War and peace: Social interactions in infections

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1642, 2014, Pages

  Leggett, Helen C ^a,b   Brown, Sam P ^c   Reece, Sarah E ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Ecology; Inclusive fitness; Plasticity; Relatedness; Transmission; Virulence

Indexed keywords

DISEASE CONTROL; EVOLUTIONARY THEORY; INCLUSIVE FITNESS; MICROBIAL ACTIVITY; PARASITE; PATHOGEN; PHENOTYPIC PLASTICITY; PUBLIC GOODS; RELATEDNESS; SOCIAL BEHAVIOR; VIRULENCE;

BIOLOGICAL MODEL; ECOLOGY; EVOLUTION; GENETICS; HOST PATHOGEN INTERACTION; INCLUSIVE FITNESS; INFECTION; ORGANISMAL INTERACTION; PATHOPHYSIOLOGY; PHENOTYPE; PLASTICITY; RELATEDNESS; REPRODUCTIVE FITNESS; REVIEW; SOCIAL BEHAVIOR; TRANSMISSION; VIRULENCE;

ECOLOGY; INCLUSIVE FITNESS; PLASTICITY; RELATEDNESS; TRANSMISSION; VIRULENCE;

BIOLOGICAL EVOLUTION; GENETIC FITNESS; HOST-PATHOGEN INTERACTIONS; INFECTION; MICROBIAL INTERACTIONS; MODELS, BIOLOGICAL; PHENOTYPE; SOCIAL BEHAVIOR; VIRULENCE;

EID: 84897135766     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0365     Document Type: Review

References (152)

1. West SA, Diggle SP, Buckling A, Gardner A, Griffin AS. 2007 The social lives of microbes. Annu. Rev. Ecol. Evol. Syst. 38, 53-77. (doi:10.1146/annurev. ecolsys.38.091206.095740)
2. Nadell CD, Bucci V, Drescher K, Levin SA, Bassler BL, Xavier JB. 2013 Cutting through the complexity of cell collectives. Proc. R. Soc. B 280, 20122770. (doi:10.1098/rspb.2012.2770)
3. Crespi BJ. 2001 The evolution of social behavior in microorganisms. Trends Ecol. Evol. 16, 178-183. (doi:10.1016/S0169-5347(01)02115-2)
4. Webb JS, Givskov M, Kjelleberg S. 2003 Bacterial biofilms: prokaryotic adventures in multicellularity. Curr. Opin. Microbiol. 6, 578-585. (doi:10.1016/j. mib.2003.10.014)
5. Kolter R, Greenberg EP. 2006 Microbial sciences: the superficial life of microbes. Nature 18, 300-302. (doi:10.1038/441300a)
6. West SA, Griffin AS, Gardner A, Diggle SP. 2006 Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4, 597-607. (doi:10.1038/ nrmicro1461)
7. Diggle SP, Griffin AS, Campbell GS, West SA. 2007 Cooperation and conflict in quorum-sensing bacterial populations. Nature 450, 411-414. (doi:10.1038/nature0627915)
8. Foster KR, Parkinson K, Thompson CRL. 2007 What can microbial genetics teach sociobiology? Trends Genet. 23, 74-80. (doi:10.1016/j.tig.2006.12.003)
9. Hense BA, Kuttler C, Muller J, Rothballer M, Hartmann A, Kreft JU. 2007 Does efficiency sensing unify diffusion and quorum sensing? Nat. Rev. Microbiol. 5, 230-239. (doi:10.1038/nrmicro1600)
10. Williams P, Winzer K, Chan WC, Camara M. 2007 Look who's talking: communication and quorum sensing in the bacterial world. Phil. Trans. R. Soc. B 362, 1119-1134. (doi:10.1098/rstb.2007.2039)
11. Brown SP, Buckling A. 2008 A social life for discerning microbes. Cell 135, 600-603. (doi:10. 1016/j.cell.2008.10.030)
12. MacLean R. 2008 The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies. Heredity 100, 471-477. (doi:10.1038/sj.hdy.6801073)
13. Popat R, Crusz SA, Diggle SP. 2008 The social behaviours of bacterial pathogens. Br. Med. Bull. 87, 63-75. (doi:10.1093/bmb/ldn030)
14. Brown SP, Inglis R, Taddei F. 2009 SYNTHESIS: evolutionary ecology of microbial wars: within-host competition and (incidental) virulence. Evol. Appl. 2, 32-39. (doi:10.1111/j.1752-4571.2008.00059.x)
15. Reece SE, Pollitt LC, Colegrave N, Gardner A. 2011 The meaning of death: evolution and ecology of apoptosis in protozoan parasites. PLoS Pathog. 7, e1002320. (doi:10.1371/journal.ppat.1002320)
