Multiple-genotype infections and their complex effect on virulence

Zoology

Volumn 119, Issue 4, 2016, Pages 339-349

  Bose, Joy ^a,b   Kloesener, Michaela H ^a   Schulte, Rebecca D ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

Co infection; Epidemiology; Genotype specific interaction; Parasite genotypes

Indexed keywords

ANIMAL; EVOLUTION; GENETICS; GENOTYPE; HOST PARASITE INTERACTION; PARASITE; PATHOGENICITY; VIRULENCE;

ANIMALS; BIOLOGICAL EVOLUTION; GENOTYPE; HOST-PARASITE INTERACTIONS; PARASITES; VIRULENCE;

EID: 84977110597     PISSN: 09442006     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.zool.2016.06.003     Document Type: Review

References (133)

1. Alizon, S., Co-infection and super-infection models in evolutionary epidemiology. Interface Focus, 3, 2013, 20130031.
2. Alizon, S., Lion, S., Within-host parasite cooperation and the evolution of virulence. Proc. R. Soc. B 278 (2011), 3738–3747.
3. Alizon, S., Michalakis, Y., Adaptive virulence evolution: the good old fitness-based approach. Trends Ecol. Evol. 30 (2015), 248–254.
4. Alizon, S., van Baalen, M., Multiple infections, immune dynamics, and the evolution of virulence. Am. Nat. 172 (2008), E150–E168.
5. Alizon, S., Hurford, A., Mideo, N., van Baalen, M., Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22 (2009), 245–259.
6. Alizon, S., Luciani, F., Regoes, R.R., Epidemiological and clinical consequences of within-host evolution. Trends Microbiol. 19 (2011), 24–32.
7. Alizon, S., de Roode, J.C., Michalakis, Y., Multiple infections and the evolution of virulence. Ecol. Lett. 16 (2013), 556–567.
8. Anderson, R.M., May, R.M., Coevolution of hosts and parasites. Parasitology 85 (1982), 411–426.
9. Arnot, R., The evolving efforts to control hepatitis B virus. Pediatr. Infect. Dis. J. 17 (1998), S26–29.
10. Atkinson, S., Williams, P., Quorum sensing and social networking in the microbial world. J. R. Soc. Interface 6 (2009), 959–978.
11. Bakkal, S., Robinson, S.M., Ordonez, C.L., Waltz, D.A., Riley, M.A., Role of bacteriocins in mediating interactions of bacterial isolates taken from cystic fibrosis patients. Microbiology 156 (2010), 2058–2067.
12. Ball, G.H., Parasitism and evolution. Am. Nat. 77 (1943), 345–364.
13. Balmer, O., Tanner, M., Prevalence and implications of multiple-strain infections. Lancet Infect. Dis. 11 (2011), 868–878.
14. Balmer, O., Stearns, S.C., Schötzau, A., Brun, R., Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology 90 (2009), 3367–3378.
15. Bell, A.S., de Roode, J.C., Sim, D., Read, A.F., Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60 (2006), 1358–1371.
16. Ben-Ami, F., Routtu, J., The expression and evolution of virulence in multiple infections: the role of specificity, relative virulence and relative dose. BMC Evol. Biol., 13, 2013, 97.
17. Ben-Ami, F., Mouton, L., Ebert, D., The effects of multiple infections on the expression and evolution of virulence in a Daphnia–endoparasite system. Evolution 62 (2008), 1700–1711.
18. Bharaj, P., Chahar, H.S., Pandey, A., Diddi, K., Dar, L., Guleria, R., Kabra, S.K., Broor, S., Concurrent infections by all four dengue virus serotypes during an outbreak of dengue in 2006 in Delhi, India. Virol. J., 5, 2008, 1.
19. Bieger, A., Ebert, D., Expression of parasite virulence at different host population densities under natural conditions. Oecologia 160 (2009), 247–255.
20. Boldin, B., Diekmann, O., Superinfections can induce evolutionarily stable coexistence of pathogens. J. Math. Biol. 56 (2008), 635–672.
21. Bose, J., Schulte, R.D., Testing GxG interactions between coinfecting microbial parasite genotypes within hosts. Front. Genet. 5 (2014), 1–9.
