1932

Abstract

Despite their simplicity, viruses exhibit certain types of social interactions. Situations in which a given virus achieves higher fitness in combination with other members of the viral population have been described at the level of transmission, replication, suppression of host immune responses, and host killing, enabling the evolution of viral cooperation. Although cellular coinfection with multiple viral particles is the typical playground for these interactions, cooperation between viruses infecting different cells is also established through cellular and viral-encoded communication systems. In general, the stability of cooperation is compromised by cheater genotypes, as best exemplified by defective interfering particles. As predicted by social evolution theory, cheater invasion can be avoided when cooperators interact preferentially with other cooperators, a situation that is promoted in spatially structured populations. Processes such as transmission bottlenecks, organ compartmentalization, localized spread of infection foci, superinfection exclusion, and even discrete intracellular replication centers promote multilevel spatial structuring in viruses.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-091919-071712
2021-09-29
2024-07-19
Loading full text...

Full text loading...

/deliver/fulltext/virology/8/1/annurev-virology-091919-071712.html?itemId=/content/journals/10.1146/annurev-virology-091919-071712&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Fenner F 1962. The reactivation of animal viruses. Br. Med. J. 2:135–42
    [Google Scholar]
  2. 2. 
    Andino R, Domingo E 2015. Viral quasispecies. Virology 479–480:46–51
    [Google Scholar]
  3. 3. 
    Huang AS, Baltimore D. 1970. Defective viral particles and viral disease processes. Nature 226:325–27
    [Google Scholar]
  4. 4. 
    Doceul V, Hollinshead M, van der Linden L, Smith GL. 2010. Repulsion of superinfecting virions: a mechanism for rapid virus spread. Science 327:873–76
    [Google Scholar]
  5. 5. 
    Andreu-Moreno I, Bou J-V, Sanjuán R. 2020. Cooperative nature of viral replication. Sci. Adv. 6:eabd4942
    [Google Scholar]
  6. 6. 
    Domingo-Calap P, Segredo-Otero EA, Durán-Moreno M, Sanjuán R. 2019. Social evolution of innate immunity evasion in a virus. Nat. Microbiol. 4:1006–13
    [Google Scholar]
  7. 7. 
    Borges AL, Zhang JY, Rollins MF, Osuna BA, Wiedenheft B, Bondy-Denomy J. 2018. Bacteriophage cooperation suppresses CRISPR-Cas3 and Cas9 immunity. Cell 174:917–25
    [Google Scholar]
  8. 8. 
    Landsberger M, Gandon S, Meaden S, Rollie C, Chevallereau A et al. 2018. Anti-CRISPR phages cooperate to overcome CRISPR-Cas immunity. Cell 174:908–16
    [Google Scholar]
  9. 9. 
    Erez Z, Steinberger-Levy I, Shamir M, Doron S, Stokar-Avihail A et al. 2017. Communication between viruses guides lysis-lysogeny decisions. Nature 541:488–93
    [Google Scholar]
  10. 10. 
    Díaz-Muñoz SL. 2019. Uncovering virus-virus interactions by unifying approaches and harnessing high-throughput tools. mSystems 4:e00121-19
    [Google Scholar]
  11. 11. 
    Díaz-Muñoz SL, Sanjuán R, West S. 2017. Sociovirology: conflict, cooperation, and communication among viruses. Cell Host Microbe 22:437–41
    [Google Scholar]
  12. 12. 
    West SA, Cooper GA. 2016. Division of labour in microorganisms: an evolutionary perspective. Nat. Rev. Microbiol. 14:716–23
    [Google Scholar]
  13. 13. 
    Nadell CD, Drescher K, Foster KR. 2016. Spatial structure, cooperation and competition in biofilms. Nat. Rev. Microbiol. 14:589–600
    [Google Scholar]
  14. 14. 
    DaPalma T, Doonan BP, Trager NM, Kasman LM. 2010. A systematic approach to virus–virus interactions. Virus Res 149:1–9
    [Google Scholar]
  15. 15. 
    West SA, Griffin AS, Gardner A, Diggle SP. 2006. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4:597–607
    [Google Scholar]
  16. 16. 
    Lion S, Jansen VA, Day T. 2011. Evolution in structured populations: beyond the kin versus group debate. Trends Ecol. Evol. 26:193–201
    [Google Scholar]
  17. 17. 
    Marshall JA. 2011. Group selection and kin selection: formally equivalent approaches. Trends Ecol. Evol. 26:325–32
    [Google Scholar]
  18. 18. 