16. Buckling A, Brockhurst MA. 2008 Kin selection and the evolution of virulence. Heredity 100, 484-488. (doi:10.1038/sj.hdy.6801093)
17. Nogueira T, Rankin DJ, Touchon M, Taddei F, Brown SP, Rocha EPC. 2009 Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence. Curr. Biol. 19, 1683-1691. (doi:10.1016/j.cub.2009.08.056)
18. Rankin DJ, Rocha EPC, Brown SP. 2010 What traits are carried on mobile genetic elements, and why? Heredity 106, 1-10. (doi:10.1038/hdy.2010.24)
19. Brown SP, West SA, Diggle SP, Griffin AS. 2009 Social evolution in microorganisms and a Trojan horse approach to medical intervention strategies. Phil. Trans. R. Soc. B 364, 3157-3168. (doi:10. 1098/rstb.2009.0055)
20. Mideo N, Day T. 2008 On the evolution of reproductive restraint in malaria. Proc. R. Soc. B 275, 1217-1224. (doi:10.1098/rspb.2007.1545)
21. Reece SE, Drew DR, Gardner A. 2008 Sex ratio adjustment and kin discrimination in malaria parasites. Nature 453, 609-615. (doi:10.1038/ nature06954)
22. Mideo N et al. 2013 Life in cells, hosts, and vectors: parasite evolution across scales. Infect. Genet. Evol. 13, 344-347. (doi:10.1016/j.meegid.2012.03.016)
23. Mideo N, Reece SE. 2012 Plasticity in parasite phenotypes: evolutionary and ecological implications for disease. Future Microbiol. 7, 17-24. (doi:10.2217/fmb.11.134)
24. Hamilton WD. 1964 The genetical evolution of social behaviour II. J. Theor. Biol. 7, 17-52. (doi:10. 1016/0022-5193(64)90039-6)
25. West SA, Griffin AS, Gardner A. 2007 Evolutionary explanations for cooperation. Curr. Biol. 17, R661-R672. (doi:10.1016/j.cub.2007.06.004)
26. Hamilton WD. 1970 Selfish and spiteful behaviour in an evolutionary model. Nature 228, 1218-1220. (doi:10.1038/2281218a0)
27. Lacey EA, Sherman PW. 1991 Social organisation of naked mole-rat colonies: evidence for divisions of labor. In The biology of the naked mole-rat (eds PW Sherman, JUM Jarvis, RD Alexander), pp. 275-336. Princeton, New Jersey: Princeton University Press.
28. Šumbera R, Zelová J, Kunc P, Kni{dotless}žková I, Burda H. 2007 Patterns of surface temperatures in two molerats (Bathyergidae) with different social systems as revealed by IR-thermography. Physiol. Behav. 92, 526-532. (doi:10.1016/j.physbeh.2007.04.029)
29. Spinks AC, Plagányi EE. 1999 Reduced starvation risks and habitat constraints promote cooperation in the common mole-rat, Cryptomys hottentotus hottentotus: a computer-simulated foraging model. Oikos 85, 435-444. (doi:10.2307/3546693)
30. Queller DC, Zacchi F, Cervo R, Turillazzi S, Henshaw MT, Santorelli LA, Strassmann JE. 2000 Unrelated helpers in a social insect. Nature 405, 784-787. (doi:10.1038/35015552)
31. Telfer S, Lambin W, Birtles R, Beldomenico P, Burthe S, Paterson S, Begon M. 2010 Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243-246. (doi:10. 1126/science.1190333)
32. Bertram BCR. 1975 Social factors influencing reproduction in wild lions. J. Zool. 177, 463-482. (doi:10.1111/j.1469-7998.1975.tb02246.x)
33. Boland CRJ, Heinsohn R, Cockburn A. 1997 Deception by helpers in cooperatively breeding white-winged choughs and its experimental manipulation. Behav. Ecol. Sociobiol. 41, 251-256. (doi:10.1007/s002650050386)
34. Griffin AS, West SA, Buckling A. 2004 Cooperation and competition in pathogenic bacteria. Nature 430, 1024-1027. (doi:10.1038/nature02744)
35. Harrison F, Browning LE, Vos M, Buckling A. 2006 Cooperation and virulence in acute Pseudomonas aeruginosa infections. BMC Biol. 4, 21. (doi:10.1186/ 1741-7007-4-21)
36. Meyer JM, Neely A, Stintzi A, Georges C, Holder IA. 1996 Pyoverdin is essential for virulence of Pseudomonas aeruginosa. Infect. Immun. 64, 518-523.