22. Bremermann, H.J., Pickering, J., A game-theoretical model of parasite virulence. J. Theor. Biol. 100 (1983), 411–426.
23. Brown, M.J.F., Loosli, R., Schmid-Hempel, P., Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91 (2000), 421–427.
24. Brown, S.P., Grenfell, B.T., An unlikely partnership: parasites, concomitant immunity and host defence. Proc. Biol. Sci. 268 (2001), 2543–2549.
25. Brown, S.P., Johnstone, R.A., Cooperation in the dark: signalling and collective action in quorum-sensing bacteria. Proc. R. Soc. B 268 (2001), 961–965.
26. Brown, S.P., Hochberg, M.E., Grenfell, B.T., Does multiple infection select for raised virulence?. Trends Microbiol. 10 (2002), 401–405.
27. Buckling, A., Brockhurst, M.A., Kin selection and the evolution of virulence. Heredity 100 (2008), 484–488.
28. Buono, L., Lopez-Villavicencio, M., Shykoff, J.A., Snirc, A., Giraud, T., Influence of multiple infection and relatedness on virulence: disease dynamics in an experimental plant population and its castrating parasite. PLoS One, 9, 2014, e98526.
29. Chao, L., Hanley, K.A., Burch, C.L., Dahlberg, C., Turner, P.E., Kin selection and parasite evolution: higher and lower virulence with hard and soft selection. Q. Rev. Biol. 75 (2000), 261–275.
30. Choisy, M., de Roode, J.C., Mixed infections and the evolution of virulence: effects of resource competition parasite plasticity, and impaired host immunity. Am. Nat. 175 (2010), E105–E118.
31. Cooper, T.F., Heinemann, J.A., Selection for plasmid post-segregational killing depends on multiple infection: evidence for the selection of more virulent parasites through parasite-level competition. Proc. Biol. Sci. 272 (2005), 403–410.
32. Cox, F.E., Concomitant infections, parasites and immune responses. Parasitology 122 (2001), S23–S38.
33. Davies, C.M., Fairbrother, E., Webster, J.P., Mixed strain schistosome infections of snails and the evolution of parasite virulence. Parasitology 124 (2002), 31–38.
34. Day, T., Proulx, S.R., A general theory for the evolutionary dynamics of virulence. Am. Nat. 163 (2004), E40–E63.
35. de Roode, J.C., Culleton, R., Cheesman, S.J., Carter, R., Read, A.F., Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections. Proc. Biol. Sci. 271 (2004), 1073–1080.
36. de Roode, J.C., Helinski, M.E.H., Anwar, M.A., Read, A.F., Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. Am. Nat. 166 (2005), 531–542.
37. de Roode, J.C., Pansini, R., Cheesman, S.J., Helinski, M.E.H., Huijben, S., Wargo, A.R., Bell, A.S., Chan, B.H.K., Walliker, D., Read, A.F., Virulence and competitive ability in genetically diverse malaria infections. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 7624–7628.
38. Ding, C., Festa, R.A., Sun, T.S., Wang, Z.Y., Iron and copper as virulence modulators in human fungal pathogens. Mol. Microbiol. 93 (2014), 10–23.
39. Doumayrou, J., Avellan, A., Froissart, R., Michalakis, Y., An experimental test of the transmission-virulence trade-off hypothesis in a plant virus. Evolution 67 (2013), 477–486.
40. Dwyer, G., Levin, S.A., Buttel, L., A simulation model of the population dynamics and evolution of myxomatosis. Ecol. Monogr. 60 (1990), 423–447.
41. Ebert, D., Bull, J.J., Challenging the trade-off model for the evolution of virulence: is virulence management feasible?. Trends Microbiol. 11 (2003), 15–20.
42. Ebert, D., Mangin, K.L.K., The influence of host demography on the evolution of virulence of a microsporidian gut parasite. Evolution 51 (1997), 1828–1837.
43. Escriu, F., Fraile, A., García-Arenal, F., Evolution of virulence in natural populations of the satellite RNA of cucumber mosaic virus. Phytopathology 90 (2000), 480–485.
44. Evison, S.E.F., Foley, K., Jensen, A.B., Hughes, W.O.H., Genetic diversity, virulence and fitness evolution in an obligate fungal parasite of bees. J. Evol. Biol. 28 (2015), 1–10.
