Should Symbionts Be Nice or Selfish? Antiviral Effects of Wolbachia Are Costly but Reproductive Parasitism Is Not

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Arthropods are commonly infected with heritable bacteria, and some of these symbionts can protect their hosts against infection and/or be reproductive parasites. Which of these traits evolves will depend on whether the trait is costly to the symbiont and the host. Using a panel of strains of the symbiont Wolbachia in the fruit fly Drosophila simulans, we found that the beneficial effect of antiviral protection and the parasitic phenotype of cytoplasmic incompatibility occur independently across the strains. We found that high antiviral protection is associated with high symbiont densities and strong reductions in other life-history traits affecting the fitness of both the symbiont and the host. In contrast cytoplasmic incompatibility did not induce costs on these traits. This trade-off between antiviral protection and other fitness components may select for reduced antiviral protection, which would endanger the long-term success of programs using Wolbachia to block the transmission of mosquito-borne viruses.

Vyšlo v časopise: Should Symbionts Be Nice or Selfish? Antiviral Effects of Wolbachia Are Costly but Reproductive Parasitism Is Not. PLoS Pathog 11(7): e32767. doi:10.1371/journal.ppat.1005021
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005021

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Zdroje

1. Douglas AE. The microbial dimension in insect nutritional ecology. Funct Ecol. 2009;23 : 38–47.

2. Moran N, Tran P, Gerardo N. Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl Environ Microbiol. 2005;71 : 8802–8810. 16332876

3. Russell J, Moran N. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc R Soc B Biol Sci. 2006;273 : 603–10.

4. Oliver KM, Russell JA, Moran NA, Hunter MS. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. 2003;100 : 1803–1807. 12563031

5. Xie JL, Vilchez I, Mateos M. Spiroplasma Bacteria Enhance Survival of Drosophila hydei Attacked by the Parasitic Wasp Leptopilina heterotoma. PLoS One. 2010;5: e12149. doi: 10.1371/journal.pone.0012149 20730104

6. Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ. Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science. 2010;329 : 212–5. doi: 10.1126/science.1188235 20616278

7. Teixeira L, Ferreira A, Ashburner M. The Bacterial Symbiont Wolbachia Induces Resistance to RNA Viral Infections in Drosophila melanogaster. Plos Biol. 2008;6 : 2753–2763.

8. Scarborough CL, Ferrari J, Godfray HCJ. Aphid protected from pathogen by endosymbiont. Science. United States; 2005;310 : 1781. 16357252

9. Hedges L, Brownlie J, O’Neill S, Johnson K. Wolbachia and virus protection in insects. Science. 2008;322 : 702. doi: 10.1126/science.1162418 18974344

10. Engelstädter J, Hurst GDD. The Ecology and Evolution of Microbes that Manipulate Host Reproduction. Annu Rev Ecol Evol Syst. 2009;40 : 127–149.

11. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, et al. Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science. 2011;332 : 254–6. doi: 10.1126/science.1199410 21474763

12. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell. 2009;139 : 1268–78. doi: 10.1016/j.cell.2009.11.042 20064373

13. Glaser RL, Meola MA. The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS One. 2010;5: e11977. doi: 10.1371/journal.pone.0011977 20700535

14. Martinez J, Longdon B, Bauer S, Chan Y-S, Miller WJ, Bourtzis K, et al. Symbionts Commonly Provide Broad Spectrum Resistance to Viruses in Insects: A Comparative Analysis of Wolbachia Strains. Schneider DS, editor. PLoS Pathog. 2014;10: e1004369. doi: 10.1371/journal.ppat.1004369 25233341

15. Van den Hurk AF, Hall-Mendelin S, Pyke AT, Frentiu FD, McElroy K, Day A, et al. Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti. PLoS Negl Trop Dis. 2012;6: e1892. doi: 10.1371/journal.pntd.0001892 23133693

16. Kambris Z, Cook P, Phuc H, Sinkins S. Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science. 2009;326 : 134–136. doi: 10.1126/science.1177531 19797660

17. Kambris Z, Blagborough AM, Pinto SB, Blagrove MSC, Godfray HCJ, Sinden RE, et al. Wolbachia stimulates immune gene expression and inhibits plasmodium development in Anopheles gambiae. PLoS Pathog. 2010;6: e1001143. doi: 10.1371/journal.ppat.1001143 20949079

18. Hughes GL, Koga R, Xue P, Fukatsu T, Rasgon JL. Wolbachia infections are virulent and inhibit the human malaria parasite Plasmodium falciparum in Anopheles gambiae. PLoS Pathog. 2011;7: e1002043. doi: 10.1371/journal.ppat.1002043 21625582

19. Ye YH, Woolfit M, Rancès E, O’Neill SL, McGraw E a. Wolbachia-Associated Bacterial Protection in the Mosquito Aedes aegypti. PLoS Negl Trop Dis. 2013;7.

