Addicted? Reduced host resistance in populations with defensive symbionts

Proceedings of the Royal Society B: Biological Sciences

Volumn 283, Issue 1833, 2016, Pages

  Martinez, Julien ^a   Cogni, Rodrigo ^a,b   Cao, Chuan ^a   Smith, Sophie ^a   Illingworth, Christopher J R ^a   Jiggins, Francis M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Antiviral resistance; Drosophila melanogaster; Wolbachia

Indexed keywords

ALLELE; ANTIBIOTIC RESISTANCE; BACTERIUM; DEFENSE BEHAVIOR; EVOLUTION; FLY; GENOME; HERITABILITY; HOST-SYMBIONT INTERACTION; INFECTIVITY;

ARTHROPODA; DROSOPHILA C VIRUS; DROSOPHILA MELANOGASTER; HEXAPODA; WOLBACHIA;

ALLELE; ANIMAL; DISEASE RESISTANCE; DROSOPHILA MELANOGASTER; GENE; GENETIC SELECTION; GENETICS; INSECT VIRUS; MICROBIOLOGY; MOLECULAR EVOLUTION; SYMBIOSIS; VIROLOGY; WOLBACHIA;

ALLELES; ANIMALS; DISEASE RESISTANCE; DROSOPHILA MELANOGASTER; EVOLUTION, MOLECULAR; GENES, INSECT; INSECT VIRUSES; SELECTION, GENETIC; SYMBIOSIS; WOLBACHIA;

EID: 84975267532     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2016.0778     Document Type: Article

References (48)

