Arthropod Endosymbiosis and Evolution

  • Jennifer A. White
  • Massimo Giorgini
  • Michael R. Strand
  • Francesco Pennacchio


The association of “two species that live on or in one another” was first described in the nineteenth century, and the word symbiosis was proposed to denote this biological phenomenon (Sapp 1994). The discovery that lichens are organisms generated by the integration of a fungus and blue-green algae, that is, cyanobacteria, was followed by a number of other studies that have shown how the association of different species is widespread in nature and characterized by different degrees of benefit-sharing. Symbiosis encompasses both antagonistic relationships, in which one organism takes advantage of the other, and mutualistic relationships, where both partners gain advantage from their association. There are also cases where no clear benefit or harm is evident for both interacting species, which are then, in some cases, considered commensals. The term symbiosis applies to all these type of species associations, and not only to mutualism, as is sometimes erroneously done (Sapp 1994).


  1. Adachi-Hagimori T, Miura K, Abe Y (2011) Gene flow between sexual and asexual strains of parasitic wasps: a possible case of sympatric speciation caused by a parthenogenesis-inducing bacterium. J Evol Biol 24:1254–1262PubMedCrossRefGoogle Scholar
  2. Adachi-Hagimori T, Miura K, Stouthamer R (2008) A new cytogenetic mechanism for bacterial endosymbiont-induced parthenogenesis in Hymenoptera. Proc R Soc B 275:2667–2673PubMedCrossRefGoogle Scholar
  3. Allen JM, Light JE, Perotti MA, Braig HR, Reed DL (2009) Mutational meltdown in primary endosymbionts: selection limits Muller’s ratchet. PLoS ONE 4(3):e4969. doi:10.1371/journal.pone.0004969
  4. Anbutsu H, Fukatsu T (2011) Spiroplasma as a model insect endosymbiont. Environ Microbiol Rep 3:144–153CrossRefGoogle Scholar
  5. Arakaki N, Noda H, Yamagishi K (2000) Wolbachia-induced parthenogenesis in the egg parasitoid Telenomus nawai. Entom Exper Appl 96:177–184CrossRefGoogle Scholar
  6. Batut J, Andersson SG, O’Callaghan D (2004) The evolution of chronic infection strategies in the alpha-proteobacteria. Nat Rev Microbiol 2:933–945PubMedCrossRefGoogle Scholar
  7. Baumann P (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189PubMedCrossRefGoogle Scholar
  8. Bentley JK, Veneti Z, Heraty J, Hurst GD (2007) The pathology of embryo death caused by the male-killing Spiroplasma bacterium in Drosophila nebulosa. BMC Biol 5:9. doi:10.1186/1741-7007-5-9
  9. Bézier A, Annaheim M, Herbiniere J, Wetterwald C, Gyapay G, Bernard-Samain S, Wincker P, Roditi I, Heller M, Belghazi M, Pfister-Wilhem R, Periquet G, Dupuy C, Huguet E, Volkoff A-N, Lanzrein B, Drezen J-M (2009) Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323:926–930PubMedCrossRefGoogle Scholar
  10. Bideshi DK, Bigot Y, Federici BA, Spears T (2010) Ascoviruses. In: Asgari S, Johnson K (eds) Insect virology. Caister Academic, Norfolk, pp 3–34Google Scholar
  11. Bigot Y, Rabouille A, Doury G, Sizaret P-Y, Delbost F, Hamelin M-H, Periquet G (1997) Biological and molecular features of the relationships between Diadromus pulchellus ascovirus, a parasitoid hymenopteran wasp (Diadromus pulchellus) and its lepidopteran host, Acrolepiopsis assectella. J Gen Virol 78:1149–1163PubMedGoogle Scholar
  12. Bonning BC (2005) Baculoviruses: biology, biochemistry, and molecular biology. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science, vol 6. Elsevier, Amsterdam, pp 233–270CrossRefGoogle Scholar
