to evolution of robustness against gene loss in host signaling networks. Mol Syst Biol 4:202PubMedGoogle Scholar
  3. 3.
    Ehrlich PR, Raven PH (1964) Butterflies and plants – a study in coevolution. Evolution 18:586–608Google Scholar
  4. 4.
    Buckling A, Hodgson DJ (2007) Short-term rates of parasite evolution predict the evolution of host diversity. J Evol Biol 20:1682–1688PubMedGoogle Scholar
  5. 5.
    Hamilton WD (1980) Sex versus non-sex versus parasite. OIKOS 35:282–290Google Scholar
  6. 6.
    Pal C, Macia MD, Oliver A, Schachar I, Buckling A (2007) Coevolution with viruses drives the evolution of bacterial mutation rates. Nature 450:1079–1081PubMedGoogle Scholar
  7. 7.
    Fellous S, Quillery E, Duncan AB, Kaltz O (2011) Parasitic infection reduces dispersal of ciliate host. Biol Lett 7:327–329PubMedGoogle Scholar
  8. 8.
    Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology 85:411–426PubMedGoogle Scholar
  9. 9.
    Bull JJ (1994) Perspective – Virulence. Evolution 48:1423–1437Google Scholar
  10. 10.
    Koskella B, Lively CM (2007) Advice of the rose: experimental coevolution of a trematode parasite and its snail host. Evolution 61:152–159PubMedGoogle Scholar
  11. 11.
    Laine AL (2006) Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales. Proc Roy Soc Lond B 273:267–273Google Scholar
  12. 12.
    Morran LT, Schmidt OG, Gelarden IA, Parrish RC, Lively CM (2011) Running with the Red Queen: Host-parasite coevolution selects for biparental sex. Science 333:216–218PubMedGoogle Scholar
  13. 13.
    Schulte RD, Makus C, Hasert B, Michiels NK, Schulenburg H (2010) Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proc Natl Acad Sci 107:7359–7364PubMedGoogle Scholar
  14. 14.
    Thompson JN (2009) The coevolving web of life. Am Nat 173:125–140PubMedGoogle Scholar
  15. 15.
    Thrall PH, Burdon JJ, Bever JD (2002) Local adaptation in the Linum marginale-Melampsora lini host- pathogen interaction. Evolution 56:1340–1351PubMedGoogle Scholar
  16. 16.
    Bohannan BJM, Lenski RE (2000) Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol Lett 3:362–377Google Scholar
  17. 17.
    Calendar RL (2005) The bacteriophages. Oxford University Press, OxfordGoogle Scholar
  18. 18.
    Chopin MC, Chopin A, Bidnenko E (2005) Phage abortive infection in lactococci: variations on a theme. Curr Opin Microbiol 8:473–479PubMedGoogle Scholar
  19. 19.
    Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nature Rev Microbiol 8:317–327Google Scholar
  20. 20.
    Tock MR, Dryden DTF (2005) The biology of restriction and anti-restriction. Curr Opin Microbiol 8:466–472PubMedGoogle Scholar
  21. 21.
    Mattick JS (2002) Type IV pili and twitching motility. Ann Rev Microbiol 56:289–314Google Scholar
  22. 22.
    Samuel ADT, Pitta TP, Ryu WS, Danese PN, Leung ECW, Berg HC (1999) Flagellar determinants of bacterial sensitivity to chi-phage. Proc Natl Acad Sci USA 96:9863–9866PubMedGoogle Scholar
  23. 23.
    Icho T, Iino T (1978) Isolation and characterization of motile Escherichia coli mutants resistant to bacteriophage-chi. J Bacteriol 134:854–860PubMedGoogle Scholar
  24. 24.
    Brockhurst MA, Buckling A, Rainey PB (2005) The effect of a bacteriophage on diversification of the opportunistic bacterial pathogen, Pseudomonas aeruginosa. Proc Roy Soc Lond B 272:1385–1391Google Scholar
  25. 25.
