The Causes and Consequences of Changes in Virulence following Pathogen Host Shifts

PLoS Pathogens

Volumn 11, Issue 3, 2015, Pages 1-18

  Longdon, Ben ^a   Hadfield, Jarrod D ^b   Day, Jonathan P ^a   Smith, Sophia C L ^a   McGonigle, John E ^a   Cogni, Rodrigo ^a,c   Cao, Chuan ^a   Jiggins, Francis M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DROSOPHILA C VIRUS; DROSOPHILA MELANOGASTER; FEMALE; MALE; MORTALITY; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; VIRUS; VIRUS LOAD; VIRUS TRANSMISSION; VIRUS VIRULENCE; ANIMAL; DROSOPHILA; GENETICS; HOST RANGE; PATHOGENICITY; RNA VIRUS; VIROLOGY; VIRULENCE;

DROSOPHILIDAE; RNA VIRUSES;

ANIMALS; DROSOPHILA; HOST SPECIFICITY; PHYLOGENY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA VIRUSES; VIRAL LOAD; VIRULENCE;

EID: 84926507558     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004728     Document Type: Article

References (84)

1. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, et al. (2008) Global trends in emerging infectious diseases. Nature 451: 990–993. doi: 10.1038/nature06536 18288193
2. Woolhouse ME, Haydon DT, Antia R, (2005) Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol Evol 20: 238–244. 16701375
3. Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, et al. (2005) Fruit bats as reservoirs of Ebola virus. Nature 438: 575–576. 16319873
4. Swanepoel R, Leman PA, Burt FJ, Zachariades NA, Braack LEO, et al. (1996) Experimental inoculation of plants and animals with Ebola virus. Emerging Infectious Diseases 2: 321–325. 8969248
5. Chua KB, Bellini WJ, Rota PA, Harcourt BH, Tamin A, et al. (2000) Nipah virus: a recently emergent deadly paramyxovirus. Science 288: 1432–1435. 10827955
6. Middleton DJ, Morrissy CJ, van der Heide BM, Russell GM, Braun MA, et al. (2007) Experimental Nipah virus infection in pteropid bats (Pteropus poliocephalus). J Comp Pathol 136: 266–272. 17498518
7. 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 19196383
8. Weiss RA, (2002) Virulence and pathogenesis. Trends Microbiol 10: 314–317. 12110209
9. Anderson RM, May RM, (1982) Coevolution of hosts and parasites. Parasitology 85 (Pt 2): 411–426. 6755367
10. Anderson RM, May RM, (1991) Infectious Diseases of humans; dynamics and control. Oxford: Oxford University Press.
11. Read AF, (1994) The evolution of virulence. Trends Microbiol 2: 73–76. 8156274
12. Toft CA, Karter AJ, (1990) Parasite-host coevolution. Trends Ecol Evol 5: 326–329. doi: 10.1016/0169-5347(90)90179-H 21232384
13. Ebert D, Bull JJ, Stearns SC, Koella JC, (2008) The evolution and expression of virulence. In: Evolution in Health and Disease. 2nd ed. Oxford: Oxford University Press. pp. 153–167.
14. Margolis E, Levin BR, Gutirrez JQ, Baquero F, (2008) The evolution of bacteria-host interactions: virulence and the immune over-response. In: Introduction to the evolutionary biology of bacterial and fungal pathogens. Washington D.C.: ASM Press.
15. Graham AL, Allen JE, Read AF, (2005) Evolutionary causes and consequences of immunopathology. Annual Review of Ecology Evolution and Systematics 36: 373–397.
16. Levin BR, Bull JJ, (1994) Short-sighted evolution and the virulence of pathogenic microorganisms. Trends Microbiol 2: 76–81. 8156275
17. Antonovics J, Boots M, Ebert D, Koskella B, Poss M, et al. (2013) The origin of specificity by means of natural selection: evolved and nonhost resistance in host-pathogen interactions. Evolution 67: 1–9. doi: 10.1111/j.1558-5646.2012.01793.x 23289557
18. Jensen KH, Little TJ, Skorping A, Ebert D, (2006) Empirical support for optimal virulence in a castrating parasite. PLoS Biol 4: e197. doi: 10.1371/annotation/6f580f9f-d724-433c-9e12-f402fac28829 16719563