  13. Bordenstein SR (2003) Symbiosis and the origin of species. In: Bourtzis K, Miller TA (eds) Insect symbiosis, vol 1. CRC Press, Boca Raton, pp 283–304CrossRefGoogle Scholar
  14. Bordenstein SR, Bordenstein SR (2011) Temperature affects the tripartite interactions between bacteriophage WO, Wolbachia, and cytoplasmic incompatibility. PLoS One 6(12):e29106. doi:10.1371/journal.pone.0029106
  15. Bordenstein SR, O’Hara FP, Werren JH (2001) Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409:707–710PubMedCrossRefGoogle Scholar
  16. Bossan B, Koehncke A, Hammerstein P (2011) A new model and method for understanding Wolbachia-induced cytoplasmic incompatibility. PLoS ONE 6(5):e19757. doi:10.1371/journal.pone.0019757
  17. Bouchon D, Cordaux R, Grève P (2009) Feminizing Wolbachia and the evolution of sex determination in isopods. In: Bourtzis K, Miller TA (eds) Insect symbiosis, vol 3., CRCBoca Raton, FL, pp 273–294Google Scholar
  18. Bourtzis K, Braig HR, Karr TL (2003) Cytoplasmic incompatibility. In: Bourtzis K, Miller TA (eds) Insect symbiosis, vol 1. CRC, Boca Raton, pp 217–246CrossRefGoogle Scholar
  19. Braquart-Varnier C, Lachat M, Herbiniere J, Johnson M, Caubet Y, Bouchon D, Sicard M (2008) Wolbachia mediate variation of host immunocompetence. PLoS One 3 (9):e3286. doi:10.1371/journal.pone.0003286
  20. Breeuwer JA, Werren JH (1990) Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346:558–560PubMedCrossRefGoogle Scholar
  21. Breeuwer JAJ, Werren JH (1995) Hybrid breakdown between two haplodiploid species: the role of nuclear and cytoplasmic genes. Evolution 49:705–717CrossRefGoogle Scholar
  22. Brennan LJ, Keddie BA, Braig HR, Harris HL (2008) The endosymbiont Wolbachia pipientis induces the expression of host antioxidant proteins in an Aedes albopictus cell line. PLoS ONE 3(5):e2083. doi:10.1371/journal.pone.0002083 PubMedCrossRefGoogle Scholar
  23. Bressan A, Arneodo J, Simonato M, Haines WP, Boudon-Padieu E (2009) Characterization and evolution of two bacteriome-inhabiting symbionts in cixiid planthoppers (Hemiptera: Fulgoromorpha: Pentastirini). Environ Microbiol 11:3265–3279PubMedCrossRefGoogle Scholar
  24. Brownlie JC, Johnson KN (2009) Symbiont-mediated protection in insect hosts. Trends Microbiol 17:348–354PubMedCrossRefGoogle Scholar
  25. Brumin M, Kontsedalov S, Ghanim M (2011) Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci 18:57–66CrossRefGoogle Scholar
  26. Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Interscience, New YorkGoogle Scholar
  27. Burke GR, Strand MR (2012) Deep sequencing identifies viral and wasp genes with potential roles in replication of Microplitis demolitor bracovirus. J Virol 86:3293–3306PubMedCrossRefGoogle Scholar
  28. Carolan JC, Caragea D, Reardon KT, Mutti NS, Dittmer N, Pappan K, Cui F, Castanet M, Poulain J, Dossat C, Tagu D, Reese JC, Reeck GR, Wilkinson TL, Edwards OR (2011) Predicted effector molecules in the salivary secretome of the pea aphid (Acyrthosiphon pisum): a dual transcriptomic/proteomic approach. J Proteome Res 10:1505–1518PubMedCrossRefGoogle Scholar
  29. Carrapiço F (2010) How symbiogenic is evolution? Theory Biosci 129:135–139PubMedCrossRefGoogle Scholar
  30. Caspi-Fluger A, Inbar M, Mozes-Daube N, Katzir N, Portnoy V, Belausov E, Hunter MS, Zchori-Fein E (2012) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc R Soc B 279:1791–1796PubMedCrossRefGoogle Scholar