37. Bell AS, De Roode JC, Sim D, Read AF. 2006 Withinhost competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60, 1358-1371. (doi:10.1554/05-611.1)
38. Leggett HC, Benmayor R, Hodgson DJ, Buckling A. 2013 Experimental evolution of adaptive phenotypic plasticity in a parasite. Curr. Biol. 23, 139-142. (doi:10.1016/j.cub.2012.11.045)
39. Boomsma JJ. 2009 Lifetime monogamy and the evolution of eusociality. Phil. Trans. R. Soc. B 364, 3191-3207. (doi:10.1098/rstb.2009.0101)
40. Kamiya T, Poulin R. 2013 Caste ratios affect the reproductive output of social trematode colonies. J. Evol. Biol. 26, 509-516. (doi:10.1111/jeb.12062)
41. Ackermann M, Stecher B, Freed NE, Songhet P, Hardt WD, Doebeli M. 2008 Self-destructive cooperation mediated by phenotypic noise. Nature 454, 987-990. (doi:10.1038/nature07067)
42. Refardt D, Bergmiller T, Kümmerli R. 2013 Altruism can evolve when relatedness is low: evidence from bacteria committing suicide upon phage infection. Proc. R. Soc. B 280, 20123035. (doi:10.1098/rspb. 2012.3035)
43. Pollitt LC, Colegrave N, Khan SM, Sajid M, Reece SE. 2010 Investigating the evolution of apoptosis in malaria parasites: the importance of ecology. Parasit. Vectors 16, 105. (doi:10.1186/1756-3305-3-105)
44. Giron D, Dunn DW, Hardy ICW, Strand MR. 2004 Aggression by polyembryonic wasp soldiers correlates with kinship but not resource competition. Nature 430, 676-679. (doi:10.1038/ nature02721)
45. Keller L, Ross KG. 1998 Selfish genes: a green beard in the red fire ant. Nature 394, 573-575. (doi:10. 1038/29064)
46. Massey RC, Buckling A, Ffrench-Constant R. 2004 Interference competition and parasite virulence. Proc. R. Soc. Lond. B 271, 785-788. (doi:10.1098/ rspb.2004.2676)
47. Inglis RF, Brown SP, Buckling A. 2012 Spite versus cheats: competition among social strategies shapes virulence in Pseudomonas aeruginosa. Evolution 66, 3472-3484. (doi:10.1111/j.1558-5646.2012.01706.x)
48. Hamilton WD. 1964 The genetical evolution of social behaviour I. J. Theor. Biol. 7, 1-16. (doi:10. 1016/0022-5193(64)90038-4)
49. Trivers RL. 1985 Social evolution. Menlo Park, CA: Benjamin/Cummings.
50. West SA, Griffin AS, Gardner A. 2007 Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20, 415-432. (doi:10.1111/j.1420-9101.2006.01258.x)
51. Gardner A, West SA, Wild G. 2011 The genetical theory of kin selection. J. Evol. Biol. 24, 1020-1043. (doi:10.1111/j.1420-9101.2011.02236.x)
52. Bourke AFG. 2011 Principles of social evolution. Oxford Series in Ecology and Evolution. Oxford, UK: Oxford University Press.