    Birch J. 2018. Kin selection, group selection, and the varieties of population structure. Br. J. Philos. Sci. 71:259–86
    [Google Scholar]
  19. 19. 
    Fletcher JA, Doebeli M. 2009. A simple and general explanation for the evolution of altruism. Proc. Biol. Sci. 276:13–19
    [Google Scholar]
  20. 20. 
    West SA, Gardner A. 2013. Adaptation and inclusive fitness. Curr. Biol. 23:R577–84
    [Google Scholar]
  21. 21. 
    Sanjuán R. 2017. Collective infectious units in viruses. Trends Microbiol 22:402–12
    [Google Scholar]
  22. 22. 
    Usmani SM, Zirafi O, Muller JA, Sandi-Monroy NL, Yadav JK et al. 2014. Direct visualization of HIV-enhancing endogenous amyloid fibrils in human semen. Nat. Commun. 5:3508
    [Google Scholar]
  23. 23. 
    Cuevas JM, Durán-Moreno M, Sanjuán R. 2017. Multi-virion infectious units arise from free viral particles in an enveloped virus. Nat. Microbiol. 2:17078
    [Google Scholar]
  24. 24. 
    Anschau V, Sanjuán R. 2020. Fibrinogen gamma chain promotes aggregation of vesicular stomatitis virus in saliva. Viruses 12:282
    [Google Scholar]
  25. 25. 
    Beniac DR, Melito PL, Devarennes SL, Hiebert SL, Rabb MJ et al. 2012. The organisation of Ebola virus reveals a capacity for extensive, modular polyploidy. PLOS ONE 7:e29608
    [Google Scholar]
  26. 26. 
    Shirogane Y, Watanabe S, Yanagi Y. 2012. Cooperation between different RNA virus genomes produces a new phenotype. Nat. Commun. 3:1235
    [Google Scholar]
  27. 27. 
    Feng Z, Hensley L, McKnight KL, Hu F, Madden V et al. 2013. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 496:367–71
    [Google Scholar]
  28. 28. 
    Chen YH, Du W, Hagemeijer MC, Takvorian PM, Pau C et al. 2015. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell 160:619–30
    [Google Scholar]
  29. 29. 
    Santiana M, Ghosh S, Ho BA, Rajasekaran V, Du WL et al. 2018. Vesicle-cloaked virus clusters are optimal units for inter-organismal viral transmission. Cell Host Microbe 24:208–20
    [Google Scholar]
  30. 30. 
    Bou J-V, Sanjuán R. 2021. Experimental evolution reveals a genetic basis for membrane-associated virus release. Mol. Biol. Evol. 38:358–67
    [Google Scholar]
  31. 31. 
    Ramakrishnaiah V, Thumann C, Fofana I, Habersetzer F, Pan Q et al. 2013. Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7.5 cells. PNAS 110:13109–13
    [Google Scholar]
  32. 32. 
    Arantes TS, Rodrigues RA, Dos Santos Silva LK, Oliveira GP, de Souza HL et al. 2016. The large Marseillevirus explores different entry pathways by forming giant infectious vesicles. J. Virol. 90:5246–55
    [Google Scholar]
  33. 33. 
    Sanjuán R, Thoulouze MI. 2019. Why viruses sometimes disperse in groups. Virus Evol 5:vez01
    [Google Scholar]
  34. 34. 
    Shcherbatova O, Grebennikov D, Sazonov I, Meyerhans A, Bocharov G 2020. Modeling of the HIV-1 life cycle in productively infected cells to predict novel therapeutic targets. Pathogens 9:255
    [Google Scholar]
  35. 35. 
    Aunins TR, Marsh KA, Subramanya G, Uprichard SL, Perelson AS, Chatterjee A. 2018. Intracellular hepatitis C virus modeling predicts infection dynamics and viral protein mechanisms. J. Virol. 92:e02098-17
    [Google Scholar]
  36. 36. 
    Heldt FS, Kupke SY, Dorl S, Reichl U, Frensing T. 2015. Single-cell analysis and stochastic modelling unveil large cell-to-cell variability in influenza A virus infection. Nat. Commun. 6:8938
    [Google Scholar]
  37. 37. 
    Stiefel P, Schmidt FI, Dorig P, Behr P, Zambelli T et al. 2012. Cooperative vaccinia infection demonstrated at the single-cell level using FluidFM. Nano Lett 12:4219–27
    [Google Scholar]
  38. 38. 