19. Marshall ID, Fenner F, (1958) Studies in the epidemiology of infectious myxomatosis of rabbits. V. Changes in the innate resistance of Australian wild rabbits exposed to myxomatosis. J Hyg (Lond) 56: 288–302. 13563871
20. Kerr PJ, (2012) Myxomatosis in Australia and Europe: a model for emerging infectious diseases. Antiviral Res 93: 387–415. doi: 10.1016/j.antiviral.2012.01.009 22333483
21. de Roode JC, Yates AJ, Altizer S, (2008) Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc Natl Acad Sci U S A 105: 7489–7494. doi: 10.1073/pnas.0710909105 18492806
22. Fraser C, Hollingsworth TD, Chapman R, de Wolf F, Hanage WP, (2007) Variation in HIV-1 set-point viral load: Epidemiological analysis and an evolutionary hypothesis. Proceedings of the National Academy of Sciences of the United States of America 104: 17441–17446. 17954909
23. Blumberg S, Lloyd-Smith JO, (2013) Inference of R(0) and transmission heterogeneity from the size distribution of stuttering chains. PLoS Comput Biol 9: e1002993. doi: 10.1371/journal.pcbi.1002993 23658504
24. Andre JB, Hochberg ME, (2005) Virulence evolution in emerging infectious diseases. Evolution 59: 1406–1412. 16153027
25. Fenner F, Ratcliffe FN, (1965) Myxomatosis. Cambridge: Cambridge University press.
26. Engelstadter J, Hurst GD, (2006) The dynamics of parasite incidence across host species. Evolutionary Ecology 20: 603–616.
27. Waxman D, Weinert LA, Welch JJ, (2014) Inferring host range dynamics from comparative data: the protozoan parasites of new world monkeys. Am Nat 184: 65–74. doi: 10.1086/676589 24921601
28. Longdon B, Brockhurst MA, Russell CA, Welch JJ, Jiggins FM, (2014) The Evolution and Genetics of Virus Host Shifts. PLoS Pathog 10: e1004395. doi: 10.1371/journal.ppat.1004395 25375777
29. Faria NR, Suchard MA, Rambaut A, Streicker DG, Lemey P, (2013) Simultaneously reconstructing viral cross-species transmission history and identifying the underlying constraints. Philos Trans R Soc Lond B Biol Sci 368: 20120196. doi: 10.1098/rstb.2012.0196 23382420
30. Longdon B, Hadfield JD, Webster CL, Obbard DJ, Jiggins FM, (2011) Host phylogeny determines viral persistence and replication in novel hosts. PLoS Pathogens 7: e1002260. doi: 10.1371/journal.ppat.1002260 21966271
31. Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF, et al. (2010) Host Phylogeny Constrains Cross-Species Emergence and Establishment of Rabies Virus in Bats. Science 329: 676–679. doi: 10.1126/science.1188836 20689015
32. de Vienne DM, Hood ME, Giraud T, (2009) Phylogenetic determinants of potential host shifts in fungal pathogens. Journal of Evolutionary Biology 22: 2532–2541. doi: 10.1111/j.1420-9101.2009.01878.x 19878406
33. Gilbert GS, Webb CO, (2007) Phylogenetic signal in plant pathogen-host range. Proceedings of the National Academy of Sciences of the United States of America 104: 4979–4983. 17360396
34. Perlman SJ, Jaenike J, (2003) Infection success in novel hosts: An experimental and phylogenetic study of Drosophila-parasitic nematodes. Evolution 57: 544–557. 12703944
35. Tinsley MC, Majerus MEN, (2007) Small steps or giant leaps for male-killers? Phylogenetic constraints to male-killer host shifts. Bmc Evolutionary Biology 7.
36. Jiggins FM, Kim KW, (2005) The evolution of antifungal peptides in Drosophila. Genetics 171: 1847–1859. 16157672
37. Salazar-Jaramillo L, Paspati A, van de Zande L, Vermeulen CJ, Schwander T, et al. (2014) Evolution of a cellular immune response in Drosophila: a phenotypic and genomic comparative analysis. Genome Biology and Evolution.
38. Christian PD, (1987) Studies of Drosophila C and A viruses in Australian populations of Drosophila melanogaster: Australian National University. 305 p.