53. Tibayrenc M, Ayala FJ. 2012 Reproductive clonality of pathogens: a perspective on pathogenic viruses, bacteria, fungi, and parasitic protozoa. Proc. Natl Acad. Sci. USA 109, E3305-E3313. (doi:10.1073/ pnas.1212452109)
54. Gardner A, Grafen A. 2009 Capturing the superorganism: a formal theory of group adaptation. J. Evol. Biol. 22, 659-671. (doi:10. 1111/j.1420-9101.2008.01681.x)
55. Dumas Z, Kummerli R. 2012 Cost of cooperation rules selection for cheats in bacterial metapopulations. J. Evol. Biol. 25, 473-484. (doi:10.1111/j.1420-9101.2011.02437.x)
56. Hardin G. 1988 Tragedy of the commons. Science 162, 1243-1248. (doi:10.1126/science.162.3859. 1243)
57. Nowak M. 2011 Supercooperators: altruism, evolution, and why we need each other to succeed. New York, NY: The Free Press.
58. Dugatkin LA. 2002 Animal cooperation among unrelated individuals. Naturwissenschaften 89, 533-541. (doi:10.1007/s00114-002-0379-y)
59. Chuang JS, Rivoire O, Leibler S. 2009 Simpson's paradox in a synthetic microbial system. Science 323, 272-275. (doi:10.1126/science.1166739)
60. Xavier JB, Kim W, Foster KR. 2011 A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa. Mol. Microbiol. 79, 166-179. (doi:10.1111/j.1365-2958.2010.07436.x)
61. Sachs JL, Mueller UG, Wilcox TP, Bull JJ. 2004 The evolution of cooperation. Q. Rev. Biol. 79, 135-160. (doi:10.1086/383541)
62. Lehmann L, Keller L. 2006 The evolution of cooperation and altruism-a general framework and a classification of models. J. Evol. Biol. 19, 1365-1376. (doi:10.1111/j.1420-9101.2006)
63. Nadell CD, Xavier JB, Foster KR. 2009 The sociobiology of biofilms. FEMS Microbiol. Rev. 33, 206-224. (doi:10.1111/j.1574-6976.2008.00150.x)
64. Dawkins R. 1976 The selfish gene. Oxford, UK: Oxford University Press.
65. Gardner A, West SA. 2010 Greenbeards. Evolution 64, 25-38. (doi:10.1111/j.1558-5646.2009.00842.x)
66. Benabentos R et al. 2009 Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium. Curr. Biol. 19, 567-572. (doi:10. 1016/j.cub.2009.02.037)
67. Hirose S, Benabentos R, Ho HI, Kuspa A, Shaulsky G. 2011 Self-recognition in social amoebae is mediated by allelic pairs of tiger genes. Science 333, 467-470. (doi:10.1126/science.1203903)
68. Sharp SP, McGowan A, Wood MJ, Hatchwell BJ. 2005 Learned kin recognition cues in a social bird. Nature 434, 1127-1130. (doi:10.1038/nature 03522)
69. Mateo JM. 2002 Kin-recognition abilities and nepotism as a function of sociality. Proc. R. Soc. Lond. B 269, 721-727. (doi:10.1098/rspb. 2001.1947)
70. Rousset F, Roze D. 2007 Constraints on the origin and maintenance of genetic kin recognition. Evolution 61, 2320-2330. (doi:10.1111/j.1558-5646.2007.00191.x)
71. Schuster M, Lostroh CP, Ogi T, Greenberg EP. 2003 Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185, 2066-2079. (doi:10.1128/JB.185.7.2066-2079.2003)
72. Darch SE, West SA, Winzer K, Diggle SP. 2012 Density-dependent fitness benefits in quorumsensing bacterial populations. Proc. Natl Acad. Sci. USA 109, 8259-8263. (doi:10.1073/pnas. 1118131109)
73. Mantel PY et al. 2013 Malaria-infected erythrocytederived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe 13, 521-534. (doi:10.1016/j.chom.2013.04.009)
74. Regev-Rudzki N et al. 2013 Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles. Cell 153, 1120-1133. (doi:10.1016/j.cell.2013.04.029)
75. Reece SE, Ali E, Schneider P, Babiker HA. 2010 Stress, drugs and the evolution of reproductive restraint in malaria parasites. Proc. R. Soc. B 277, 3123-3129. (doi:10.1098/rspb.2010.0564)
76. Pollitt LC, Mideo N, Drew D, Schneider P, Colegrave N, Reece SE. 2011 Competition and the evolution of reproductive restraint in malaria parasites. Am. Nat. 177, 358-367. (doi:10.1086/658175)
77. Levin BR. 1996 The evolution and maintenance of virulence in microparasites. Emerg. Infect. Dis. 2, 93-102. (doi:10.3201/eid0202.960203)
78. Margolis E, Levin BR. 2007 Within-host evolution for the invasiveness of commensal bacteria: an experimental study of bacteremias resulting from Haemophilus influenzae nasal carriage. J. Infect. Dis. 196, 1068-1075. (doi:10.1086/520934)
79. Ebert D. 1998 The evolution and expression of virulence. In Evolution in health and disease (ed. SC Stearns), pp. 153-167. Oxford, UK: Oxford University Press.
