Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps

Heredity

Volumn 112, Issue 4, 2014, Pages 399-408

  Xie, J ^a   Butler, S ^a   Sanchez, G ^a   Mateos, M ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

cytoplasmic incompatibility; defensive mutualism; heritable endosymbiont; insect endosymbiont; Mollicutes; reproductive manipulation

Indexed keywords

BACTERIUM; COEXISTENCE; CYTOPLASMIC INCOMPATIBILITY; DIVERGENCE; ENDOSYMBIONT; EVOLUTIONARY BIOLOGY; FITNESS; FLY; HERITABILITY; HOST RANGE; HOST-SYMBIONT INTERACTION; MATERNAL EFFECT; NATURAL ENEMY; NEMATODE; PARASITOID; WASP;

BACTERIA (MICROORGANISMS); DROSOPHILA MELANOGASTER; HEXAPODA; LEPTOPILINA BOULARDI; LEPTOPILINA HETEROTOMA; MELANOGASTER; MOLLICUTES; SPIROPLASMA; VESPOIDEA; VESPULA VULGARIS; WOLBACHIA;

ANIMAL; CYTOPLASM; DEFENSE MECHANISM; DROSOPHILA MELANOGASTER; EVOLUTION; FEMALE; MALE; MICROBIOLOGY; PARASITOLOGY; PHYSIOLOGY; SPIROPLASMA; SURVIVAL; SYMBIOSIS; WASP; WOLBACHIA;

ANIMALS; BIOLOGICAL EVOLUTION; CYTOPLASM; DEFENSE MECHANISMS; DROSOPHILA MELANOGASTER; FEMALE; MALE; SPIROPLASMA; SURVIVAL ANALYSIS; SYMBIOSIS; WASPS; WOLBACHIA;

EID: 84896493528     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2013.118     Document Type: Article

References (67)