    Boulle M, Muller TG, Dahling S, Ganga Y, Jackson L et al. 2016. HIV cell-to-cell spread results in earlier onset of viral gene expression by multiple infections per cell. PLOS Pathog 12:e1005964
    [Google Scholar]
  39. 39. 
    Andreu-Moreno I, Sanjuán R 2018. Collective infection of cells by viral aggregates promotes early viral proliferation and reveals a cellular-level Allee effect. Curr. Biol. 28:3212–19
    [Google Scholar]
  40. 40. 
    Zhong P, Agosto LM, Ilinskaya A, Dorjbal B, Truong R et al. 2013. Cell-to-cell transmission can overcome multiple donor and target cell barriers imposed on cell-free HIV. PLOS ONE 8:e53138
    [Google Scholar]
  41. 41. 
    Voigt EA, Swick A, Yin J. 2016. Rapid induction and persistence of paracrine-induced cellular antiviral states arrest viral infection spread in A549 cells. Virology 496:59–66
    [Google Scholar]
  42. 42. 
    Howat TJ, Barreca C, O'Hare P, Gog JR, Grenfell BT 2006. Modelling dynamics of the type I interferon response to in vitro viral infection. J. R. Soc. Interface 3:699–709
    [Google Scholar]
  43. 43. 
    Voigt EA, Yin J. 2015. Kinetic differences and synergistic antiviral effects between type I and type III interferon signaling indicate pathway independence. J. Interferon Cytokine Res. 35:734–47
    [Google Scholar]
  44. 44. 
    Oyler-Yaniv A, Oyler-Yaniv J, Whitlock BM, Liu Z, Germain RN et al. 2017. A tunable diffusion-consumption mechanism of cytokine propagation enables plasticity in cell-to-cell communication in the immune system. Immunity 46:609–20
    [Google Scholar]
  45. 45. 
    Bourke AF. 2014. Hamilton's rule and the causes of social evolution. Philos. Trans. R. Soc. B 369:20130362
    [Google Scholar]
  46. 46. 
    Garijo R, Cuevas JM, Briz A, Sanjuán R. 2016. Constrained evolvability of interferon suppression in an RNA virus. Sci. Rep. 6:24722
    [Google Scholar]
  47. 47. 
    Hille F, Richter H, Wong SP, Bratovič M, Ressel S, Charpentier E. 2018. The biology of CRISPR-Cas: backward and forward. Cell 172:1239–59
    [Google Scholar]
  48. 48. 
    Borges AL, Davidson AR, Bondy-Denomy J. 2017. The discovery, mechanisms, and evolutionary impact of anti-CRISPRs. Annu. Rev. Virol. 4:37–59
    [Google Scholar]
  49. 49. 
    Zhang F, Song G, Tian Y. 2019. Anti-CRISPRs: the natural inhibitors for CRISPR-Cas systems. Anim. Models Exp. Med. 2:69–75
    [Google Scholar]
  50. 50. 
    Cressler CE, McLeon DV, Rozins C, Van Den Hoogen J, Day T. 2016. The adaptive evolution of virulence: a review of theoretical predictions and empirical tests. Parasitology 143:915–30
    [Google Scholar]
  51. 51. 
    Boots M, Mealor M. 2007. Local interactions select for lower pathogen infectivity. Science 315:1284–86
    [Google Scholar]
  52. 52. 
    Kerr B, Neuhauser C, Bohannan BJM, Dean AM. 2006. Local migration promotes competitive restraint in a host-pathogen “tragedy of the commons. .” Nature 442:75–78
    [Google Scholar]
  53. 53. 
    Roychoudhury P, Shrestha N, Wiss VR, Krone SM. 2013. Fitness benefits of low infectivity in a spatially structured population of bacteriophages. Proc. Biol. Sci. 281:20132563
    [Google Scholar]
  54. 54. 
    Stokar-Avihail A, Tal N, Erez Z, Lopatina A, Sorek R. 2019. Widespread utilization of peptide communication in phages infecting soil and pathogenic bacteria. Cell Host Microbe 25:746–55
    [Google Scholar]
  55. 55. 
    Dou C, Xiong J, Gu Y, Yin K, Wang J et al. 2018. Structural and functional insights into the regulation of the lysis-lysogeny decision in viral communities. Nat. Microbiol. 3:1285–94
    [Google Scholar]
  56. 56. 