80. Bull JJ, Ebert D. 2008 Invasion thresholds and the evolution of nonequilibrium virulence. Evol. Appl. 1, 172-182. (doi:10.1111/j.1752-4571.2007. 00003.x)
81. Alizon S, Hurford A, Mideo N, Van Baalen M. 2009 Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22, 245-259. (doi:10.1111/j.1420-9101.2008.01658.x)
82. Levin BR, Eden CS. 1990 Selection and evolution of virulence in bacteria-an ecumenical excursion and modest suggestion. Parasitology 100, S103-SS15. (doi:10.1017/S0031182000073054)
83. Brown SP, Cornforth DM, Mideo N. 2012 Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends Microbiol. 20, 336-342. (doi:10.1016/j.tim.2012.04.005)
84. Levin BR, Bull JJ. 1994 Short-sighted evolution and the virulence of pathogenic microorganisms. Trends Microbiol. 2, 76-81. (doi:10.1016/0966-842X(94)90538-X)
85. Anderson RM, May RM. 1982 Coevolution of hosts and parasites. Parasitology 85, 411-426. (doi:10. 1017/S0031182000055360)
86. Bremermann HJ, Pickering J. 1983 A gametheoretical model of parasite virulence. J. Theor. Biol. 100, 411-426. (doi:10.1016/0022-5193(83)90438-1)
87. Nowak MA, May RM. 1994 Superinfection and the evolution of parasite virulence. Proc. R. Soc. Lond. B 255, 81-89. (doi:10.1098/rspb.1994.0012)
88. Frank SA. 1996 Models of parasite virulence. Q. Rev. Biol. 71, 37-78. (doi:10.1086/419267)
89. de Roode JC, Yates AJ, Altizer S. 2008 Virulencetransmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc. Natl Acad. Sci. USA 105, 7489-7494. (doi:10.1073/pnas.0710909105)
90. Brown SP, Hochberg ME, Grenfell BT. 2002 Does multiple infection select for raised virulence? Trends Microbiol. 10, 401-405. (doi:10.1016/S0966-842X(02)02413-7)
91. Leggett HC, Buckling A, Long GH, Boots M. 2013 Generalism and the evolution of parasite virulence. Trends Ecol. Evol. 28, 592-596. (doi:10.1016/j.tree. 2013.07.002)
92. Alizon S, de Roode JC, Michalakis Y. 2013 Multiple infections and the evolution of virulence. Ecol. Lett. 16, 556-567. (doi:10.1111/ele.12076)
93. Buckling A, Harrison F, Vos M, Brockhurst MA, Gardner A, West SA, Griffin A. 2007 Siderophoremediated cooperation and virulence in Pseudomonas aeruginosa. FEMS Microbiol. Ecol. 62, 135-141. (doi:10.1111/j.1574-6941.2007. 00388.x)
94. Kummerli R, Griffin AS, West SA, Buckling A, Harrison F. 2009 Viscous medium promotes cooperation in the pathogenic bacterium Pseudomonas aeruginosa. Proc. R. Soc. B 276, 3531-3538. (doi:10.1098/rspb.2009.0861)
95. Morgan AD, Quigley BJZ, Brown SP, Buckling A. 2012 Selection on non-social traits limits the invasion of social cheats. Ecol. Lett. 15, 841-846. (doi:10.1111/j.1461-0248.2012.01805.x)
96. Zhang XX, Rainey PB. 2013 Exploring the sociobiology of pyoverdin-producing Pseudomonas. Evolution 67, 3161-3174. (doi:10. 1111/evo.12183)
