Evolution of Virulence in Emerging Epidemics

English version České info

Theory predicts that selection for pathogen virulence and horizontal transmission is highest at the onset of an epidemic but decreases thereafter, as the epidemic depletes the pool of susceptible hosts. We tested this prediction by tracking the competition between the latent bacteriophage λ and its virulent mutant λcI857 throughout experimental epidemics taking place in continuous cultures of Escherichia coli. As expected, the virulent λcI857 is strongly favored in the early stage of the epidemic, but loses competition with the latent virus as prevalence increases. We show that the observed transient selection for virulence and horizontal transmission can be fully explained within the framework of evolutionary epidemiology theory. This experimental validation of our predictions is a key step towards a predictive theory for the evolution of virulence in emerging infectious diseases.

Vyšlo v časopise: Evolution of Virulence in Emerging Epidemics. PLoS Pathog 9(3): e32767. doi:10.1371/journal.ppat.1003209
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003209

Souhrn

Zdroje

1. FrankSA (1996) Models of parasite virulence. Q Rev Biol 71: 37–78.

2. Dieckmann U, Metz JAJ, Sabelis MW, Sigmund K (2002) Adaptive dynamics of infectious diseases: in pursuit of virulence management. Cambridge: Cambridge University Press. 532 p.

3. YoshidaT, JonesLE, EllnerSP, FussmannGF, Hairston JrNG (2003) Rapid evolution drives ecological dynamics in a predator-prey system. Nature 424: 303–306.

4. HairstonNG, EllnerSP, GeberMA, YoshidaT, FoxJA (2005) Rapid evolution and the convergence of ecological and evolutionary time. Ecology Letters 8: 1114–1127.

5. BullJJ, MillsteinJ, OrcuttJ, WichmanHA (2006) Evolutionary feedback mediated through population density, illustrated with viruses in chemostats. Am. Nat 167: E39–E51.

6. AristaS, GiammancoGM, De GraziaS, RamirezS, Lo BiundoC, et al. (2006) Heterogeneity and temporal dynamics of evolution of G1 human rotaviruses in a settled population. J Virol 80: 10724–10733.

7. GallimoreCI, Iturriza-GomaraM, XerryJ, AdigweJ, GrayJJ (2007) Inter-seasonal diversity of norovirus genotypes: Emergence and selection of virus variants. Arch Virol 152: 1295–1303.

8. OjosnegrosS, BeerenwinkelN, AntalT, NowakMA, EscarmisC, et al. (2010) Competition-colonization dynamics in an RNA virus. Proc Natl Acad Sci USA 107: 2108–2112.

9. WrightCF, MorelliMJ, ThébaudG, KnowlesNJ, HerzykP, et al. (2011) Beyond the consensus: Dissecting within-host viral population diversity of foot-and-mouth disease virus by using next-generation genome sequencing. J Virol 85: 2266–2275.

10. VijaykrishnaD, SmithGJ, PybusOG, ZhuH, BhattS, et al. (2011) Long-term evolution and transmission dynamics of swine influenza A virus. Nature 473: 519–522.

11. LenskiRE, MayRM (1994) The evolution of virulence in parasites and pathogens: Reconciliation between two competing hypotheses. J Theor Biol 169: 253–265.

12. DayT, GandonS (2007) Applying population-genetic models in theoretical evolutionary epidemiology. Ecol Lett 10: 876–888.

13. BullJJ, EbertD (2008) Invasion thresholds and the evolution of nonequilibrium virulence. Evol Appl 1: 172–182.

14. BolkerBM, NandaA, ShahD (2010) Transient virulence of emerging pathogens. J R Soc Interface 7: 811–822.

15. StewartFM, LevinBR (1984) The population biology of bacterial viruses: why be temperate. Theor Popul Biol 26: 93–117.

16. DayT, ProulxSR (2004) A General Theory for the Evolutionary Dynamics of Virulence. Am. Nat 163: E40–E63.

17. Day T, Gandon S. (2006) Insights from Price's equation into evolutionary epidemiology. In: Feng Z Dieckmann U, Levin S, editors. Disease evolution: models, concepts and data analyses. The American Mathematical Society.

18. GandonS, DayT (2007) The evolutionary epidemiology of vaccination. J R Soc Interface 4: 803–817.

19. Dykhuizen DE, Dean AM. (2009) Experimental Evolution from the Bottom Up. In: Garland T, Rose MR editors. Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments. Berkley: University of California Press.

