Experimental selection reveals a trade-off between fecundity and lifespan in the coliphage Qß

Open Biology

Volumn 3, Issue JUN, 2013, Pages

  García Villada, Libertad ^a   Drake, John W ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Bacteriophage Q ; Phage evolutionary constraints; Phage fecundity lifespan trade off; Phage life history evolution

Indexed keywords

ARTICLE; BACTERIOPHAGE QSS; COLIPHAGE; ESCHERICHIA COLI; FERTILITY; GENETIC SELECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOLECULAR EVOLUTION; PHAGE EVOLUTIONARY CONSTRAINTS; PHAGE FECUNDITY/LIFESPAN TRADE-OFF; PHAGE LIFE-HISTORY EVOLUTION; PHYSIOLOGY; VIROLOGY; VIRUS GENOME; ALLOLEVIVIRUS;

BACTERIOPHAGE QSS; PHAGE EVOLUTIONARY CONSTRAINTS; PHAGE FECUNDITY/LIFESPAN TRADE-OFF; PHAGE LIFE-HISTORY EVOLUTION;

ALLOLEVIVIRUS; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; FERTILITY; GENOME, VIRAL; SELECTION, GENETIC;

EID: 84885593764     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.130043     Document Type: Article

References (43)

1. Williams GC. 1966 Natural selection, the costs of reproduction, and a refinement of Lack's principle. Am. Nat. 100, 687-690. See http://www.jstor.org/ stable/2459305.
2. Futuyma DJ. 1998 Evolutionary biology, 3rd edn. Sunderland, MA: Sinauer Associates, Inc.
3. Reznick D. 1985 Costs of reproduction: an evaluation of the empirical evidence. Oikos 44, 257-267. See http://www.jstor.org/stable/3544698. (Pubitemid 16280805)
4. Shao Y, Wang I-N. 2008 Bacteriophage adsorption rate and optimal lysis time. Genetics 180, 471-482. (doi:10.1534/genetics.108.090100)
5. Dennehy JJ. 2009 Bacteriophages as model organisms for virus emergence research. Trends Microbiol. 17, 450-457. (doi:10.1016/j.tim.2009.07.006)
6. De Paepe M, Taddei F. 2006 Viruses' life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biol. 4, e193. (doi:10.1371/journal.pbio.0040193)
7. Tuomi J, Hakala T, Haukioja E. 1983 Alternative concepts of reproductive effort, costs of reproduction, and selection in life-history evolution. Am. Zool. 23, 25-34. (doi:10.1093/icb/23.1.25)
8. Abedon ST, Hyman P, Thomas C. 2003 Experimental examination of bacteriophage latent-period evolution as a response to bacterial availability. Appl. Environ. Microbiol. 69, 7499-7506. (doi:10.1128/AEM.69.12.7499-7506.2003) (Pubitemid 38585406)
9. Heineman RH, Bull JJ. 2007 Testing optimality with experimental evolution: lysis time in a bacteriophage. Evolution 61, 1695-1709. (doi:10.1111/j.1558-5646.2007.00132.x) (Pubitemid 47013467)
10. Chantranupong L, Heineman RH. 2012 A common, non-optimal phenotypic endpoint in experimental adaptations of bacteriophage lysis time. BMC Evol. Biol. 12, 37. (doi:10.1186/1471-2148-12-37)
11. Stent GS. 1963 In Molecular biology of bacterial viruses (ed. DM Whitaker, R Emerson, D Kennedy, GW Beadle), 1st edn. San Francisco, CA: W.H. Freeman and Company.
12. Lenski RE, Travisano M. 1994 Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc. Natl Acad. Sci. USA 91, 6808-6814. (doi:10.1073/pnas.91.15.6808) (Pubitemid 24226751)
13. Novella IS, Duarte EA, Elena SF, Moya A, Domingo E, Holland JJ. 1995 Exponential increases of RNA virus fitness during large population transmissions. Proc. Natl Acad. Sci. USA 92, 5841-5844. (doi:10.1073/pnas.92.13. 5841)
14. Wichman HA, Badgett MR, Scott LA, Boulianne CM, Bull JJ. 1999 Different trajectories of parallel evolution during viral adaptation. Science 285, 422-424. (doi:10.1126/science.285.5426.422) (Pubitemid 29343967)
15. Elena SF, Sanjuán R. 2007 Virus evolution: insights from an experimental approach. Annu. Rev. Ecol. Evol. Syst. 38, 27-52. (doi:10.1146/annurev.ecolsys. 38.091206.095637)
16. Abedon ST. 1989 Selection for bacteriophage latent period length by bacterial density: a theoretical examination. Microb. Ecol. 18, 79-88. (doi:10.1007/BF02030117) (Pubitemid 19253378)
17. Wang I-N, Dykhuizen DE, Slobodkin LB. 1996 The evolution of phage lysis time. Evol. Ecol. 10, 545-558. (doi:10.1007/BF01237884)
18. Van Duin J, Tsareva N. 2006 Single-stranded RNA phages. In The bacteriophages (ed. R Calendar), pp. 175-196, 2nd edn. New York, NY: Oxford University Press.
19. Doermann AH. 1952 The intracellular growth of bacteriophages. I. Liberation of intracellular bacteriophage T4 by premature lysis with another phage or with cyanide. J. Gen. Physiol. 35, 645-656. (doi:10.1085/jgp.35.4.645)
20. Anderson TF, Doermann AH. 1952 The intracellular growth of bacteriophages. II. The growth of T3 studied by sonic disintegration and by T6-cyanide lysis of infected cells. J. Gen. Physiol. 35, 657-667. (doi:10.1085/jgp.35.4.657)