97. Kümmerli R, Ross-Gillespie A. In press. Explaining the sociobiology of pyoverdin-producing Pseudomonas: a comment on Zhang and Rainey (2013). Evolution. (doi:10.1111/evo.12311)
98. Frost LS, Leplae R, Summers AO, Toussaint A. 2005 Mobile genetic elements: the agents of open source evolution. Nat. Rev. Microbiol. 3, 722-732. (doi:10. 1038/nrmicro1235)
99. Smith J. 2001 The social evolution of bacterial pathogenesis. Proc. R. Soc. Lond. B 268, 61-69. (doi:10.1098/rspb.2000.1330)
100. Mc Ginty SE, Rankin DJ, Brown SP. 2011 Horizontal gene transfer and the evolution of bacterial cooperation. Evolution 65, 21-32. (doi:10.1111/j. 1558-5646.2010.01121.x)
101. Mc Ginty SE, Lehmann L, Brown SP, Rankin DJ. 2013 The interplay between relatedness and horizontal gene transfer drives the evolution of plasmid-carried public goods. Proc. R. Soc. B 280, 20130400. (doi:10.1098/rspb.2013.0400)
102. Dimitriu T, Lotton C, Bernard-Capelle J, Brown SP, Linder AB, Taddei F. Submitted. Genetic information transfer promotes cooperation by increasing relatedness in bacteria.
103. Pigliucci M. 2001 Phenotypic plasticity: beyond nature and nurture. Baltimore, MD: John Hopkins University Press.
104. Mitchell A, Romano GH, Groisman B, Yona A, Dekel E, Kupiec M, Dahan O, Pilpel Y. 2009 Adaptive prediction of environmental changes by microorganisms. Nature 460, 220-224. (doi:10. 1038/nature08112)
105. Mideo N, Reece SE, Smith AL, Metcalf CJ. 2013 The Cinderella syndrome: why do malaria-infected cells burst at midnight? Trends Parasitol. 29, 10-16. (doi:10.1016/j.pt.2012.10.006)
106. O'Donnell AJ, Schneider P, McWatters HG, Reece SE. 2011 Fitness costs of disrupting circadian rhythms in malaria parasites. Proc. R. Soc. B 278, 2429-2436. (doi:10.1098/rspb.2010.2457)
107. O'Donnell AJ, Mideo N, Reece SE. 2013 Disrupting rhythms in Plasmodium chabaudi: costs accrue quickly and independently of how infections are initiated. Malaria J. 12, 372. (doi:10.1186/1475-2875-12-372)
108. Greischer MA, Read AF, Bjørnstad ON. 2014 Synchrony in malaria infections: how intensifying within-host competition can be adaptive. Am. Nat. 183, E36-E49. (doi:10.1086/674357)
109. Witkowski B, Lelievre J, Barragan MJ, Laurent V, Su XZ, Berry A, Benoit-Vical F. 2010 Increased tolerance to artemisinin in Plasmodium falciparum is mediated by a quiescence mechanism. Antimicrob. Agents Chemother. 54, 1872-1877. (doi:10.1128/ AAC.01636-09)
110. Abedon ST. 1990 Selection for lysis inhibition in bacteriophage. J. Theor. Biol. 146, 501-511. (doi:10.1016/S0022-5193(05)80375-3)
111. Abedon ST. 1992 Lysis of lysis-inhibited bacteriophage T4-infected cells. J. Bacteriol. 174, 8073-8080.
112. Abedon ST. 1994 Lysis and the interaction between free phages and infected cells. In Molecular biology of bacteriophage T4 (eds J Karam et al.), pp. 397-405. Washington, DC: American Society for Microbiology.