45. Ewald, P.W., Host–parasite relations, vectors, and the evolution of disease severity. Annu. Rev. Ecol. Syst. 14 (1983), 465–485.
46. Frank, S.A., Models of parasite virulence. Q. Rev. Biol. 71 (1996), 37–78.
47. Frank, S.A., Foundations of Social Evolution. 1998, Princeton University Press, Princeton.
48. Fraser, C., Hollingsworth, T.D., Chapman, R., de Wolf, F., Hanage, W.P., Variation in HIV-1 set-point viral load: epidemiological analysis and an evolutionary hypothesis. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 17441–17446.
49. Gandon, S., Mackinnon, M.J., Nee, S., Read, A.F., Imperfect vaccines and the evolution of pathogen virulence. Nature 414 (2001), 751–756.
50. Garbutt, J., Bonsall, M.B., Wright, D.J., Raymond, B., Antagonistic competition moderates virulence in Bacillus thuringiensis. Ecol. Lett. 14 (2011), 765–772.
51. Gardner, A., West, S.A., Spite and the scale of competition. J. Evol. Biol. 17 (2004), 1195–1203.
52. Gardner, A., West, S.A., Buckling, A., Bacteriocins, spite and virulence. Proc. R. Soc. B 271 (2004), 1529–1535.
53. Gower, C.M., Webster, J.P., Intraspecific competition and the evolution of virulence in a parasitic trematode. Evolution 59 (2005), 544–553.
54. Hamilton, W.D., The genetical evolution of social behaviour. I. J. Theor. Biol. 7 (1964), 1–16.
55. Hamilton, W.D., The genetical evolution of social behaviour. II. J. Theor. Biol. 7 (1964), 17–52.
56. Hamilton, W.D., Selfish and spiteful behaviour in an evolutionary model. Nature 228 (1970), 1218–1220.
57. Hansen, J., Day, T., Coinfection and the evolution of drug-resistence. J. Evol. Biol. 27 (2014), 2595–2604.
58. Harrison, F., Browning, L.E., Vos, M., Buckling, A., Cooperation and virulence in acute Pseudomonas aeruginosa infections. BMC Biol., 4, 2006, 21.
59. Hodgson, D.J., Hitchman, R.B., Vanbergen, A.J., Hails, R.S., Possee, R.D., Cory, J.S., Host ecology determines the relative fitness of virus genotypes in mixed-genotype nucleopolyhedrovirus infections. J. Evol. Biol. 17 (2004), 1018–1025.
60. Hood, M.E., Dynamics of multiple infection and within-host competition by the anther-smut pathogen. Am. Nat. 162 (2003), 122–133.
61. Imhoof, B., Schmid-Hempel, P., Single-clone and mixed-clone infections versus host environment in Crithidia bombi infecting bumblebees. Parasitology 117 (1998), 331–336.
62. Inglis, R.F., Gardner, A., Cornelis, P., Buckling, A., Spite and virulence in the bacterium Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 5703–5707.
63. Izhar, R., Ben-Ami, F., Host age modulates parasite infectivity, virulence and reproduction. J. Anim. Ecol. 84 (2015), 1018–1028.
64. Jäger, I., Schjørring, S., Multiple infections: relatedness and time between infections affect the establishment and growth of the cestode Schistocephalus solidus in its stickleback host. Evolution 60 (2006), 616–622.
65. Jensen, K.H., Little, T., Skorping, A., Ebert, D., Empirical support for optimal virulence in a castrating parasite. PLoS Biol., 4, 2006, e197.
66. Jokela, J., Lively, C.M., Taskinen, J., Peters, A.D., Effect of starvation on parasite-induced mortality in a freshwater snail (Potamopyrgus antipodarum). Oecologia 119 (1999), 320–325.
67. Karvonen, A., Rellstab, C., Louhi, K.-R., Jokela, J., Synchronous attack is advantageous: mixed genotype infections lead to higher infection success in trematode parasites. Proc. R. Soc. B 279 (2012), 171–176.
68. Konkel, M.E., Tilly, K., Temperature-regulated expression of bacterial virulence genes. Microbes Infect. 2 (2000), 157–166.
69. Koskella, B., Giraud, T., Hood, M.E., Pathogen relatedness affects the prevalence of within-host competition. Am. Nat. 168 (2006), 121–126.