1. Bian GW, Xu Y, Lu P, Xie Y, Xi ZY (2010). The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathogen 6: E1000833
2. Brownlie JC, Johnson KN (2009). Symbiont-mediated protection in insect hosts. Trends Microbiol 17: 348-354
3. Douglas AE (1998). Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43: 17-37
4. Dyer KA, Jaenike J (2004). Evolutionarily stable infection by a male-killing endosymbiont in Drosophila innubila: Molecular evidence from the host and parasite genomes. Genetics 168: 1443-1455
5. Engelstadter J, Hurst GDD (2009). The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst 40: 127-149
6. Ferrari J, Vavre F (2011). Bacterial symbionts in insects or the story of communities affecting communities. Philos Trans R Soc Ser B 366: 1389-1400
7. Fleury F, Gibert P, Ris N, Allemand R (2009). Ecology and life history evolution of frugivorous Drosophila parasitoids. Adv Parasitol 70: 3-44
8. Frentiu FD, Robinson J, Young PR, McGraw EA, O'Neill SL (2010). Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PLoS One 5: E13398
9. Fytrou A, Schofield PG, Kraaijeveld AR, Hubbard SF (2006). Wolbachia infection suppresses both host defence and parasitoid counter-defence. Proc R Soc Ser B 273: 791-796
10. 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
11. Goto S, Anbutsu H, Fukatsu T (2006). Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Appl Environ Microbiol 72: 4805-4810
12. Gueguen G, Rajwani R, Paddibhatla I, Morales J, Govind S (2011). VLPs of Leptopilina boulardi share biogenesis and overall stellate morphology with VLPs of the heterotoma clade. Virus Res 160: 159-165
13. Haselkorn TS, Markow TA, Moran NA (2009). Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol Ecol 18: 1294-1305
14. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN (2008). Wolbachia and virus protection in insects. Science 322: 702
15. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008). How many species are infected with Wolbachia?-A statistical analysis of current data. FEMS Microbiol Lett 281: 215-220
16. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE et al. (2011). Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332: 254-256
17. Hurst GDD, Hutchence KJ (2010). Host defence: Getting by with a little help from our friends. Curr Biol 20: R806-R808
18. Hurst LD (1991). The incidences and evolution of cytoplasmic male killers. Proc R Soc Ser B 244: 91-99
19. Iturbe-Ormaetxe I, Walker T, Neill SLO (2011). Wolbachia and the biological control of mosquito-borne disease. EMBO Rep 12: 508-518
20. Jaenike J (2012). Population genetics of beneficial heritable symbionts. Trends Ecol Evol 27: 226-232
21. Jaenike J, Stahlhut JK, Boelio LM, Unckless RL (2010a). Association between Wolbachia and Spiroplasma within Drosophila neotestacea: An emerging symbiotic mutualism? Mol Ecol 19: 414-425
22. Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ (2010b). Adaptation via symbiosis: Recent spread of a Drosophila defensive symbiont. Science 329: 212-215
23. Kacsoh BZ, Schlenke TA (2012). High hemocyte load is associated with increased resistance against parasitoids in Drosophila suzukii, a relative of D. melanogaster. PLoS One 7: E34721
24. Kraaijeveld AR, Barker CL, Godfray HCJ (2008). Stage-specific sex differences in Drosophila immunity to parasites and pathogens. Evol Ecol 22: 217-228
25. Lee MJ, Kalamarz ME, Paddibhatla I, Small C, Rajwani R, Govind S (2009). Virulence factors and strategies of Leptopilina spp.: Selective responses in Drosophila hosts. Adv Parasitol 70: 123-145
26. Lemaitre B, Hoffmann J (2007). The host defense of Drosophila melanogaster. Annu Rev Immunol 25: 697-743
27. Longdon B, Fabian D, Hurst G, Jiggins F (2012). Male-killing Wolbachia do not protect Drosophila bifasciata against viral infection. BMC Microbiol 12: S8
28. Lukasik P, van Asch M, Guo H, Ferrari J, Charles JGH, van Der Putten W (2012). Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecol Lett 16: 214-218
29. Martinez J, Duplouy A, Woolfit M, Vavre F, O'Neill SL, Varaldi J (2012). Influence of the virus LbFV and of Wolbachia in a host-parasitoid interaction. PLoS One 7: E35081
30. Martins AB, Ventura I, Klaczko L (2010). Spiroplasma infection in Drosophila melanogaster: What is the advantage of killing males? J Invertebr Pathol 105: 145-150
31. Mateos M, Castrezana SJ, Nankivell BJ, Estes AM, Markow TA, Moran NA (2006 Heritable endosymbionts of Drosophila. Genetics 174: 363-376
32. Montenegro H, Petherwick A, Hurst G, Klaczko L (2006). Fitness effects of Wolbachia and Spiroplasma in Drosophila melanogaster. Genetica 127: 207-215
33. Montenegro H, Solferini VN, Klaczko LB, Hurst GDD (2005). Male-killing Spiroplasma naturally infecting Drosophila melanogaster. Insect Mol Biol 14: 281-288
34. Montenegro H, Souza WN, Leite DDS, Klaczko LB (2000). Male-killing selfish cytoplasmic element causes sex-ratio distortion in Drosophila melanogaster. Heredity 85: 465-470
35. Morales J, Chiu H, Oo T, Plaza R, Hoskins S, Govind S (2005). Biogenesis, structure, and immune-suppressive effects of virus-like particles of a Drosophila parasitoid, Leptopilina victoriae. J Insect Physiol 51: 181-195