    Gallego del Sol F, Penadés JR, Marina A 2019. Deciphering the molecular mechanism underpinning phage arbitrium communication systems. Mol. Cell 74:59–72
    [Google Scholar]
  57. 57. 
    Lauring AS, Andino R. 2010. Quasispecies theory and the behavior of RNA viruses. PLOS Pathog 6:e1001005
    [Google Scholar]
  58. 58. 
    Shirogane Y, Watanabe S, Yanagi Y. 2019. Cooperation between different variants: a unique potential for virus evolution. Virus Res 264:68–73
    [Google Scholar]
  59. 59. 
    Brooke CB. 2017. Population diversity and collective interactions during influenza virus infection. J. Virol. 91:e01164-17
    [Google Scholar]
  60. 60. 
    Xue KS, Hooper KA, Ollodart AR, Dingens AS, Bloom JD 2016. Cooperation between distinct viral variants promotes growth of H3N2 influenza in cell culture. eLife 5:e13974
    [Google Scholar]
  61. 61. 
    Sicard A, Michalakis Y, Gutierrez S, Blanc S. 2016. The strange lifestyle of multipartite viruses. PLOS Pathog 12:e1005819
    [Google Scholar]
  62. 62. 
    Lucía-Sanz A, Manrubia S. 2017. Multipartite viruses: adaptive trick or evolutionary treat?. NPJ Syst. Biol. Appl. 3:34
    [Google Scholar]
  63. 63. 
    Sicard A, Pirolles E, Gallet R, Vernerey M-S, Yvon M et al. 2019. A multicellular way of life for a multipartite virus. eLife 8:e43599
    [Google Scholar]
  64. 64. 
    Simón O, Williams T, López-Ferber M, Caballero P. 2004. Genetic structure of a Spodoptera frugiperda nucleopolyhedrovirus population: high prevalence of deletion genotypes. Appl. Environ. Microbiol. 70:5579–88
    [Google Scholar]
  65. 65. 
    Serrano A, Williams T, Simón O, López-Ferber M, Caballero P, Muñoz D. 2013. Analagous population structures for two alphabaculoviruses highlight a functional role for deletion mutants. Appl. Environ. Microbiol. 79:1118–25
    [Google Scholar]
  66. 66. 
    Tanner EJ, Kirkegaard KA, Weinberger LS. 2016. Exploiting genetic interference for antiviral therapy. PLOS Genet 12:e1005986
    [Google Scholar]
  67. 67. 
    Sardanyés J, Elena SF. 2010. Error threshold in RNA quasispecies models with complementation. J. Theor. Biol. 265:278–86
    [Google Scholar]
  68. 68. 
    Segredo-Otero E, Sanjuán R. 2019. The effect of genetic complementation on the fitness and diversity of viruses spreading as collective infectious units. Virus Res 267:41–48
    [Google Scholar]
  69. 69. 
    Vignuzzi M, López CB. 2019. Defective viral genomes are key drivers of the virus-host interaction. Nat. Microbiol. 4:1075–87
    [Google Scholar]
  70. 70. 
    Rezelj VV, Levi LI, Vignuzzi M. 2018. The defective component of viral populations. Curr. Opin. Virol. 33:74–80
    [Google Scholar]
  71. 71. 
    Genoyer E, López CB. 2019. The impact of defective viruses on infection and immunity. Annu. Rev. Virol. 6:547–66
    [Google Scholar]
  72. 72. 
    Muñoz D, Castillejo JI, Caballero P. 1998. Naturally occurring deletion mutants are parasitic genotypes in a wild-type nucleopolyhedrovirus population of Spodoptera exigua. Appl. Environ. Microbiol. 64:4372–77
    [Google Scholar]
  73. 73. 
    Andreu-Moreno I, Sanjuán R 2020. Collective viral spread mediated by virion aggregates promotes the evolution of defective interfering particles. mBio 11:e02156-19
    [Google Scholar]
  74. 74. 
    Li Q, Liu Q, Huang W, Li X, Wang Y 2018. Current status on the development of pseudoviruses for enveloped viruses. Rev. Med. Virol. 28:e1963
    [Google Scholar]
  75. 75. 
    Chao L, Elena SF. 2017. Nonlinear trade-offs allow the cooperation game to evolve from Prisoner's Dilemma to Snowdrift. Proc. Biol. Sci. 284:20170228
    [Google Scholar]
  76. 76. 