70. Lagrue, C., McEwan, J., Poulin, R., Keeney, D.B., Co-occurrences of parasite clones and altered host phenotype in a snail–trematode system. Int. J. Parasitol. 37 (2007), 1459–1467.
71. Lamont, I.L., Beare, P.A., Ochsner, U., Vasil, A.I., Vasil, M.L., Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 7072–7077.
72. Leggett, H.C., Benmayor, R., Hodgson, D.J., Buckling, A., Experimental evolution of adaptive phenotypic plasticity in a parasite. Curr. Biol. 23 (2013), 139–142.
73. Leggett, H.C., Brown, S.P., Reece, S.E., War and peace: social interactions in infections. Phil. Trans. R. Soc. Lond. B, 369, 2014, 20130365.
74. Levin, B.R., Bull, J.J., Short-sighted evolution and the virulence of pathogenic microorganisms. Trends Microbiol. 2 (1994), 76–81.
75. Levin, S., Pimentel, D., Selection of intermediate rates of increase in parasite–host systems. Am. Nat. 117 (1981), 308–315.
76. Lion, S., Multiple infections, kin selection and the evolutionary epidemiology of parasite traits. J. Evol. Biol. 26 (2013), 2107–2122.
77. Lively, C.M., Johnson, S.G., Delph, L.F., Clay, K., Thinning reduces the effect of rust infection on jewelweed (Impatiens capensis). Ecology 76 (1995), 1859–1862.
78. Lopez-Medina, E., Fan, D., Coughlin, L.A., Ho, E.X., Lamont, I.L., Reimmann, C., Hooper, L.V., Koh, A.Y., Candida albicans inhibits Pseudomonas aeruginosa virulence through suppression of pyochelin and pyoverdine biosynthesis. PLoS Pathog., 11, 2015, e1005129.
79. López-Villavicencio, M., Jonot, O., Coantic, A., Hood, M.E., Enjalbert, J., Giraud, T., Multiple infections by the anther smut pathogen are frequent and involve related strains. PLoS Pathog., 3, 2007, e176.
80. Lord, C.C., Barnard, B., Day, K., Hargrove, J.W., McNamara, J.J., Paul, R.E., Trenholme, K., Woolhouse, M.E., Aggregation and distribution of strains in microparasites. Phil. Trans. R. Soc. Lond. B 354 (1999), 799–807.
81. Louhi, K.R., Karvonen, A., Rellstab, C., Louhi, R., Jokela, J., Prevalence of infection as a predictor of multiple genotype infection frequency in parasites with multiple-host life cycle. J. Anim. Ecol. 82 (2013), 191–200.
82. Louhi, K.R., Sundberg, L.R., Jokela, J., Karvonen, A., Interactions among bacterial strains and fluke genotypes shape virulence of co-infection. Proc. R. Soc. B, 282, 2015, 20152097.
83. Luijckx, P., Ben-Ami, F., Mouton, L., Du Pasquier, L., Ebert, D., Cloning of the unculturable parasite Pasteuria ramosa and its Daphnia host reveals extreme genotype–genotype interactions. Ecol. Lett. 14 (2011), 125–131.
84. Mackinnon, M.J., Read, A.F., Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53 (1999), 689–703.
85. Mackinnon, M.J., Read, A.F., Virulence in malaria: an evolutionary viewpoint. Phil. Trans. R. Soc. Lond. B 359 (2004), 965–986.
86. Masri, L., Branca, A., Sheppard, A.E., Papkou, A., Laehnemann, D., Guenther, P.S., Prahl, S., Saebelfeld, M., Hollensteiner, Liesegang, H., Brzuskiewicz, E., Daniel, R., Michiels, N.K., Schulte, R.D., Kurtz, J., Rosenstiel, P., Telschow, A., Bornberg-Bauer, E., Schulenburg, H., Host–pathogen coevolution: the selective advantage of Bacillus thuringiensis virulence and its Cry toxin genes. PLoS Biol., 13, 2015, e1002169.