  31. Caubet Y, Hatcher MJ, Mocquard JP, Rigaud T (2000) Genetic conflict and changes in heterogametic mechanisms of sex determination. J Evol Biol 13:766–777CrossRefGoogle Scholar
  32. Champion de Crespigny FE, Hurst LD, Wedell N (2008) Do Wolbachia-associated incompatibilities promote polyandry? Evolution 62:107–122PubMedCrossRefGoogle Scholar
  33. Champion de Crespigny FE, Wedell N (2006) Wolbachia infection reduces sperm competitive ability in an insect. Proc R Soc B 273:1455–1458PubMedCrossRefGoogle Scholar
  34. Champion de Crespigny FE, Wedell N (2007) Mate preferences in Drosophila infected with Wolbachia? Behav Ecol Sociobiol 61:1229–1235CrossRefGoogle Scholar
  35. Chapman RF (1998) The insects: structure and function, 4th edn. Cambridge University Press, New YorkCrossRefGoogle Scholar
  36. Charlat S, Hornett EA, Fullard JH, Davies N, Roderick GK, Wedell N, Hurst GD (2007a) Extraordinary flux in sex ratio. Science 317:214PubMedCrossRefGoogle Scholar
  37. Charlat S, Hurst GDD, Merçot H (2003) Evolutionary consequences of Wolbachia infections. Trends Genet 19:217–223PubMedCrossRefGoogle Scholar
  38. Charlat S, Reuter M, Dyson EA, Hornett EA, Duplouy A, Davies N, Roderick GK, Wedell N, Hurst GD (2007b) Male-killing bacteria trigger a cycle of increasing male fatigue and female promiscuity. Curr Biol 17:273–277PubMedCrossRefGoogle Scholar
  39. Charles H, Condemine G, Nardon C, Nardon P (1997) Genome size characterization of the principal endocellular symbiotic bacteria of the weevil Sitophilus oryzae, using pulsed field gel electrophoresis. Insect Biochem Mol Biol 27:345–350CrossRefGoogle Scholar
  40. Chevalier F, Herbiniere-Gaboreau J, Charif D, Mitta G, Gavory F, Wincker P, Greve P, Braquart-Varnier C, Bouchon D (2012) Feminizing Wolbachia: a transcriptomics approach with insights on the immune response genes in Armadillidium vulgare. BMC Microbiol 12(1):S1. doi:1471-2180-12-S1-S1 [pii] 10.1186/1471-2180-12-S1-S1
  41. Clark EL, Karley AJ, Hubbard SF (2010) Insect endosymbionts: manipulators of insect herbivore trophic interactions? Protoplasma 244:25–51PubMedCrossRefGoogle Scholar
  42. Clark ME, Bailey-Jourdain C, Ferree PM, England SJ, Sullivan W, Windsor DM, Werren JH (2008) Wolbachia modification of sperm does not always require residence within developing sperm. Heredity 101:420–428PubMedCrossRefGoogle Scholar
  43. Colvin J, Omongo CA, Govindappa MR, Stevenson PC, Maruthi MN et al (2006) Host-plant viral infection effects on arthropod-vector population growth, development and behaviour: management and epidemiological implications. Adv Virol Res 67:419–452CrossRefGoogle Scholar
  44. Conord C, Despres L, Vallier A, Balmand S, Miquel C, Zundel S, Lemperiere G, Heddi A (2008) Long-term evolutionary stability of bacterial endosymbiosis in Curculionoidea: additional evidence of symbiont replacement in the Dryophthoridae family. Mol Biol Evol 25:859–868PubMedCrossRefGoogle Scholar
  45. Darby AC, Choi JH, Wilkes T, Hughes MA, Werren JH, Hurst GDD, Colbourne JK (2010) Characteristics of the genome of Arsenophonus nasoniae, son-killer bacterium of the wasp Nasonia. Insect Mol Biol 19:75–89PubMedCrossRefGoogle Scholar
  46. Dedeine F, Ahrens M, Calcaterra L, Shoemaker DD (2005) Social parasitism in fire ants (Solenopsis spp.): a potential mechanism for interspecies transfer of Wolbachia. Mol Ecol 14:1543–1548PubMedCrossRefGoogle Scholar
  47. Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Bouletreau M (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci USA 98:6247–6252PubMedCrossRefGoogle Scholar