113. Abedon ST. 1999 Bacteriophage T4 resistance to lysis-inhibition collapse. Genet Res, 74, 1-11. (doi:10.1017/S0016672399003833)
114. Kümmerli R, Jiricny N, Clarke LS, West SA, Griffin AS. 2009 Phenotypic plasticity of a cooperative behaviour in bacteria. J. Evol. Biol. 22, 589-598. (doi:10.1111/j. 1420-9101.2008.01666.x)
115. Kümmerli R, Brown SP. 2010 Molecular and regulatory properties of a public good shape the evolution of cooperation. Proc. Natl Acad. Sci. USA 107, 18 921-18 926. (doi:10.1073/pnas. 1011154107)
116. Rutherford ST, Bassler BL. 2012 Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2, a012427. (doi:10.1101/cshperspect.a012427)
117. Viney M, Reece SE. 2013 Adaptive noise. Proc. R. Soc. B 280, 20131104. (doi:10.1098/rspb. 2013.1104)
118. Pollitt LC, Churcher TS, Dawes EJ, Khan SM, Sajid M, Basánez MG, Colegrave N, Reece SE. 2013 Costs of crowding for the transmission of malaria parasites. Evol. Appl. 6, 617-629. (doi:10.1111/eva.12048)
119. Schlichting CD, Pigliucci M. 1998 Phenotypic evolution: a reaction norm perspective. Sunderland, MA: Sinauer Associates Incorporated.
120. Ramiro RS, Alpedrinha J, Carter L, Gardner A, Reece SE. 2011 Sex and death: the effects of innate immune factors on the sexual reproduction of malaria parasites. PLoS Pathog. 7, e1001309. (doi:10.1371/journal.ppat.1001309)
121. Reece SE, Khan SM, Waters AP, Janse CJ, Kaczanowski S. 2012 Why are male malaria parasites in such a rush? Sex-specific evolution and host-parasite interactions. Evol. Med. Public Health. 2013, 3-13. (doi:10.1093/emph/eos003)
122. West-Eberhard MJ. 2003 Developmental plasticity and evolution. Oxford, UK: Oxford University Press.
123. Hamilton WD. 1967 Extraordinary sex ratios: a sexratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science 156, 477-488. (doi:10.1126/science.156. 3774.477)
124. DeWitt TJ, Sih A, Wilson DS. 1998 Costs and limits of phenotypic plasticity. Trends Ecol. Evol. 13, 77-81. (doi:10.1016/S0169-5347(97)01274-3)
125. Stover CK et al. 2000 Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406, 959-964. (doi:10.1038/ 35023079)
126. Duan K, Surette MG. 2007 Environmental regulation of Pseudomonas aeruginosa PAO1 Las and Rhl quorum-sensing systems. J. Bacteriol. 189, 4827-4836. (doi:10.1128/JB.00043-07)
127. Bielecki P et al. 2011 In vivo expression profiling of Pseudomonas aeruginosa infections reveals nichespecific and strain-independent transcriptional programs. PLoS ONE 6, e24235. (doi:10.1371/ journal.pone.0024235)
128. Jiricny N, Diggle SP, West SA, Evans BA, Ballantyne G, Ross-Gillespie A, Griffin AS. 2010 Fitness correlates with the extent of cheating in a bacterium. J. Evol. Biol. 23, 738-747. (doi:10.1111/ j.1420-9101.2010.01939.x)
129. Bragonzi A, Paroni M, Nonis A, Cramer N, Montanari S, Rejman J, Di Serio C, Döring G, Tümmler B. 2009 Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am. J. Respir. Crit. Care Med. 180, 138-145. (doi:10.1164/rccm.200812-1943OC)
130. Harrison F, Paul J, Massey RC, Buckling A. 2008 Interspecific competition and siderophore-mediated cooperation in Pseudomonas aeruginosa. Isme J. 2, 49-55. (doi:10.1038/ismej.2007.96)
131. Grant AJ, Restif O, McKinley TJ, Sheppard M, Maskell DJ, Mastroeni P. 2008 Modelling within-host spatiotemporal dynamics of invasive bacterial disease. PLoS Biol. 6, e74. (doi:10.1371/journal.pbio. 0060074)
132. Mitri S, Xavier J, Foster KR. 2011 Social evolution in multispecies biofilms. Proc. Natl Acad. Sci. USA 108(Suppl. 2), 10 839-10 846. (doi:10.1073/pnas. 1100292108)