    Lythgoe KA, Chao L (2003) Mechanisms of coexistence of a bacteria and a bacteriophage in a spatially homogeneous environment. Ecol Lett 6:326–334Google Scholar
  26. 26.
    Hashemolhosseini S, Holmes Z, Mutschler B, Henning U (1994) Alterations of receptor specificities of coliphages of the T2 family. J Mol Biol 240:105–110PubMedGoogle Scholar
  27. 27.
    Qimron U, Marintcheva B, Tabor S, Richardson CC (2006) Genomewide screen of E. coli genes affecting growth of T7 bacteriophage. Proc Natl Acad Sci USA 103:19039–19044PubMedGoogle Scholar
  28. 28.
    Mizoguchi K, Morita M, Fischer CR, Yoichi M, Tanji Y, Unno H (2003) Coevolution of bacteriophage PP01 and Escherichia coli O157: H7 in continuous culture. App Environ Microbiol 69:170–176Google Scholar
  29. 29.
    Buckling A, Rainey PB (2002a) Antagonistic coevolution between a bacterium and a bacteriophage. Proc Roy Soc Lond B 269:931–936Google Scholar
  30. 30.
    Paterson S, Vogwill T, Buckling A, Benmayor R, Spiers AJ, Thomson NR, Quail M, Smith F, Walker D, Libberton B, Fenton A, Hall N, Brockhurst MA (2010) Antagonistic coevolution accelerates molecular evolution. Nature 464:275–278PubMedGoogle Scholar
  31. 31.
    Scanlan PD, Hall AR, Lopez-Pascua LDC, Buckling A (2011) Genetic basis of infectivity evolution in a bacteriophage. Mol Ecol 20:981–989PubMedGoogle Scholar
  32. 32.
    Lenski RE, Levin BR (1985) Constraints on the coevolution of bacteria and virulent phage – a model, some experiments, and predictions for natural communities. Am Nat 125:585–602Google Scholar
  33. 33.
    Forde SE, Thompson JN, Holt RD, Bohannan BJM (2008) Coevolution drives temporal changes in fitness and diversity across environments in a bacteria-bacteriophage interaction. Evolution 62:1830–1839PubMedGoogle Scholar
  34. 34.
    Hall AR, Scanlan PD, Morgan AD, Buckling A (2011a) Host-parasite coevolutionary arms races give way to flcutuating selection. Ecol Lett 14:635–642PubMedGoogle Scholar
  35. 35.
    Flores CO, Meyer JR, Valverde S, Farr L, Weitz JS (2011) Statistical structure of host-phage interactions. Proc Natl Acad Sci USA 108:E288–E297PubMedGoogle Scholar
  36. 36.
    Agrawal A, Lively CM (2002) Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evol Ecol Res 4:79–90Google Scholar
  37. 37.
    Frank SA (1993) Specificity versus detectable polymorphism in host-parasite genetics. Proc Roy Soc Lond B 254:191–197Google Scholar
  38. 38.
    Gandon S, Buckling A, Decaestecker E, Day T (2008) Host-parasite coevolution and patterns of adaptation across time and space. J Evol Biol 21:1861–1866PubMedGoogle Scholar
  39. 39.
    Morgan AD, Gandon S, Buckling A (2005) The effect of migration on local adaptation in a coevolving host-parasite system. Nature 437:253–256PubMedGoogle Scholar
  40. 40.
    Fenton A, Antonovics J, Brockhurst MA (2009) Inverse-gene-for-gene infection genetics and coevolutionary dynamics. Am Nat 174:E230–E242PubMedGoogle Scholar
  41. 41.
    Flor HH (1956) The complementary genetic system in flax and flax rust. Adv Genet 8:29–54Google Scholar
  42. 42.
    Sasaki A (2000) Host-parasite coevolution in a multilocus gene-for-gene system. Proc Roy Soc Lond B 267:2183–2188Google Scholar
  43. 43.
    Avrani S, Wurtzel O, Sharon I, Sorek R, Lindell D (2011) Genomic island variability facilitates Prochlorococcus-virus coexistence. Nature 474:604–608PubMedGoogle Scholar
  44. 44.