20. Kriesner P, Hoffmann AA, Lee SF, Turelli M, Weeks AR. Rapid Sequential Spread of Two Wolbachia Variants in Drosophila simulans. PLoS Pathog. 2013;9: e1003607. doi: 10.1371/journal.ppat.1003607 24068927

21. Hoffmann A, Clancy D, Duncan J. Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility. Heredity. 1996;76 : 1–8. 8575931

22. Werren JH, Baldo L, Clark ME. Wolbachia: master manipulators of invertebrate biology. Nature. 2008;6 : 741–751.

23. Bull JJ, Turelli M. Wolbachia versus dengue: Evolutionary forecasts. Evol Med Public Heal. 2013;2013 : 197–201.

24. McGraw E a, O’Neill SL. Beyond insecticides: new thinking on an ancient problem. Nat Rev Microbiol. 2013;11 : 181–93. doi: 10.1038/nrmicro2968 23411863

25. Riegler M, Sidhu M, Miller WJ, O’Neill SL. Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr Biol. 2005;15 : 1428–33. 16085497

26. Richardson MF, Weinert LA, Welch JJ, Linheiro RS, Magwire MM, Jiggins FM, et al. Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster. PLoS Genet. 2012;8: e1003129. doi: 10.1371/journal.pgen.1003129 23284297

27. Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, Jiggins FM, et al. Wolbachia Variants Induce Differential Protection to Viruses in Drosophila melanogaster: A Phenotypic and Phylogenomic Analysis. Malik HS, editor. PLoS Genet. 2013;9: e1003896. doi: 10.1371/journal.pgen.1003896 24348259

28. Carrington LB, Lipkowitz JR, Hoffmann AA, Turelli M. A re-examination of Wolbachia-induced cytoplasmic incompatibility in California Drosophila simulans. PLoS One. 2011;6: e22565. doi: 10.1371/journal.pone.0022565 21799900

29. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F, et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature; 2011;476 : 454–7. doi: 10.1038/nature10356 21866160

30. Hoffmann AA, Iturbe-Ormaetxe I, Callahan AG, Phillips BL, Billington K, Axford JK, et al. Stability of the wMel Wolbachia Infection following Invasion into Aedes aegypti Populations. PLoS Negl Trop Dis. 2014;8: e3115. doi: 10.1371/journal.pntd.0003115 25211492

31. Frentiu FD, Zakir T, Walker T, Popovici J, Pyke AT, van den Hurk A, et al. Limited dengue virus replication in field-collected Aedes aegypti mosquitoes infected with Wolbachia. PLoS Negl Trop Dis. 2014;8: e2688. doi: 10.1371/journal.pntd.0002688 24587459

32. Turelli M. Evolution of incompatibility-inducing microbes and their hosts. Evolution. 1994;48 : 1500–1513.

33. Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA. From Parasite to Mutualist: Rapid Evolution of Wolbachia in Natural Populations of Drosophila. Plos Biol. 2007;5 : 997–1005.

34. Chrostek E, Marialva MSP, Yamada R, O’Neill SL, Teixeira L. High Anti-Viral Protection without Immune Upregulation after Interspecies Wolbachia Transfer. PLoS One. 2014;9: e99025. doi: 10.1371/journal.pone.0099025 24911519

35. McMeniman CJ, Lane AM, Fong AWC, Voronin D a, Iturbe-Ormaetxe I, Yamada R, et al. Host adaptation of a Wolbachia strain after long-term serial passage in mosquito cell lines. Appl Environ Microbiol. 2008;74 : 6963–9. doi: 10.1128/AEM.01038-08 18836024

36. Osborne SE, Iturbe-Ormaetxe I, Brownlie JC, O’Neill SL, Johnson KN. Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl Environ Microbiol. 2012;78 : 6922–9. doi: 10.1128/AEM.01727-12 22843518

37. Osborne SE, Leong YS, O’Neill SL, Johnson KN. Variation in Antiviral Protection Mediated by Different Wolbachia Strains in Drosophila simulans. Plos Pathog. 2009;5 : 9.