87. Massad, E., Transmission rates and the evolution of pathogenicity. Evolution 41 (1987), 1127–1130.
88. Mideo, N., Parasite adaptations to within-host competition. Trends Parasitol. 25 (2009), 261–268.
89. Mideo, N., Alizon, S., Day, T., Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol. Evol. 23 (2008), 511–517.
90. Nowak, M.A., May, R.M., Superinfection and the evolution of parasite virulence. Proc. Biol. Sci. 255 (1994), 81–89.
91. Paul, R.E.L., Lafond, T., Müller-Graf, C.D.M., Nithiuthai, S., Brey, P.T., Koella, J.C., Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections. BMC Evol. Biol., 4, 2004, 30.
92. Petney, T.N., Andrews, R.H., Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. Int. J. Parasitol. 28 (1998), 377–393.
93. Pollitt, E.J.G., West, S.A., Crusz, S.A., Burton-Chellew, M.N., Diggle, S.P., Cooperation quorum sensing, and evolution of virulence in Staphylococcus aureus. Infect. Immun. 82 (2014), 1045–1051.
94. Pollitt, L.C., Bram, J.T., Blanford, S., Jones, M.J., Read, F., Existing infection facilitates establishment and density of malaria parasites in their mosquito vector. PLoS Pathog., 11, 2015, e1005003.
95. Råberg, L., de Roode, J.C., Bell, A.S., Stamou, P., Gray, D., Read, A.F., The role of immune-mediated apparent competition in genetically diverse malaria infections. Am. Nat. 168 (2006), 41–53.
96. Rauch, G., Kalbe, M., Reusch, T.B.H., Partitioning average competition and extreme-genotype effects in genetically diverse infections. Oikos 117 (2008), 399–405.
97. Raymond, B., Davis, D., Bonsall, M.B., Competition and reproduction in mixed infections of pathogenic and non-pathogenic Bacillus spp. J. Invertebr. Pathol. 96 (2007), 151–155.
98. Read, A.F., The evolution of virulence. Trends Microbiol. 2 (1994), 73–76.
99. Read, A.F., Taylor, L.H., The ecology of genetically diverse infections. Science 292 (2001), 1099–1102.
100. Restif, O., Kaltz, O., Condition-dependent virulence in a horizontally and vertically transmitted bacterial parasite. Oikos 114 (2006), 148–158.
101. Rigaud, T., Perrot-Minnot, M.-J., Brown, M.J.F., Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proc. R. Soc. B 277 (2010), 3693–3702.
102. Riley, M.A., Wertz, J.E., Bacteriocins: evolution, ecology, and application. Annu. Rev. Microbiol. 56 (2002), 117–137.
103. Rumbaugh, K.P., Diggle, S.P., Watters, C.M., Ross-Gillespie, A., Griffin, A.S., West, S.A., Quorum sensing and the social evolution of bacterial virulence. Curr. Biol. 19 (2009), 341–345.
104. Salvaudon, L., Héraudet, V., Shykoff, J.A., Genotype-specific interactions and the trade-off between host and parasite fitness. BMC Evol. Biol., 7, 2007, 189.
105. Schjørring, S., Koella, J.C., Sub-lethal effects of pathogens can lead to the evolution of lower virulence in multiple infections. Proc. Biol. Sci. 270 (2003), 189–193.
106. Schmid-Hempel, P., Evolutionary Parasitology. 2011, Oxford University Press, Oxford.
107. Schulenburg, H., Ewbank, J.J., Diversity and specificity in the interaction between Caenorhabditis elegans and the pathogen Serratia marcescens. BMC Evol. Biol., 4, 2004, 49.
108. Seppälä, O., Karvonen, A., Rellstab, C., Louhi, K.-R., Jokela, J., Reciprocal interaction matrix reveals complex genetic and dose-dependent specificity among coinfecting parasites. Am. Nat. 180 (2012), 306–315.
109. Sharp, G.B., Kawaoka, Y., Jones, D.J., Bean, W.J., Pryor, S.P., Hinshaw, V., Webster, R.G., Coinfection of wild ducks by influenza A viruses: distribution patterns and biological significance. J. Virol. 71 (1997), 6128–6135.
110. Smith, J., Superinfection drives virulence evolution in experimental populations of bacteria and plasmids. Evolution 65 (2011), 831–841.
111. Sofonea, M.T., Alizon, S., Michalakis, Y., From within-host interactions to epidemiological competition: a general model for multiple infections. Phil. Trans. R. Soc. B, 370, 2015, 20140303.