  48. Degnan PH, Leonardo TE, Cass BN, Hurwitz B, Stern D, Gibbs RA, Richards S, Moran NA (2010) Dynamics of genome evolution in facultative symbionts of aphids. Environ Microbiol 12:2060–2069PubMedGoogle Scholar
  49. Degnan PH, Moran NA (2008) Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage. Mol Ecol 17:916–929PubMedCrossRefGoogle Scholar
  50. Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA (2009) Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci USA 106:9063–9068PubMedCrossRefGoogle Scholar
  51. De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Métraux J-P, Van Loon LC, Dicke M, Pieterse CMJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant-Microbe Interact 18:923–937PubMedCrossRefGoogle Scholar
  52. Dion E, Zele F, Simon JC, Outreman Y (2011) Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts. J Evol Biol 24:741–750PubMedCrossRefGoogle Scholar
  53. Dixon AFG (1998) Aphid ecology. Chapman and Hall, LondonGoogle Scholar
  54. Dobson SL, Bourtzis K, Braig HR, Jones BF, Zhou W, Rousset F, O’Neill SL (1999) Wolbachia infections are distributed throughout insect somatic and germ line tissue. Insect Biochem Mol Biol 29:153–160PubMedCrossRefGoogle Scholar
  55. Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev 64:409–434PubMedCrossRefGoogle Scholar
  56. Drezen JM, Herniou EA, Bézier A (2012) Evolutionary progenitors of bracoviruses. In: Beckage NE, Drezen JM (eds) Parasitoid viruses. Elsevier, Amsterdam, pp 15–31CrossRefGoogle Scholar
  57. Dunn AM, Andrews T, Ingrey H, Riley J, Wedell N (2006) Strategic sperm allocation under parasitic sex-ratio distortion. Biol Lett 2:78–80PubMedCrossRefGoogle Scholar
  58. Dunning Hotopp JC (2011) Horizontal gene transfer between bacteria and animals. Trends Genet 27:157–163PubMedCrossRefGoogle Scholar
  59. Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstadter J, Hurst GD (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6:27. doi:10.1186/1741-7007-6-27
  60. Duron O, Wilkes TE, Hurst GD (2010) Interspecific transmission of a male-killing bacterium on an ecological timescale. Ecol Lett 13:1139–1148PubMedCrossRefGoogle Scholar
  61. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223PubMedCrossRefGoogle Scholar
  62. Engelstädter J, Hurst GDD (2009) The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst 40:127–149CrossRefGoogle Scholar
  63. Falabella P, Perugino G, Caccialupi P, Riviello L, Varricchio P, Tranfaglia A, Rossi M, Malva C, Graziani F, Moracci M, Pennacchio F (2005) A novel fatty acid binding protein produced by teratocytes of the aphid parasitoid Aphidius ervi. Insect Mol Biol 14:195–205PubMedCrossRefGoogle Scholar
  64. Falabella P, Riviello L, De Stradis ML, Stigliano C, Varricchio P, Grimaldi A, de Eguileor M, Graziani F, Gigliotti S, Pennacchio F (2009) Aphidius ervi teratocytes release an extracellular enolase. Insect Biochem Mol Biol 39:801–813PubMedCrossRefGoogle Scholar
  65. Federici BA (1991) Viewing polydnaviruses as gene vectors of endoparasitic Hymenoptera. Redia 74:387–392Google Scholar
  66. Fereres A, Moreno A (2009) Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Res 14:158–168CrossRefGoogle Scholar
  67. Ferrari J, Scarborough CL, Godfray HCJ (2007) Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids. Oecologia 153:323–329PubMedCrossRefGoogle Scholar
  68. Ferrari J, West JA, Via S, Godfray HCJ (2012) Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution 66:375–390PubMedCrossRefGoogle Scholar