38. Chrostek E, Teixeira L. Mutualism Breakdown by Amplification of Wolbachia Genes. PLOS Biol. 2015;13: e1002065. doi: 10.1371/journal.pbio.1002065 25668031

39. Veneti Z, Clark ME, Zabalou S, Karr TL, Savakis C, Bourtzis K. Cytoplasmic incompatibility and sperm cyst infection in different Drosophila-Wolbachia associations. Genetics. 2003;164 : 545–52. 12807775

40. Veneti Z, Clark M, Karr T. Heads or tails: host-parasite interactions in the Drosophila-Wolbachia system. Appl Environ Microbiol. 2004;70 : 5366–5372. 15345422

41. Clancy DJ, Hoffmann AA. Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans. Entomol Exp Appl. 1998;86 : 13–24.

42. Clark M, Veneti Z, Bourtzis K, Karr T. Wolbachia distribution and cytoplasmic incompatibility during sperm development: the cyst as the basic cellular unit of CI expression. Mech Dev. 2003;120 : 185–198. 12559491

43. Didelot X, Falush D. Inference of Bacterial Microevolution Using Multilocus Sequence Data. Genet. 2007;175 : 1251–1266.

44. Zabalou S, Apostolaki A, Pattas S, Veneti Z, Paraskevopoulos C, Livadaras I, et al. Multiple rescue factors within a Wolbachia strain. Genetics. 2008;178 : 2145–60. doi: 10.1534/genetics.107.086488 18430940

45. Harcombe W, Hoffmann AA. Wolbachia effects in Drosophila melanogaster: in search of fitness benefits. J Invertebr Pathol. 2004;87 : 45–50. 15491598

46. De Almeida F, Moura AS, Cardoso AF, Winter CE, Bijovsky AT, Suesdek L. Effects of Wolbachia on fitness of Culex quinquefasciatus (Diptera; Culicidae). Infect Genet Evol. 2011;11 : 2138–43. doi: 10.1016/j.meegid.2011.08.022 21907309

47. McMeniman CJ, O’Neill SL. A virulent Wolbachia infection decreases the viability of the dengue vector Aedes aegypti during periods of embryonic quiescence. PLoS Negl Trop Dis. 2010;4: e748. doi: 10.1371/journal.pntd.0000748 20644622

48. Min K, Benzer S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci U S A. 1997;94 : 10792–10796. 9380712

49. Gavotte L, Mercer DR, Stoeckle JJ, Dobson SL. Costs and benefits of Wolbachia infection in immature Aedes albopictus depend upon sex and competition level. J Invertebr Pathol. Elsevier Inc.; 2010;105 : 341–6. doi: 10.1016/j.jip.2010.08.005 20807539

50. Yeap HL, Mee P, Walker T, Weeks AR, O’Neill SL, Johnson P, et al. Dynamics of the “popcorn” Wolbachia infection in outbred Aedes aegypti informs prospects for mosquito vector control. Genetics. 2011;187 : 583–95. doi: 10.1534/genetics.110.122390 21135075

51. Suh E, Dobson SL. Reduced competitiveness of Wolbachia infected Aedes aegypti larvae in intra -⁠ and inter-specific immature interactions. J Invertebr Pathol. Elsevier Inc.; 2013;114 : 173–177. doi: 10.1016/j.jip.2013.08.001 23933013

52. Turley AP, Zalucki MP, O’Neill SL, McGraw EA. Transinfected Wolbachia have minimal effects on male reproductive success in Aedes aegypti. Parasit Vectors. Parasites & Vectors; 2013;6 : 36.

53. Joshi D, McFadden MJ, Bevins D, Zhang F, Xi Z. Wolbachia strain wAlbB confers both fitness costs and benefit on Anopheles stephensi. Parasit Vectors. 2014;7 : 336. doi: 10.1186/1756-3305-7-336 25041943

54. Cayetano L, Rothacher L, Simon J, Vorburger C. Cheaper is not always worse: strongly protective isolates of a defensive symbiont are less costly to the aphid host. Proc R Soc B Biol Sci. 2015;282.