36. Moran NA, McCutcheon JP, Nakabachi A (2008). Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165-190
37. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu GJ, Pyke AT, Hedges LM et al. (2009). A Wolbachia symbiont in Aedes aegypti limits infection with Dengue, Chikungunya, and Plasmodium. Cell 139: 1268-1278
38. Nunes MD, Nolte V, Schlotterer C (2008). Nonrandom Wolbachia infection status of Drosophila melanogaster strains with different mtDNA haplotypes. Mol Biol Evol 25: 2493-2498
39. O'Neill SL, Hoffmann AA, Werren JH (1997). Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford University Press: New York, NY, USA
40. Oliver K, Russell J, Moran N, Hunter M (2003). Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100: 1803-1807
41. Oliver KM, Moran NA, Hunter MS (2005). Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102: 12795-12800
42. Oliver KM, Noge K, Huang EM, Campos JM, Becerra JX, Hunter MS (2012). Parasitic wasp responses to symbiont-based defense in aphids. BMC Biol 10: 11
43. Osborne SE, Leong YS, O'Neill SL, Johnson KN (2009). Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathogen 5: E1000656
44. Ota T, Kawabe M, Oishi K, Poulson DF (1979). Non-male-killing spiroplasmas in Drosophila hydei. J Hered 70: 211-213
45. Patot S, Lepetit D, Charif D, Varaldi J, Fleury F (2009). Molecular detection, penetrance, and transmission of an inherited virus responsible for behavioral manipulation of an insect parasitoid. Appl Environ Microbiol 75: 703-710
46. Richardson MF, Weinert LA, Welch JJ, Linheiro RS, Magwire MM, Jiggins FM et al. (2012 Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster. PLoS Genet 8: E1003129
47. Riegler M, Sidhu M, Miller WJ, O'Neill SL (2005). Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr Biol 15: 1428-1433
48. Russo J, Dupas S, Frey F, Carton Y, Brehelin M (1996). Insect immunity: Early events in the encapsulation process of parasitoid (Leptopilina boulardi) eggs in resistant and susceptible strains of Drosophila. Parasitology 112: 135-142
49. Scarborough CL, Ferrari J, Godfray HCJ (2005). Aphid protected from pathogen by endosymbiont. Science 310: 1781-1781
50. Schlenke TA, Morales J, Govind S, Clark AG (2007). Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. PLoS Pathogen 3: 1486-1501
51. Silva N, Guenther L, Xie J, Mateos M (2012). Infection densities of three Spiroplasma strains in the host Drosophila melanogaster. Symbiosis 57: 83-93
52. Tamura K, Subramanian S, Kumar S (2004). Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol 21: 36-44
53. 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
54. Thomas P, Kenny N, Eyles D, Moreira LA, O'Neill SL, Asgari S (2011). Infection with the wMel and wMelPop strains of Wolbachia leads to higher levels of melanization in the hemolymph of Drosophila melanogaster, Drosophila simulans and Aedes aegypti. Dev Comp Immunol 35: 360-365
55. Unckless RL, Jaenike J (2012). Maintenance of a male-killing Wolbachia in Drosophila innubila by male-killing dependent and male-killing independent mechanisms. Evolution 66: 678-689
56. Varaldi J, Fouillet P, Ravallec M, Lopez-Ferber M, Bouletreau M, Fleury F (2003). Infectious behavior in a parasitoid. Science 302: 1930-1930
57. Varaldi J, Ravallec M, Labrosse C, Lopez-Ferber M, Bouletreau M, Fleury F (2006). Artifical transfer and morphological description of virus particles associated with superparasitism behaviour in a parasitoid wasp. J Insect Physiol 52: 1202-1212
58. Ventura IM, Martins AB, Lyra ML, Andrade CA, Carvalho KA, Klaczko LB (2012 Spiroplasma in Drosophila melanogaster populations: Prevalence, male-killing, molecular identification, and no association with Wolbachia. Microb Ecol 64: 794-801
59. Vorburger C, Sandrock C, Gouskov A, Castañeda LE, Ferrari J (2009). Genotypic variation and the role of defensive endosymbionts in an all-parthenogenetic host-parasitoid interaction. Evolution 63: 1439-1450
60. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ et al. (2011). The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476: 450-U101
61. Werren JH, Baldo L, Clark ME (2008). Wolbachia: Master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741-751
62. White J, Giorgini M, Strand M, Pennacchio F (2013). Arthropod endosymbiosis and evolution. In: Minelli A, Boxshall G, Fusco G (eds.) Arthropod Biology and Evolution. Springer: Berlin, Heidelberg, Germany, pp 441-477
63. Williams MJ, Wiklund ML, Wikman S, Hultmark D (2006). Rac1 signalling in the Drosophila larval cellular immune response. J Cell Sci 119: 2015-2024
64. Xie J, Tiner B, Vilchez I, Mateos M (2011). Effect of the Drosophila endosymbiont Spiroplasma on parasitoid wasp development and on the reproductive fitness of waspattacked fly survivors. Evol Ecol 25: 1065-1079
65. Xie J, Vilchez I, Mateos M (2010). Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS One 5: E12149
66. Zele F, Nicot A, Duron O, Rivero A (2012). Infection with Wolbachia protects mosquitoes against Plasmodium-induced mortality in a natural system. J Evol Biol 25: 1243-1252
67. Zug R, Hammerstein P (2012). Still a host of hosts for Wolbachia: Analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 7: E38544