  69. Ferree PM, Avery A, Azpurua J, Wilkes T, Werren JH (2008) A bacterium targets maternally inherited centrosomes to kill males in Nasonia. Curr Biol 18:1409–1414PubMedCrossRefGoogle Scholar
  70. Frydman HM, Li JM, Robson DN, Wieschaus E (2006) Somatic stem cell niche tropism in Wolbachia. Nature 441:509–512PubMedCrossRefGoogle Scholar
  71. Fukatsu T, Hosokawa T, Koga R, Nikoh N, Kato T, Hayama S, Takefushi H, Tanaka I (2009) Intestinal endocellular symbiotic bacterium of the macaque louse Pedicinus obtusus: distinct endosymbiont origins in anthropoid primate lice and the old world monkey louse. Appl Environ Microbiol 75:3796–3799PubMedCrossRefGoogle Scholar
  72. Fytrou A, Schofield PG, Kraaijeveld AR, Hubbard SF (2006) Wolbachia infection suppresses both host defence and parasitoid counter-defence. Proc R Soc B 273:791–796PubMedCrossRefGoogle Scholar
  73. Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156:145–169CrossRefGoogle Scholar
  74. Gempe T, Beye M (2011) Function and evolution of sex determination mechanisms, genes and pathways in insects. BioEssays 33:52–60PubMedCrossRefGoogle Scholar
  75. Gibson CM, Hunter MS (2010) Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecol Lett 13:223–234PubMedCrossRefGoogle Scholar
  76. Giorgini M, Bernardo U, Monti MM, Nappo AG, Gebiola M (2010) Rickettsia symbionts cause parthenogenetic reproduction in the parasitoid wasp Pnigalio soemius (Hymenoptera: Eulophidae). Appl Environ Microbiol 76:2589–2599PubMedCrossRefGoogle Scholar
  77. Giorgini M, Monti MM, Caprio E, Stouthamer R, Hunter MS (2009) Feminization and the collapse of haplodiploidy in an asexual parasitoid wasp harboring the bacterial symbiont Cardinium. Heredity 102:365–371PubMedCrossRefGoogle Scholar
  78. Giron D, Kaiser W, Imbault N, Casas J (2007) Cytokinin-mediated leaf manipulation by a leafminer caterpillar. Biol Lett 3:340–343PubMedCrossRefGoogle Scholar
  79. Gottlieb Y, Zchori-Fein E (2001) Irreversible thelytokous reproduction in Muscidifurax uniraptor. Entom Exper Appl 100:271–278CrossRefGoogle Scholar
  80. Gottlieb Y, Zchori-Fein E, Werren JH, Karr TL (2002) Diploidy restoration in Wolbachia-infected Muscidifurax uniraptor (Hymenoptera: Pteromalidae). J Invert Pathol 81:166–174CrossRefGoogle Scholar
  81. Gross R, Vavre F, Heddi A, Hurst GDD, Zchori-Fein E, Bourtzis K (2009) Immunity and symbiosis. Mol Microbiol 73:751–759PubMedCrossRefGoogle Scholar
  82. Gruwell ME, Hardy NB, Gullan PJ, Dittmar K (2010) Evolutionary relationships among primary endosymbionts of the mealybug subfamily Phenacoccinae (Hemiptera: Coccoidea: Pseudococcidae). Appl Environ Microbiol 76:7521–7525PubMedCrossRefGoogle Scholar
  83. Gündüz EA, Douglas AE (2009) Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc R Soc B 276:987–991CrossRefGoogle Scholar
  84. Hansen AK, Moran NA (2011) Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc Natl Acad Sci USA 108:2849–2854PubMedCrossRefGoogle Scholar
  85. Harmon JP, Moran NA, Ives AR (2009) Species response to environmental change: impacts of food web interactions and evolution. Science 323:1347–1350PubMedCrossRefGoogle Scholar
  86. Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702PubMedCrossRefGoogle Scholar
  87. 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 281:215–220PubMedCrossRefGoogle Scholar
  88. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, Chiel E, Duckworth VE, Dennehy TJ, Zchori-Fein E, Hunter MS (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254–256PubMedCrossRefGoogle Scholar