    Buckling A, Wei Y, Massey RC, Brockhurst MA, Hochberg ME (2006) Antagonistic coevolution with parasites increases the cost of host deleterious mutations. Proc Roy Soc Lond B 273:45–49Google Scholar
  45. 45.
    Lennon JT, Khatana SAM, Marston MF, Martiny JBH (2007) Is there a cost of virus resistance in marine cyanobacteria? ISME J 1:300–312PubMedGoogle Scholar
  46. 46.
    Poullain V, Gandon S, Brockhurst MA, Buckling A, Hochberg ME (2008) The evolution of specificity in evolving and coevolving antagonistic interactions between a bacteria and its phage. Evolution 62:1–11PubMedGoogle Scholar
  47. 47.
    Frank SA (1992) Models of plant pathogen coevolution. Trends Genet 8:213–219PubMedGoogle Scholar
  48. 48.
    Gomez P, Buckling A (2011) Bacteria-phage antagonistic coevolution in soil. Science 332:106–109PubMedGoogle Scholar
  49. 49.
    Ceyssens PJ, Glonti T, Kropinski NM, Lavigne R, Chanishvili N, Kulakov L, Lashkhi N, Tediashvili M, Merabishvili M (2011) Phenotypic and genotypic variations within a single bacteriophage species. Virol J 8:134PubMedGoogle Scholar
  50. 50.
    Glonti T, Chanishvili N, Taylor PW (2010) Bacteriophage-derived enzyme that depolymerizes the alginic acid capsule associated with cystic fibrosis isolates of Pseudomonas aeruginosa. J App Microbiol 108:695–702Google Scholar
  51. 51.
    Wong TY, Preston LA, Schiller NL (2000) Alginate lyase: Review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Ann Rev Microbiol 54:289–340Google Scholar
  52. 52.
    Stern A, Sorek R (2011) The phage-host arms race: Shaping the evolution of microbes. Bioessays 33:43–51PubMedGoogle Scholar
  53. 53.
    van der Oost J, Jore MM, Westra ER, Lundgren M, Brouns SJJ (2009) CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem Sci 34:401–407PubMedGoogle Scholar
  54. 54.
    Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712PubMedGoogle Scholar
  55. 55.
    Brouns SJJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJH, Snijders APL, Dickman MJ, Makarova KS, Koonin EV, van der Oost J (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:960–964PubMedGoogle Scholar
  56. 56.
    Deveau H, Garneau JE, Moineau S (2010) CRISPR/Cas System and Its Role in Phage-Bacteria Interactions. Ann Rev Microbiol 64:475–493Google Scholar
  57. 57.
    Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, Wells L, Terns RM, Terns MP (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139:945–956PubMedGoogle Scholar
  58. 58.
    Stern A, Keren L, Wurtzel O, Amitai G, Sorek R (2010) Self-targeting by CRISPR: gene regulation or autoimmunity? Trends Genet 26:335–340PubMedGoogle Scholar
  59. 59.
    Vale PF, Little TJ (2010) CRISPR-mediated phage resistance and the ghost of coevolution past. Proc Roy Soc Lond Ser B 277:2097–2103Google Scholar
  60. 60.
    Deveau H, Barrangou R, Garneau JE, Labonte J, Fremaux C, Boyaval P, Romero DA, Horvath P, Moineau S (2008) Phage response to CRISPR-Encoded resistance in Streptococcus thermophilus. J Bacteriol 190:1390–1400PubMedGoogle Scholar
  61. 61.
    Andersson AF, Banfield JF (2008) Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320:1047–1050PubMedGoogle Scholar
  62. 62.
    Held NL, Whitaker RJ (2009) Viral biogeography revealed by signatures in Sulfolobus islandicus genomes. Env Microbiol 11:457–466Google Scholar
  63. 63.
    Korona R, Levin BR (1993) Phage-mediated selection and the evolution and maintenance of restriction-modification. Evolution 47:556–575Google Scholar
  64. 64.
