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

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Many emerging infectious diseases are the result of a host shift, with the pathogen jumping into the new host from another species. Virulence—the harm a pathogen does to its host—can be extremely high following a host shift (for example HIV, SARs and Ebola), while other host shifts may go undetected as they cause few symptoms in the new host. We have found that variation in virulence following host shifts can be extremely large and were highly predictable from the host phylogeny, with hosts clustering together in distinct clades displaying high or low virulence. These changes in virulence result from changes in viral load, and therefore the transmission potential of the virus. This suggests there is no clear rule to predict whether a pathogen will be virulent in a novel host. However, it does suggest a simple rule of thumb may be that if a pathogen causes high levels of virulence in any given host species, it will typically cause similar levels of virulence in closely related hosts.

Vyšlo v časopise: The Causes and Consequences of Changes in Virulence following Pathogen Host Shifts. PLoS Pathog 11(3): e32767. doi:10.1371/journal.ppat.1004728
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004728

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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 (2008) The evolution and expression of virulence. In: Stearns SC, Koella JC, editors. Evolution in Health and Disease. 2nd ed. Oxford: Oxford University Press. pp. 153–167.

14. Margolis E, Levin BR (2008) The evolution of bacteria-host interactions: virulence and the immune over-response. In: Gutirrez JQ, Baquero F, editors. 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