112. Strandh, M., Råberg, L., Within-host competition between Borrelia afzelii ospC strains in wild hosts as revealed by massively parallel amplicon sequencing. Phil. Trans. R. Soc. Lond. B, 370, 2015, 20140293.
113. Susi, H., Barrès, B., Vale, P.F., Laine, A.-L., Co-infection alters population dynamics of infectious disease. Nat. Commun., 6, 2015, 5975.
114. Susi, H., Vale, P.F., Laine, A.-L., Host genotype and coinfection modify the relationship of within and between host transmission. Am. Nat. 186 (2015), 252–263.
115. Taylor, L.H., Walliker, D., Read, A.F., Mixed-genotype infections of the rodent malaria Plasmodium chabaudi are more infectious to mosquitoes than single-genotype infections. Parasitology 115 (1997), 121–132.
116. Taylor, L.H., Walliker, D., Read, A.F., Mixed-genotype infections of malaria parasites: within-host dynamics and transmission success of competing clones. Proc. Biol. Sci. 264 (1997), 927–935.
117. Taylor, L.H., Mackinnon, M.J., Read, A.F., Virulence of mixed-clone and single-clone infections of the rodent malaria Plasmodium chabaudi. Evolution 52 (1998), 583–591.
118. Taylor, L.H., Welburn, S.C., Woolhouse, M.E.J., Theileria annulata: virulence and transmission from single and mixed clone infections in cattle. Exp. Parasitol. 100 (2002), 186–195.
119. Turner, P.E., Chao, L., Sex and the evolution of intrahost competition in RNA virus phi6. Genetics 150 (1998), 523–532.
120. Turner, P.E., Chao, L., Prisoner's dilemma in an RNA virus. Nature 398 (1999), 441–443.
121. Turner, P.E., Chao, L., Escape from prisoner's dilemma in RNA phage phi6. Am. Nat. 161 (2003), 497–505.
122. van Baalen, M., Sabelis, M.W., The scope for virulence management: a comment on Ewald's view on the evolution of virulence. Trends Microbiol. 3 (1995), 414–416.
123. van Baalen, M., Sabelis, M.W., The dynamics of multiple infection and the evolution of virulence. Am. Nat. 146 (1995), 881–910.
124. van Leeuwen, E., O'Neill, S., Matthews, A., Raymond, B., Making pathogens sociable: the emergence of high relatedness through limited host invasibility. ISME J. 9 (2015), 2315–2323.
125. Vardo-Zalik, A.M., Schall, J.J., Clonal diversity alters the infection dynamics of a malaria parasite (Plasmodium mexicanum) in its vertebrate host. Ecology 90 (2009), 529–536.
126. Wargo, A., Huijben, S., de Roode, J., Shepherd, J., Read, A., Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 19914–19919.
127. Webster, J.P., Woolhouse, M.E.J., Selection and strain specificity of compatibility between snail intermediate hosts and their parasitic schistosomes. Evolution 52 (1998), 1627–1634.
128. West, S.A., Buckling, A., Cooperation, virulence and siderophore production in bacterial parasites. Proc. R. Soc. B 270 (2003), 37–44.
129. West, S.A., Pen, I., Griffin, A.S., Cooperation and competition between relatives. Science 296 (2002), 72–75.
130. West, S.A., Diggle, S.P., Buckling, A., Gardner, A., Griffin, A.S., The social lives of microbes. Annu. Rev. Ecol. Evol. Syst. 38 (2007), 53–77.
131. Wild, G., Gardner, A., West, S.A., Adaptation and the evolution of parasite virulence in a connected world. Nature 459 (2009), 983–986.
132. Williams, P.D., Dobson, A.P., Dhondt, K.V., Hawley, D.M., Dhondt, A.A., Evidence of trade-offs shaping virulence evolution in an emerging wildlife pathogen. J. Evol. Biol. 27 (2014), 1271–1278.
133. Zwart, M.P., van der Werf, W., van Oers, M.M., Hemerik, L., van Lent, J.M.V., de Visser, J.A.G.M., Vlak, J.M., Cory, J.S., Mixed infections and the competitive fitness of faster-acting genetically modified viruses. Evol. Appl. 2 (2009), 209–221.