    Levin BR (1988) Frequency-dependent selection in bacterial-populations. Phil Trans Roy Soc Lond B 319:459–472Google Scholar
  65. 65.
    Hamilton WD (1964) The genetical evolution of social behaviour, I & II. J Theor Biol 7:1–52PubMedGoogle Scholar
  66. 66.
    Maynard-Smith J (1964) Group selection and kin selection. Nature 201:1145–1147Google Scholar
  67. 67.
    Andre JB, Day T (2005) The effect of disease life history on the evolutionary emergence of novel pathogens. Proc Roy Soc Lond B 272:1949–1956Google Scholar
  68. 68.
    Carval D, Ferriere R (2010) A unified model for the coevolution of resistance, tolerance, and virulence. Evolution 64:2988–3009PubMedGoogle Scholar
  69. 69.
    Kashiwagi A, Yomo T (2011) Ongoing phenotypic and genomic changes in experimental coevolution of RNA bacteriophage Q beta and Escherichia coli. PLoS Genet 7:8Google Scholar
  70. 70.
    Koskella B, Thompson JN, Preston GM, Buckling A (2011) Local Biotic Environment Shapes the Spatial Scale of Bacteriophage Adaptation to Bacteria. Am Nat 177:440–451PubMedGoogle Scholar
  71. 71.
    Agrawal AF, Lively CM (2003) Modelling infection as a two-step process combining gene-for-gene and matching-allele genetics. Proc Roy Soc Lond B 270:323–334Google Scholar
  72. 72.
    Kerr B, Neuhauser C, Bohannan BJM, Dean AM (2006) Local migration promotes competitive restraint in a host-pathogen tragedy of the commons. Nature 442:75–78PubMedGoogle Scholar
  73. 73.
    Boots M, Sasaki A (1999) Small worlds and the evolution of virulence: infection occurs locally and at a distance. Proc Roy Soc Lond B 266:1933–1938Google Scholar
  74. 74.
    Lion S, Boots M (2010) Are parasites prudent in space? Ecol Letts 13:1245–1255Google Scholar
  75. 75.
    Wild G, Gardner A, West SA (2009) Adaptation and the evolution of parasite virulence in a connected world. Nature 459:983–986PubMedGoogle Scholar
  76. 76.
    Gallet R, Shao YP, Wang IN (2009) High adsorption rate is detrimental to bacteriophage fitness in a biofilm-like environment. BMC Evol Biol 9:241PubMedGoogle Scholar
  77. 77.
    Hochberg ME, van Baalen M (1998) Antagonistic coevolution over productivity gradients. Am Nat 152:620–634PubMedGoogle Scholar
  78. 78.
    Lopez-Pascua LDC, Brockhurst MA, Buckling A (2010) Antagonistic coevolution across productivity gradients: an experimental test of the effects of dispersal. J Evol Biol 23:207–211PubMedGoogle Scholar
  79. 79.
    Lopez-Pascua LDC, Buckling A (2008) Increasing productivity accelerates host-parasite coevolution. J Evol Biol 21:853–860PubMedGoogle Scholar
  80. 80.
    Forde SE, Thompson JN, Bohannan BJM (2004) Adaptation varies through space and time in a coevolving host-parasitoid interaction. Nature 431:841–844PubMedGoogle Scholar
  81. 81.
    Forde SE, Thompson JN, Bohannan BJM (2007) Gene flow reverses an adaptive cline in a coevolving host-parasitoid interaction. Am Nat 169:794–801PubMedGoogle Scholar
  82. 82.
    Brockhurst MA, Morgan AD, Rainey PB, Buckling A (2003) Population mixing accelerates coevolution. Ecol Lett 6:975–979Google Scholar
  83. 83.
    Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant-animal interactions. Ann Rev Ecol Evol Syst 35:435–466Google Scholar
  84. 84.
    Zhang QG, Buckling A (2011) Antagonistic coevolution limits population persistence of a virus in a thermally deteriorating environment. Ecol Lett 14:282–288PubMedGoogle Scholar
  85. 85.