55. Oliver KM, Degnan PH, Hunter MS, Moran NA. Bacteriophages Encode Factors Required for Protection in a Symbiotic Mutualism. Science. 2009;325 : 992–994. doi: 10.1126/science.1174463 19696350

56. Weldon SR, Strand MR, Oliver KM. Phage loss and the breakdown of a defensive symbiosis in aphids. Proc Biol Sci. 2013;280 : 20122103. doi: 10.1098/rspb.2012.2103 23193123

57. Frentiu FD, Robinson J, Young PR, McGraw EA, O’Neill SL. Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PLoS One. 2010;5: e13398. doi: 10.1371/journal.pone.0013398 20976219

58. Lu P, Bian G, Pan X, Xi Z. Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl Trop Dis. 2012;6: e1754. doi: 10.1371/journal.pntd.0001754 22848774

59. McGraw EA, Merritt DJ, Droller JN, O’Neill SL. Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad Sci U S A. 2002;99 : 2918–23. 11880639

60. Tram U, Ferree PM, Sullivan W. Identification of Wolbachia-host interacting factors through cytological analysis. Microbes Infect. 2003;5 : 999–1011. 12941392

61. Blows MW, Hoffmann AA. A reassessment of genetic limits to evolutionary change. Ecology. 2005;86 : 1371–1384.

62. Prout T. Some evolutionary possibilities for a microbe that causes incompatibility in its host. Evolution. 1994;48 : 909–911.

63. Frank SA. Cytoplasmic Incompatibility and Population Structure. J Theor Biol. 1997;184 : 327–330.

64. Haygood R, Turelli M. Evolution of incompatibility-inducing microbes in subdivided host populations. Evolution. United States; 2009;63 : 432–447.

65. Hurst L, McVean GT. Clade Selection, Reversible Evolution and the Persistence of Selfish Elements: The Evolutionary Dynamics of Cytoplasmic Incompatibility. Proc R Soc London Ser B-Biological Sci. 1996;263 : 97–104.

66. Vavre F, Charlat S. Making (good) use of Wolbachia: what the models say. Curr Opin Microbiol. 2012;15 : 263–8. doi: 10.1016/j.mib.2012.03.005 22494817

67. Maciel-de-Freitas R, Koella JC, Lourenço-de-Oliveira R. Lower survival rate, longevity and fecundity of Aedes aegypti (Diptera: Culicidae) females orally challenged with dengue virus serotype 2. Trans R Soc Trop Med Hyg. 2011;105 : 452–458. doi: 10.1016/j.trstmh.2011.05.006 21700303

68. Yoon IK, Getis A, Aldstadt J, Rothman AL, Tannitisupawong D, Koenraadt CJM, et al. Fine scale spatiotemporal clustering of dengue virus transmission in children and Aedes aegypti in rural Thai villages. PLoS Negl Trop Dis. 2012;6: e1730. doi: 10.1371/journal.pntd.0001730 22816001

69. Poinsot D, Bourtzis K, Markakis G, Savakis C. Wolbachia Transfer from Drosophila melanogaster into D. simulans: Host Effect and Cytoplasmic Incompatibility Relationships. Genetics. 1998;150 : 227–237. 9725842

70. Veneti Z, Zabalou S, Papafotiou G, Paraskevopoulos C, Pattas S, Livadaras I, et al. Loss of reproductive parasitism following transfer of male-killing Wolbachia to Drosophila melanogaster and Drosophila simulans. Heredity. 2012;109 : 306–12. doi: 10.1038/hdy.2012.43 22892635

71. O’Neill SL, Giordano R, Colbert AM, Karr TL, Robertson HM. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci U S A. 1992;89 : 2699–702. 1557375

72. Awrahman ZA, Champion de Crespigny F, Wedell N. The impact of Wolbachia, male age and mating history on cytoplasmic incompatibility and sperm transfer in Drosophila simulans. J Evol Biol. 2013; 1–10.

73. Reynolds KT, Hoffmann AA. Male age, host effects and the weak expression or non-expression of cytoplasmic incompatibility in Drosophila strains infected by maternally transmitted Wolbachia. Genet Res. 2002;80 : 79–87. 12534211

74. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Meth. Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.; 2012;9 : 671–675.

75. Sullivan W, Ashburner M, Hawley R. Drosophila Protocols. New York: Cold Spring Harbor Laboratory Press; 2000.

76. R Core Team. R: A Language and Environment for Statistical Computing [Internet]. Pimenta PF, editor. Vienna, Austria; 2013. Available: http://www.r-project.org

77. Felsenstein J. Phylogenies and the Comparative Method. The American Naturalist. 1985. pp. 1–15.

78. Orme D. The caper package: comparative analysis of phylogenetics and evolution in R. 2013.