39. Kapun M, Nolte V, Flatt T, Schlotterer C, (2010) Host Range and Specificity of the Drosophila C Virus. Plos One 5: e12421. doi: 10.1371/journal.pone.0012421 20865043
40. Jousset FX, (1976) Host Range of Drosophila-Melanogaster C Virus among Diptera and Lepidoptera. Annales De Microbiologie A127: 529–&. 823856
41. Chtarbanova S, (2011) Tissue-specific pathologies induced by two RNA viruses in Drosophila melanogaster: University of Strasbourg.
42. Arnold PA, Johnson KN, White CR, (2013) Physiological and metabolic consequences of viral infection in Drosophila melanogaster. J Exp Biol 216: 3350–3357. doi: 10.1242/jeb.088138 23685974
43. Chtarbanova S, Lamiable O, Lee KZ, Galiana D, Troxler L, et al. (2014) Drosophila C virus systemic infection leads to intestinal obstruction. J Virol 88: 14057–14069. doi: 10.1128/JVI.02320-14 25253354
44. Ferreira AG, Naylor H, Esteves SS, Pais IS, Martins NE, et al. (2014) The toll-dorsal pathway is required for resistance to viral oral infection in Drosophila. PLoS Pathog 10: e1004507. doi: 10.1371/journal.ppat.1004507 25473839
45. Dostert C, Jouanguy E, Irving P, Troxler L, Galiana-Arnoux D, et al. (2005) The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of drosophila. Nat Immunol 6: 946–953. 16086017
46. Kemp C, Mueller S, Goto A, Barbier V, Paro S, et al. (2013) Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. J Immunol 190: 650–658. doi: 10.4049/jimmunol.1102486 23255357
47. Teixeira L, Ferreira A, Ashburner M, (2008) The Bacterial Symbiont Wolbachia Induces Resistance to RNA Viral Infections in Drosophila melanogaster. Plos Biology 6: 2753–2763.
48. Longdon B, Cao C, Martinez J, Jiggins FM, (2013) Previous Exposure to an RNA Virus Does Not Protect against Subsequent Infection in Drosophila melanogaster. Plos One 8: e73833. doi: 10.1371/journal.pone.0073833 24040086
49. Jousset FX, Plus N, Croizier G, Thomas M, (1972) [Existence in Drosophila of 2 groups of picornavirus with different biological and serological properties]. C R Acad Sci Hebd Seances Acad Sci D 275: 3043–3046. 4631976
50. Sullivan W, Ashburner M, Hawley S, (2000) Drosophila Protocols. New York: Cold Spring Harbor Laboratory Press.
51. Reed LJ, Muench H, (1938) A simple method of estimating fifty per cent endpoints. The American Journal of Hygiene 27: 493–497.
52. Obbard DJ, Maclennan J, Kim K-W, Rambaut A, O’Grady PM, et al. (2012) Estimating divergence dates and substitution rates in the Drosophila phylogeny. Molecular Biology and Evolution 29: 3459–3473. doi: 10.1093/molbev/mss150 22683811
53. Zhou W, Rousset F, O'Neil S, (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci 265: 509–515. 9569669
54. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN, (2008) Wolbachia and Virus Protection in Insects. Science 322: 702–702. doi: 10.1126/science.1162418 18974344
55. Huey RB, Moreteau B, Moreteau JC, Gibert P, Gilchrist GW, et al. (2006) Sexual size dimorphism in a Drosophila clade, the D-obscura group. Zoology 109: 318–330. 16978850
56. Sokoloff A, (1966) Morphological Variation in Natural and Experimental Populations of Drosophila Pseudoobscura and Drosophila Persimilis. Evolution 20: 49–71.
57. Gilchrist GW, Huey RB, Serra L, (2001) Rapid evolution of wing size clines in Drosophila subobscura. Genetica 112–113: 273–286.
58. Rasband WS (1997–2011) ImageJ, U. S. National Institutes of Health, Bethesda,Maryland, USA. Available: http://imagej.nih.gov/ij/. v1.43u ed.
59. Drummond AJ, Rambaut A, (2007) BEAST: Bayesian evolutionary analysis by sampling trees. Bmc Evolutionary Biology 7: 214. 17996036
60. Hasegawa M, Kishino H, Yano TA, (1985) DATING OF THE HUMAN APE SPLITTING BY A MOLECULAR CLOCK OF MITOCHONDRIAL-DNA. Journal of Molecular Evolution 22: 160–174. 3934395
61. Shapiro B, Rambaut A, Drummond AJ, (2006) Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23: 7–9. 16177232