    Yang Y, Lyu T, Zhou R, He X, Ye K et al. 2019. The antiviral and antitumor effects of defective interfering particles/genomes and their mechanisms. Front. Microbiol. 10:1852
    [Google Scholar]
  77. 77. 
    Meir M, Harel N, Miller D, Gelbart M, Eldar A et al. 2020. Competition between social cheater viruses is driven by mechanistically different cheating strategies. Sci. Adv. 6:eabb7990
    [Google Scholar]
  78. 78. 
    Bohl K, Hummert S, Werner S, Basanta D, Deutsch A et al. 2014. Evolutionary game theory: molecules as players. Mol. Biosyst. 10:3066–74
    [Google Scholar]
  79. 79. 
    Turner PE, Chao L. 1999. Prisoner's dilemma in an RNA virus. Nature 398:441–43
    [Google Scholar]
  80. 80. 
    Chevallereau A, Meaden S, Fradet O, Landsberger M, Maestri A et al. 2020. Exploitation of the cooperative behaviors of anti-CRISPR phages. Cell Host Microbe 27:189–98
    [Google Scholar]
  81. 81. 
    Leggett HC, Wild G, West SA, Buckling A. 2017. Fast-killing parasites can be favoured in spatially structured populations. Philos. Trans. R. Soc. B 372:20160096
    [Google Scholar]
  82. 82. 
    Zwart MP, Elena SF. 2015. Matters of size: genetic bottlenecks in virus infection and their potential impact on evolution. Annu. Rev. Virol. 2:161–79
    [Google Scholar]
  83. 83. 
    Gutierrez S, Michalakis Y, Blanc S. 2012. Virus population bottlenecks during within-host progression and host-to-host transmission. Curr. Opin. Virol. 2:546–55
    [Google Scholar]
  84. 84. 
    McCrone JT, Lauring AS. 2018. Genetic bottlenecks in intraspecies virus transmission. Curr. Opin. Virol. 28:20–25
    [Google Scholar]
  85. 85. 
    Joseph SB, Swanstrom R, Kashuba ADM, Cohen MS. 2015. Bottlenecks in HIV-1 transmission: insights from the study of founder viruses. Nat. Rev. Microbiol. 13:414–25
    [Google Scholar]
  86. 86. 
    Salemi M, Rife B. 2016. Phylogenetics and phyloanatomy of HIV/SIV intra-host compartments and reservoirs: the key role of the central nervous system. Curr. HIV Res. 14:110–20
    [Google Scholar]
  87. 87. 
    Gallagher ME, Brooke CB, Ke R, Koelle K. 2018. Causes and consequences of spatial within-host viral spread. Viruses 10:627
    [Google Scholar]
  88. 88. 
    Graw F, Perelson AS. 2016. Modeling viral spread. Annu. Rev. Virol. 3:555–72
    [Google Scholar]
  89. 89. 
    Law KM, Komarova NL, Yewdall AW, Lee RK, Herrera OL et al. 2016. In vivo HIV-1 cell-to-cell transmission promotes multicopy micro-compartmentalized infection. Cell Rep 15:2771–83
    [Google Scholar]
  90. 90. 
    Yakimovich A, Gumpert H, Burckhardt CJ, Lutschg VA, Jurgeit A et al. 2012. Cell-free transmission of human adenovirus by passive mass transfer in cell culture simulated in a computer model. J. Virol. 86:10123–37
    [Google Scholar]
  91. 91. 
    Zhong P, Agosto LM, Munro JB, Mothes W. 2013. Cell-to-cell transmission of viruses. Curr. Opin. Virol. 3:44–50
    [Google Scholar]
  92. 92. 
    Bou J-V, Geller R, Sanjuán R. 2019. Membrane-associated enteroviruses undergo intercellular transmission as pools of sibling viral genomes. Cell Rep 29:714–23
    [Google Scholar]
  93. 93. 
    Shulla A, Randall G. 2016. (+) RNA virus replication compartments: a safe home for (most) viral replication. Curr. Opin. Microbiol. 32:82–88
    [Google Scholar]
  94. 94. 
    den Boon JA, Ahlquist P 2010. Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu. Rev. Microbiol. 64:241–56
    [Google Scholar]
  95. 95. 
    Harak C, Lohmann V. 2015. Ultrastructure of the replication sites of positive-strand RNA viruses. Virology 479–480:418–33
    [Google Scholar]
/content/journals/10.1146/annurev-virology-091919-071712
Loading
/content/journals/10.1146/annurev-virology-091919-071712
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error