    Morgan AD, Brockhurst MA, Lopez-Pascua LDC, Pal C, Buckling A (2007) Differential impact of simultaneous migration on coevolving hosts and parasites. BMC Evol Biol 7:1PubMedGoogle Scholar
  86. 86.
    Vogwill T, Fenton A, Buckling A, Hochberg ME, Brockhurst MA (2009b) Source populations act as coevolutionary pacemakers in experimental selection mosacis containing hotspots and coldspots. Am Nat 173:E171–E176PubMedGoogle Scholar
  87. 87.
    Gandon S, Capowiez Y, Dubois Y, Michalakis Y, Olivieri I (1996) Local adaptation and gene for gene coevolution in a metapopulation model. Proc Roy Soc Lond B 263:1003–1009Google Scholar
  88. 88.
    Vogwill T, Fenton A, Brockhurst MA (2008) The impact of parasite dispersal on antagonistic host-parasite coevolution. J Evol Biol 21:1252–1258PubMedGoogle Scholar
  89. 89.
    Tyson GW, Banfield JF (2008) Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Env Microbiol 10:200–207Google Scholar
  90. 90.
    Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241Google Scholar
  91. 91.
    Vos M, Birkett PJ, Birch E, Griffiths RI, Buckling A (2009) Local adaptation of bacteriophages to their bacterial hosts in soil. Science 325:833–833PubMedGoogle Scholar
  92. 92.
    Lenormand T (2002) Gene flow and the limits to natural selection. TREE 17:183–189Google Scholar
  93. 93.
    Lopez-Pascua LDC, Gandon S, Buckling A (2012) Abiotic heterogeneity drives parasite local adaptation in coevolving bacteria and phages. J Evol Biol 25:187–195PubMedGoogle Scholar
  94. 94.
    Matic I, Radman M, Taddei F, Picard B, Doit C, Bingen E, Denamur E, Elion J (1997) Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science 277:1833–1834PubMedGoogle Scholar
  95. 95.
    Oliver A, Canton R, Campo P, Baquero F, Blazquez J (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288:1251–1253PubMedGoogle Scholar
  96. 96.
    Giraud A, Radman M, Matic I, Taddei F (2001) The rise and fall of mutator bacteria. Curr Opin Microbiol 4:582–585PubMedGoogle Scholar
  97. 97.
    Taddei F, Radman M, Maynard-Smith J, Toupance B, Gouyon PH, Godelle B (1997) Role of mutator alleles in adaptive evolution. Nature 387:700–702PubMedGoogle Scholar
  98. 98.
    Morgan AD, Bonsall MB, Buckling A (2010) Impact of bacterial mutation rate on coevolutionary dynamics between bacteria and phages. Evolution 64:2980–2987PubMedGoogle Scholar
  99. 99.
    Rainey PB, Travisano M (1998) Adaptive radiation in a heterogeneous environment. Nature 394:69–72PubMedGoogle Scholar
  100. 100.
    Buckling A, Rainey PB (2002b) The role of parasites in sympatric and allopatric diversification. Nature 420:496–499PubMedGoogle Scholar
  101. 101.
    Vogwill T, Fenton A, Brockhurst MA (2011) Coevolving parasites enhance the diversity-decreasing effect of dispersal. Biol Lett 7:578–580PubMedGoogle Scholar
  102. 102.
    Brockhurst MA, Rainey PB, Buckling A (2004) The effect of parasites and spatial heterogeneity on the evolution of host diversity. Proc Roy Soc Lond B 271:107–111Google Scholar
  103. 103.
    Benmayor R, Buckling A, Bonsall MB, Brockhurst MA, Hodgson DJ (2008) The interactive effects of parasitesf disturbance, and productivity on experimental adaptive radiations. Evolution 62:467–477PubMedGoogle Scholar
  104. 104.
    Morgan AD, Buckling A (2004) Parasites mediate the relationship between diversity and disturbance. Ecol Lett 7:1029–1034Google Scholar
  105. 105.