20. Ptashne M. (1992) A Genetic Switch: Phage Lambda and Higher Organisms. Oxford: Blackwell Publishers.

21. St-PierreF, EndyD (2008) Determination of cell fate selection during phage lambda infection. Proc Natl Acad Sci USA 105: 20705–20710.

22. ZengL, SkinnerSO, ZongC, SippyJ, FeissM, et al. (2010) Decision making at a subcellular level determines the outcome of bacteriophage infection. Cell 141: 682–691.

23. SussmanR, JacobF (1962) Sur un système de répression thermosensible chez le bacteriophage lambda d'Escherichia coli. Comp. Rend 254: 1517–1519.

24. RefardtD, RaineyPB (2010) Tuning a genetic switch: experimental evolution and natural variation of prophage induction. Evolution 64: 1086–1097.25.

25. BailoneA, DevoretR (1978) Isolation of ultra-virulent mutants of phage lambda. Virology 84: 547–550.

26. NorthropJH (1968) Appearance of virulent bacteriophages in lysogenic e. coli cultures after prolonged growth in the presence of triethylenemelamine. J Gen Physiol 52: 136–143.

27. BerngruberTW, WeissingFJ, GandonS (2010) Inhibition of superinfection and the evolution of viral latency. J Virol 84: 10200–10208.

28. ClémentJM, LepouceE, MarchalC, HofnungM (1983) Genetic study of a membrane protein: DNA sequence alterations due to 17 lamB point mutations affecting adsorption of phage lambda. EMBO J 2: 77–80.

29. MeyerJR, DobiasDT, WeitzJS, BarrickJE, QuickRT, et al. (2012) Repeatability and Contingency in the Evolution of a Key Innovation in Phage Lambda. Science 335: 428–432.

30. KourilskyP (1973) Lysogenization by bacteriophage lambda. I. Multiple infection and the lysogenic response. Mol. Gen. Genet 122: 183–195.

31. AvlundM, DoddIB, SemseyS, SneppenK, KrishnaS (2009) Why do phage play dice?. J Virol 83.

32. JohRI, WeitzJS (2011) To lyse or not to lyse: transient-mediated stochastic fate determination in cells infected by bacteriophages. PLoS Comput. Biol 7: e1002006.

33. BullJJ, PfennigDW, WangIN (2004) Genetic details, optimization and phage life histories. Trends Ecol Evol 19: 76–82.

34. BullJJ (2006) Optimality models of phage life history and parallels in disease evolution. J Theor Biol 241: 928–938.

35. MadorN, PanetA, SteinerI (2002) The latency-associated gene of herpes simplex virus type 1 (HSV-1) interferes with superinfection by HSV-1. J Neurovirology 8: 97–102.

36. NetheM, BerkhoutB, van der KuylAC (2005) Retroviral superinfection resistance. Retrovirology 2: 52.

37. GrenfellBT, PybusOG, GogJR, WoodJLN, DalyJM, et al. (2004) Unifying the Epidemiological and Evolutionary Dynamics of Pathogens. Science 303: 327–332.

38. NowakMA, MayRM (1994) Superinfection and the evolution of parasite virulence. Proc R Soc. Lond B 255: 81–89.

39. van BaalenM, SabelisMW (1995) The dynamics of multiple infection and the evolution of virulence. Am Nat 146: 881–910.

40. de RoodeJC, PansiniR, CheesmanSJ, HelsinkiMEH, HuijbenS, et al. (2005) Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad Sci USA 102: 7624–7628.

41. ArienKK, VanhamG, ArtsEJ (2007) Is HIV-1 evolving to a less virulent form in humans? Nat Rev Micro 5: 141–151.

42. TroyerRM, CollinsKR, AbrahaA, FraundorfE, MooreDM, et al. (2005) Changes in Human Immunodeficiency Virus Type 1 Fitness and Genetic Diversity during Disease Progression. J Virol 79: 9006–9018.

43. AdiwijayaBS, KiefferTL, HenshawJ, EisenhauerK, KimkoH, et al. (2012) A viral dynamic model for treatment regimens with directacting antivirals for Chronic Hepatitis C Infection. PLoS Comput Biol 8: e1002339.

44. ReadAF, DayT, HuijbenS (2011) The evolution of drug resistance and the curious orthodoxy of aggressive chemotherapy. Proc Natl Acad Sci USA 108: 10871–10877.

45. AlizonS, LucianiF, RegoesRR (2011) Epidemiological and clinical consequences of within-host evolution. Trends Microbiol 19: 24–32.