21. Hutchison III CA, Sinsheimer RL. 1966 The process of infection with bacteriophage fX174. X. Mutations in a fX lysis gene. J. Mol. Biol. 18, 429-447. (doi:10.1016/S0022-2836(66)80035-9)
22. Wang I-N. 2006 Lysis timing and bacteriophage fitness. Genetics 172, 17-26. (doi:10.1534/genetics.105.045922) (Pubitemid 43345469)
23. Adams MH. 1959 Bacteriophages, 1st edn. New York, NY: Interscience Publishers, Inc.
24. Heineman RH, Brown SP. 2012 Experimental evolution of a bacteriophage virus reveals the trajectory of adaptation across a fecundity/longevity trade-off. PLoS ONE 7, e46322. (doi:10.1371/journal.pone.0046322)
25. Díez J, Dávila M, Escarmís C, Mateu MG, Dominguez J, Peŕez JJ, Giralt E, Melero JA, Domingo E. 1990 Unique amino acid substitutions in the capsid proteins of foot-and-mouth disease virus from a persistent infection in cell culture. J. Virol. 64, 5519-5528. (accession no. WOS:A1990EE04800036) (Pubitemid 20364546)
26. Ojosnegros S, García-Arriaza J, Escarmís C, Manrubia SC, Perales C, Arias A, García Mateu M, Domingo E. 2011 Viral genome segmentation can result from a trade-off between genetic content and particle stability. PLoS Genet. 7, e1001344. (doi:10.1371/journal.pgen.10011344)
27. García-Villada L, Drake JW. 2012 The three faces of riboviral spontaneous mutation: spectrum, mode of genome replication, and mutation rate. PLoS Genet. 8, e1002832. (doi:10.1371/journal.pgen.1002832)
28. Dessau M, Goldhill D, McBride RL, Turner PE, Modis Y. 2012 Selective pressure causes an RNA virus to trade reproductive fitness for increased structural and thermal stability of a viral enzyme. PLoS Genet. 8, e1003102. (doi:10.1371/journal.pgen.1003102)
29. Kerr B, West J, Bohannan BJM. 2008 Bacteriophages: models for exploring basic principles of ecology. In Bacteriophage ecology: population growth, evolution, and impact of bacterial viruses (ed. ST Abedon), pp. 31-63. New York, NY: Cambridge University Press.
30. Charnov EL. 1976 Optimal foraging, the marginal value theorem. Theor. Popul. Biol. 9, 129-136. (doi:10.1016/0040-5809(76)90040-X)
31. Beekwilder J, Nieuwenhuizen R, Poot R, van Duin J. 1996 Secondary structure model for the first three domains of Qß RNA. Control of A-protein synthesis. J. Mol. Biol. 256, 8-19. (doi:10.1006/jmbi.1996.0064) (Pubitemid 26104206)
32. Staples DH, Hindley J, Billeter MA, Weissmann C. 1971 Localization of Qß maturation cistron ribosome binding site. Nat. New Biol. 234, 202-204. (accession no. WOS:A1971L035700005)
33. Kashiwagi A, Yomo T. 2011 Ongoing phenotypic and genomic changes in experimental coevolution of RNA bacteriophage Qß and Escherichia coli. PLoS Genet. 7, e1002188. (doi:10.1371/journal.pgen.1002188)
34. Langlais C-L. 2007 Understanding the lytic function of A2: the maturation protein of ssRNA bacteriophage Qß. PhD dissertation. Texas A&M University, USA.
35. Novella IS, Zárate S, Metzgar D, Ebendick-Corpus BE. 2004 Positive selection of synonymous mutations in vesicular stomatitis virus. J. Mol. Biol. 342, 1415-1421. (doi:10.1016/j.jmb.2004.08.003) (Pubitemid 39213962)
36. Kidmose RT, Vasiliev NN, Chetverin AB, Andersen GR, Knudsen CR. 2010 Structure of the Qß replicase, an RNA-dependent RNA polymerase consisting of viral and host proteins. Proc. Natl Acad. Sci. USA 107, 10 884-10 889. (doi:10.1073/pnas.1003015107)
37. Holmes EC. 2009 The evolution and emergence of RNA viruses, 1st edn. New York, NY: Oxford University Press, Inc.
38. Holmes EC. 2003 Error thresholds and the constraints to RNA virus evolution. Trends Microbiol. 11, 543-546. (doi:10.1016/j.tim.2003.10.006) (Pubitemid 37500904)
39. Baranowski E, Sevilla N, Verdaguer N, Ruiz-Jarabo CM, Beck E, Domingo E. 1998 Multiple virulence determinants of foot-and-mouth disease virus in cell culture. J. Virol. 72, 6362-6372. (accession no. WOS:000074730200012) (Pubitemid 28323947)
40. Mills DR, Priano C, Merz PA, Binderow BD. 1990 Qß RNA bacteriophage: mapping cis acting elements within an RNA genome. J. Virol. 64, 3872-3881. (accession no. WOS:A1990DR59700036) (Pubitemid 20227212)
41. Kozmin SG, Pavlov YI, Dunn RL, Schaaper RM. 2000 Hypersensitivity of Escherichia coli D(uvrB-bio) mutants to 6-hydroxylaminopurine and other base analogs is due to a defect in molybdenum cofactor biosynthesis. J. Bacteriol. 182, 3361-3367. (doi:10.1128/JB.182.12.3361-3367.2000) (Pubitemid 30341596)
42. Sambrook J, Russell DW. 2001 Molecular cloning: a laboratory manual, 3rd edn. New York, NY: Cold Spring Harbor Laboratory Press.
43. Sokal RR, Rohlf FJ. 1995 Biometry, 3rd edn. New York, NY: W.H. Freeman and Company.