    Buckling A, Wills MA, Colegrave N (2003) Adaptation limits diversification of experimental bacterial populations. Science 302:2107–2109PubMedGoogle Scholar
  106. 106.
    Benmayor R, Hodgson DJ, Perron GG, Buckling A (2009) Host mixing and disease emergence. Curr Biol 19:764–767PubMedGoogle Scholar
  107. 107.
    Hall AR, Scanlan PD, Buckling A (2011b) Bacteria-phage coevolution and the emergence of generalist pathogens. Am Nat 177:44–53PubMedGoogle Scholar
  108. 108.
    Vogwill T, Fenton A, Brockhurst MA (2009a) Dispersal and natural enemies interact to drive spatial synchrony and decrease stability in patchy populations. Ecol Lett 12:1194–1200PubMedGoogle Scholar
  109. 109.
    Lennon JT, Martiny JBH (2008) Rapid evolution buffers ecosystem impacts of viruses in a microbial food web. Ecol Lett 11:1178–1188PubMedGoogle Scholar
  110. 110.
    Yoshida T, Jones LE, Ellner SP, Fussmann GF, Hairston NG (2003) Rapid evolution drives ecological dynamics in a predator-prey system. Nature 424:303–306PubMedGoogle Scholar
  111. 111.
    Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399:541–548PubMedGoogle Scholar
  112. 112.
    Thingstad TF, Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 13:19–27Google Scholar
  113. 113.
    Feist AM, Herrgard MJ, Thiele I, Reed JL, Palsson BO (2009). Reconstruction of biochemical networks in microorganisms. Nature Rev Microbiol 7:129–43Google Scholar
  114. 114.
    MacLean RC, Hall AR, Perron GG, Buckling A (2010) The population genetics of antibiotic resistance: integrating molecular mechanisms and treatment contexts. Nature Rev Genet 11:405–14PubMedGoogle Scholar
  115. 115.
    Shapiro OH, Kushmaro A, Brenner A (2010) Bacteriophage predation regulates microbial abundance and diversity in a full-scale bioreactor treating industrial wastewater. ISME J 4:327–336PubMedGoogle Scholar
  116. 116.
    Buckling A, Maclean RC, Brockhurst MA, Colegrave N (2009) The Beagle in a bottle. Nature 457:824–829PubMedGoogle Scholar
  117. 117.
    Morgan AD, Maclean RC, Buckling A (2009) Effects of antagonistic coevolution on parasite-mediated host coexistence. J Evol Biol 22:287–292PubMedGoogle Scholar
  118. 118.
    Johnson MTJ, Stinchcombe JR (2007) An emerging synthesis between community ecology and evolutionary biology. TREE 22:250–257PubMedGoogle Scholar
  119. 119.
    Nuismer SL, Thompson JN (2006) Coevolutionary alternation in antagonistic interactions. Evolution 60:2207–2217PubMedGoogle Scholar
  120. 120.
    Palumbi SR (2001) Evolution – Humans as the world’s greatest evolutionary force. Science 293:1786–1790PubMedGoogle Scholar
  121. 121.
    Levin BR, Bull JJ (2004) Population and evolutionary dynamics of phage therapy. Nature Rev Microbiol 2:166–173Google Scholar
  122. 122.
    Maura D, Debarbieux L (2011) Bacteriophages as twenty-first century antibacterial tools for food and medicine. App Microbiol Biotech 90:851–859Google Scholar
  123. 123.
    Smith HW, Huggins MB (1983) Effectiveness of phages in treating experimental Escherichia coli diarrhea in calves, piglets and lambs. J Gen Microbiol 129:2659–2675PubMedGoogle Scholar
  124. 124.
    Friedel CC, Haas J (2011) Virus-host interactomes and global models of virus-infected cells. Trends Microbiol 19:501–508PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.BiosciencesUniversity of ExeterCornwallUK
  2. 2.Institute of Integrative Biology, Biosciences BuildingUniversity of LiverpoolLiverpoolUK

Personalised recommendations