1. Gerardo NM, Parker BJ. 2014 Mechanisms of symbiont-conferred protection against natural enemies: an ecological and evolutionary framework. Curr. Opin. Insect Sci. 4, 1-7. (doi:10.1016/j.cois. 2014.08.002)
2. Zug R, Hammerstein P. 2014 Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biol. Rev. 90, 89-111. (doi:10. 1111/brv.12098)
3. Vorburger C. 2014 The evolutionary ecology of symbiont-conferred resistance to parasitoids in aphids. Insect Sci. 21, 251-264. (doi:10.1111/1744-7917.12067)
4. Teixeira L, Ferreira A, Ashburner M. 2008 The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 6, 2753-2763. (doi:10.1371/journal.pbio. 1000002)
5. Kaltenpoth M, Engl T. 2014 Defensive microbial symbionts in Hymenoptera. Funct. Ecol. 28, 315-327. (doi:10.1111/1365-2435.12089)
6. Lopanik NB. 2014 Chemical defensive symbioses in the marine environment. Funct. Ecol. 28, 328-340. (doi:10.1111/1365-2435.12160)
7. Oliver KM, Russell JA, Moran NA, Hunter MS. 2003 Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl Acad. Sci. USA 100, 1803-1807. (doi:10.1073/pnas. 0335320100)
8. Hedges L, Brownlie J, O'Neill S, Johnson K. 2008 Wolbachia and virus protection in insects. Science 322, 702. (doi:10.1126/science.1162418)
9. Moreira LA et al. 2009 A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139, 1268-1278. (doi:10.1016/j.cell.2009.11.042)
10. Oliver KM, Degnan PH, Burke GR, Moran NA. 2010 Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu. Rev. Entomol. 55, 247-266. (doi:10.1146/annurev-ento-112408-085305)
11. Werren J, Zhang W, Guo L. 1995 Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc. R. Soc. B 261, 55-71. (doi:10. 1098/rspb.1995.0117)
12. Bennett PM. 2008 Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br. J. Pharmacol. 153, S347-S357. (doi:10.1038/sj.bjp.0707607)
13. Min K, Benzer S. 1997 Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl Acad. Sci. USA 94, 10 792-10 796. (doi:10.1073/pnas.94.20. 10792)
14. Vorburger C, Ganesanandamoorthy P, Kwiatkowski M. 2013 Comparing constitutive and induced costs of symbiont-conferred resistance to parasitoids in aphids. Ecol. Evol. 3, 706-713. (doi:10.1002/ ece3.491)
15. Chrostek E, Marialva MSP, Yamada R, O'Neill SL, Teixeira L. 2014 High anti-viral protection without immune upregulation after interspecies Wolbachia transfer. PLoS ONE 9, e99025. (doi:10.1371/journal. pone.0099025)
16. Dykstra HR, Weldon SR, Martinez AJ, White JA, Hopper KR, Heimpel GE, Asplen MK, Oliver KM. 2014 Factors limiting the spread of the protective symbiont Hamiltonella defensa in the aphid Aphis craccivora. Appl. Environ. Microbiol. 80, 5818-5827. (doi:10.1128/AEM.01775-14)
17. Chrostek E, Teixeira L. 2015 Mutualism breakdown by amplification of Wolbachia genes. PLOS Biol. 13, e1002065. (doi:10.1371/journal.pbio.1002065)
18. Martinez J, Ok S, Smith S, Snoeck K, Day JP, Jiggins FM. 2015 Should symbionts be nice or selfish? Antiviral effects of Wolbachia are costly but reproductive parasitism is not. PLoS Pathog. 11, e1005021. (doi:10.1371/journal.ppat.1005021)
19. Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, Jiggins FM, Teixeira L. 2013 Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLoS Genet. 9, e1003896. (doi:10.1371/journal.pgen.1003896)
20. Osborne SE, Leong YS, O'Neill SL, Johnson KN. 2009 Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog. 5, 9. (doi:10.1371/journal.ppat.1000656)
21. Martinez J, Longdon B, Bauer S, Chan Y-S, Miller WJ, Bourtzis K, Teixeira L, Jiggins FM. 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)
22. Salazar-Jaramillo L, Paspati A, Zande L, Vermeulen CJ, Schwander T, Wertheim B. 2014 Evolution of a cellular immune response in Drosophila: a phenotypic and genomic comparative analysis. Genome Biol. Evol. 6, 273-289. (doi:10.1093/gbe/ evu012)
23. Kwiatkowski M, Vorburger C. 2012 Modeling the ecology of symbiont-mediated protection against parasites. Am. Nat. 179, 595-605. (doi:10.1086/ 665003)
24. Werren JH, Baldo L, Clark ME. 2008 Wolbachia: master manipulators of invertebrate biology. Nature 6, 741-751. (doi:10.1038/nrmicro1969)
25. Plus N, Croizier G, Jousset F, David J. 1975 Picornaviruses of laboratory and wild Drosophila melanogaster: geographical distribution and serotypic composition. Ann. Microbiol. (Paris) 126, 107-117.
26. Christian PD, Scotti PD. 1998 Picornalike viruses of insects. In The insect viruses SE-10 (eds L Miller, LA Ball), pp. 301-336. New York, NY: Springer.
27. Magwire MM, Fabian DK, Schweyen H, Cao C, Longdon B, Bayer F, Jiggins FM. 2012 Genome-wide association studies reveal a simple genetic basis of resistance to naturally coevolving viruses in Drosophila melanogaster. PLoS Genet. 8, e1003057. (doi:10.1371/journal.pgen.1003057)
28. Martins NE, Faria VG, Nolte V, Schlotterer C, Teixeira L, Sucena E, Magalhaes S. 2014 Host adaptation to viruses relies on few genes with different crossresistance properties. Proc. Natl Acad. Sci. USA 111, 5938-5943. (doi:10.1073/pnas.1400378111)
29. 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)
30. Sullivan W, Ashburner M, Hawley R. 2000 Drosophila protocols. New York, NY: Cold Spring Harbor Laboratory Press.
31. Lacerda M, Seoighe C. 2014 Population genetics inference for longitudinally-sampled mutants under strong selection. Genetics 198, 1237-1250. (doi:10. 1534/genetics.114.167957)
32. R Core Team. 2013 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
33. Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ. 2015 The incidence of bacterial endosymbionts in terrestrial arthropods. Proc. R. Soc. B 282, 20150249. (doi:10.1098/rspb.2015.0249)
34. Obbard DJ, Jiggins FM, Bradshaw NJ, Little TJ. 2011 Recent and recurrent selective sweeps of the antiviral RNAi gene Argonaute-2 in three species of Drosophila. Mol. Biol. Evol. 28, 1043-1056. (doi:10. 1093/molbev/msq280)
35. Obbard DJ, Gordon KHJ, Buck AH, Jiggins FM. 2009 The evolution of RNAi as a defence against viruses and transposable elements. Phil. Trans. R. Soc. B 364, 99-115. (doi:10.1098/rstb. 2008.0168)
36. Obbard DJ, Jiggins FM, Halligan DL, Little TJ. 2006 Natural selection drives extremely rapid evolution in antiviral RNAi genes. Curr. Biol. 16, 580-585. (doi:10.1016/j.cub.2006.01.065)
37. Oliver KM, Moran NA, Hunter MS. 2006 Costs and benefits of a superinfection of facultative symbionts in aphids. Proc. R. Soc. B 273, 1273-1280. (doi:10. 1098/rspb.2005.3436)
38. Russell JA et al. 2013 Uncovering symbiont-driven genetic diversity across North American pea aphids. Mol. Ecol. 22, 2045-2059. (doi:10.1111/mec.12211)
39. Tsuchida T, Koga R, Shibao H, Matsumoto T, Fukatsu T. 2002 Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol. Ecol. 11, 2123-2135. (doi:10.1046/j.1365-294X.2002.01606.x)
40. Glaser RL, Meola MA. 2010 The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS ONE 5, e11977. (doi:10.1371/journal.pone.0011977)
41. Osborne SE, Iturbe-Ormaetxe I, Brownlie JC, O'Neill SL, Johnson KN. 2012 Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl. Environ. Microbiol. 78, 6922-6929. (doi:10.1128/AEM.01727-12)
42. Faria VG, Martins NE, Paulo T, Teixeira L, Sucena É, Magalhães S. 2015 Evolution of Drosophila resistance against different pathogens and infection routes entails no detectable maintenance costs. Evolution 69, 2799-2809. (doi:10.1111/evo.12782)
43. Turelli M. 1994 Evolution of incompatibilityinducing microbes and their hosts. Evolution 48, 1500-1513. (doi:10.2307/2410244)
44. Hoffmann A, Clancy D, Merton E. 1994 Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster. Genetics 136, 993-999.
45. Reynolds KT, Hoffmann AA. 2002 Male age, host effects and the weak expression or non-expression of cytoplasmic incompatibility in Drosophila strains infected by maternally transmitted Wolbachia. Genet. Res. 80, 79-87. (doi:10.1017/ S0016672302005827)
46. Engelstädter J, Hurst GDD. 2009 The ecology and evolution of microbes that manipulate host reproduction. Annu. Rev. Ecol. Evol. Syst. 40, 127-149. (doi:10.1146/annurev.ecolsys.110308.120206)
47. Crotti E et al. 2012 Microbial symbionts: a resource for the management of insect-related problems. Microb. Biotechnol. 5, 307-317. (doi:10.1111/j. 1751-7915.2011.00312.x)
48. Bull JJ, Turelli M. 2013 Wolbachia versus dengue: evolutionary forecasts. Evol. Med. Public Health 2013, 197-201. (doi:10.1093/emph/eot018)