62. Rambaut A, Drummond AJ (2007) Tracer v14, Available from http://beast.bio.ed.ac.uk/Tracer
63. Rambaut A (2011) FigTree. v1.3 ed.
64. Hadfield JD, Nakagawa S, (2010) General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. Journal of Evolutionary Biology 23: 494–508. doi: 10.1111/j.1420-9101.2009.01915.x 20070460
65. Housworth EA, Martins EP, Lynch M, (2004) The phylogenetic mixed model. American Naturalist 163: 84–96. 14767838
66. Lynch M, (1991) METHODS FOR THE ANALYSIS OF COMPARATIVE DATA IN EVOLUTIONARY BIOLOGY. Evolution 45: 1065–1080.
67. Hadfield JD, (2010) MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package. Journal of Statistical Software 33: 1–22. 20808728
68. Aalen OO, Borgan Ø, Gjessing HK, (2008) Survival and Event History Analysis: A Process Point of View. New York: Springer.
69. Bennett S, (1983) Log-Logistic Regression-Models for Survival-Data. Applied Statistics-Journal of the Royal Statistical Society Series C 32: 165–171.
70. van der Linde K, Houle D, Spicer GS, Steppan SJ, (2010) A supermatrix-based molecular phylogeny of the family Drosophilidae. Genetics Research 92: 25–38. doi: 10.1017/S001667231000008X 20433773
71. Pagel M, (1999) Inferring the historical patterns of biological evolution. Nature 401: 877–884. 10553904
72. Murphy WJ, Pringle TH, Crider TA, Springer MS, Miller W, (2007) Using genomic data to unravel the root of the placental mammal phylogeny. Genome Research 17: 413–421. 17322288
73. Welch J, Bininda-Emonds O, Bromham L, (2008) Correlates of substitution rate variation in mammalian protein-coding sequences. Bmc Evolutionary Biology 8: 53. doi: 10.1186/1471-2148-8-53 18284663
74. Thomas JA, Welch JJ, Lanfear R, Bromham L, (2010) A Generation Time Effect on the Rate of Molecular Evolution in Invertebrates. Molecular Biology and Evolution 27: 1173–1180. doi: 10.1093/molbev/msq009 20083649
75. Truyen U, Evermann JF, Vieler E, Parrish CR, (1996) Evolution of canine parvovirus involved loss and gain of feline host range. Virology 215: 186–189. 8560765
76. van Rij RP, Saleh MC, Berry B, Foo C, Houk A, et al. (2006) The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes & Development 20: 2985–2995.
77. van Mierlo JT, Overheul GJ, Obadia B, van Cleef KW, Webster CL, et al. (2014) Novel Drosophila viruses encode host-specific suppressors of RNAi. PLoS Pathog 10: e1004256. doi: 10.1371/journal.ppat.1004256 25032815
78. Magwire MM, Fabian DK, Schweyen H, Cao C, Longdon B, et al. (2012) Genome-wide association studies reveal a simple genetic basis of resistance to naturally coevolving viruses in Drosophila melanogaster. Plos Genetics 8: e1003057. doi: 10.1371/journal.pgen.1003057 23166512
79. Ebert D, Bull JJ, (2003) Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends in Microbiology 11: 15–20. 12526850
80. Frank SA, Schmid-Hempel P, (2008) Mechanisms of pathogenesis and the evolution of parasite virulence. J Evol Biol 21: 396–404. doi: 10.1111/j.1420-9101.2007.01480.x 18179516
81. Boots M, Sasaki A, (1999) ‘Small worlds’ and the evolution of virulence: infection occurs locally and at a distance. 1933–1938 p.
82. Vale PF, Choisy M, Little TJ, (2013) Host nutrition alters the variance in parasite transmission potential. Biol Lett 9: 20121145. doi: 10.1098/rsbl.2012.1145 23407498
83. Martinez J, Longdon B, Bauer S, Chan YS, Miller WJ, et al. (2014) Symbionts commonly provide broad spectrum resistance to viruses in insects: a comparative analysis of Wolbachia strains. PLoS Pathog 10: e1004369. doi: 10.1371/journal.ppat.1004369 25233341
84. Russo CA, Takezaki N, Nei M, (1995) Molecular phylogeny and divergence times of drosophilid species. Mol Biol Evol 12: 391–404. 7739381