133. Popat R, Crusz SA, Messina M, Williams P, West SA, Diggle SP. 2012 Quorum-sensing and cheating in bacterial biofilms. Proc. R. Soc. B 279, 4765-4771. (doi:10.1098/rspb.2012.1976)
134. Nadell CD, Bassler BL. 2011 A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc. Natl Acad. Sci. USA 108, 14 181-14 185. (doi:10.1073/pnas.1111147108)
135. The Human Microbiome Project Consortium. 2012 Structure, function and diversity of the healthy human microbiome. Nature 486, 207-214. (doi:10. 1038/nature11234)
136. Balmer O, Stearns SC, Schötzau A, Brun R. 2009 Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology 90, 3367-3378. (doi:10. 1890/08-2291.1)
137. Eswarappa SM, Estrela S, Brown SP. 2012 Withinhost dynamics of multi-species infections: facilitation, competition and virulence. PLoS ONE 7, e38730. (doi:10.1371/journal.pone.0038730)
138. Vardo AM, Kaufhold KD, Schall JJ. 2007 Experimental test for premunition in a lizard malaria parasite (Plasmodium mexicanum). J. Parasitol. 93, 280-282. (doi:10.1645/ GE-1005R.1)
139. Portugal S et al. 2011 Host-mediated regulation of superinfection in malaria. Nat. Med. 17, 732-737. (doi:10.1038/nm.2368)
140. McQueen PG, McKenzie FE. 2006 Competition for red blood cells can enhance Plasmodium vivax parasitemia in mixed-species malaria infections. Am. J. Trop. Med. Hyg. 75, 112-125.
141. Pedersen AB, Fenton A. 2007 Emphasizing the ecology in parasite community ecology. Trends Ecol. Evol. 22, 133-139. (doi:10.1016/j.tree.2006.11.005)
142. Estrela S, Brown SP. 2013 Metabolic and demographic feedbacks shape the emergent spatial structure and function of microbial communities. PLoS Comp. Biol. 9, e1003398. (doi:10.1371/journal. pcbi.1003398)
143. Hoffmann AA et al. 2011 Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476, 454-457. (doi:10.1038/nature10356)
144. Poulin R, Morand S. 2000 The diversity of parasites. Q. Rev. Biol. 75, 277-293. (doi:10.1086/393500)
145. Foster KR. 2005 Hamiltonian medicine: why the social lives of pathogens matter. Science 308, 1269-1270. (doi:10.1126/science.1108158)
146. Rumbaugh KP, Diggle SP, Watters CM, Ross-Gillespie A, Griffin AS, West SA. 2009 Quorum sensing and the social evolution of bacterial virulence. Curr. Biol. 19, 341-345. (doi:10.1016/j.cub.2009.01.050)
147. Read AF, Day T, Huijben S. 2011 The evolution of drug resistance and the curious orthodoxy of aggressive chemotherapy. Proc. Natl Acad. Sci. USA 108, 10 871-10 877. (doi:10.1073/pnas. 1100299108)
148. André JB, Godelle B. 2005 Multicellular organization in bacteria as a target for drug therapy. Ecol. Lett. 8, 800-810. (doi:10.1111/j. 1461-0248.2005.00783.x)
149. Mellbye B, Schuster M. 2011 The sociomicrobiology of antivirulence drug resistance: a proof of concept. mBio 2, e00131. (doi:10.1128/mBio.00131-11)
150. Ross-Gillespie A, Weigert M, Brown SP, Kümmmerli R. 2014 Gallium-mediated siderophore quenching as an evolutionarily robust antibacterial treatment. Evol. Med. Publ. Health 2014, 18-29. (doi:10.1093/ emph/eou003)
151. Allen RC, Popat R, Diggle SP, Brown SP. In press. Targeting virulence: can we make evolution-proof drugs? Nat. Rev. Microbiol. (doi:10.1038/ nrmicro3232)
152. Carter LC, Mideo NM, Pollitt LC, Kafsack BFC, Llinas M, Reece SE. 2013 Stress and sex in malaria parasites: why does commitment vary? Evol. Med. Public Health 2013, 135-147. (doi:10.1093/emph/ eot011)