  89. Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci USA 107:769–774PubMedCrossRefGoogle Scholar
  90. Huguet E, Serbielle C, Moreau SJM (2012) Evolution and origin of polydnavirus virulence genes. In: Beckage NE, Drezen JM (eds) Parasitoid viruses. Elsevier, Amsterdam, pp 63–78CrossRefGoogle Scholar
  91. Huigens ME, de Almeida RP, Boons PA, Luck RF, Stouthamer R (2004a) Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc R Soc B 271:509–515PubMedCrossRefGoogle Scholar
  92. Huigens ME, Hohmann CL, Luck RF, Gort G, Stouthamer R (2004b) Reduced competitive ability due to Wolbachia infection in the parasitoid wasp Trichogramma kaykai. Entom Exper Appl 110:115–123CrossRefGoogle Scholar
  93. Huigens ME, Stouthamer R (2003) Parthenogenesis associated with Wolbachia. In: Bourtzis K, Miller TA (eds) Insect symbiosis, vol 2., CRCBoca Raton, FL, pp 247–266Google Scholar
  94. Hunter MS, Zchori-Fein E (2006) Inherited bacteroidetes symbionts in arthropods. In: Bourtzis K, Miller TA (eds) Insect symbiosis, vol 2., CRCBoca Raton, FL, pp 39–56CrossRefGoogle Scholar
  95. Hurst GDD, Jiggins FM, Majerus MEN (2003) Inherited microorganisms that selectively kill male hosts: the hidden players of insect evolution? In: Bourtzis K, Miller TA (eds) Insect symbiosis, vol 2., CRCBoca Raton, FL, pp 177–198CrossRefGoogle Scholar
  96. Ijichi N, Kondo N, Matsumoto R, Shimada M, Ishikawa H, Fukatsu T (2002) Internal spatio-temporal population dynamics of infection with three Wolbachia strains in the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae). Appl Environ Microbiol 68:4074–4080Google Scholar
  97. Jaenike J (2009) Coupled population dynamics of endosymbionts within and between hosts. Oikos 118:353–362CrossRefGoogle Scholar
  98. Jaenike J, Dyer KA, Cornish C, Minhas MS (2006) Asymmetrical reinforcement and Wolbachia infection in Drosophila. PLoS Biol 4(10):e325. doi: 10.1371/journal.pbio.0040325
  99. Jaenike J, Dyer KA, Reed LK (2003) Within-population structure of competition and the dynamics of male-killing Wolbachia. Evol Ecol Res 5:1023–1036Google Scholar
  100. Jaenike J, Polak M, Fiskin A, Helou M, Minhas M (2007) Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 3:23–25PubMedCrossRefGoogle Scholar
  101. Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212–215PubMedCrossRefGoogle Scholar
  102. Jehle JA (2010) Nudiviruses: their biology and genetics. In: Asgari S, Johnson K (eds) Insect virology. Caister Academic, Norfolk, pp 153–170Google Scholar
  103. Jiggins FM, Hurst GDD, Majerus MEN (2000) Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proc R Soc B 267:69–73PubMedCrossRefGoogle Scholar
  104. Jiu M, Zhou XP, Tong L, Xu J, Yang X, Wan F-H, LiuS-S (2007) Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS ONE 2(1):e182. doi:10.1371/journal.pone.0000182
  105. Johnstone RA, Hurst GDD (1996) Maternally inherited male-killing microorganisms may confound interpretation of mitochondrial DNA variability. Biol J Linn Soc 58:453–470CrossRefGoogle Scholar
  106. Kaiser W, Huguet E, Casas J, Commin C, Giron D (2010) Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proc R Soc B 277:2311–2319PubMedCrossRefGoogle Scholar
  107. Kambris Z, Blagborough AM, Pinto SB, Blagrove MS, Godfray HC, Sinden RE, Sinkins SP (2010) Wolbachia stimulates immune gene expression and inhibits plasmodium development in Anopheles gambiae. PLoS Pathog 6(10):e1001143. doi:10.1371/journal.ppat.1001143
  108. Kenyon SG, Hunter MS (2007) Manipulation of oviposition choice of the parasitoid wasp, Encarsia pergandiella, by the endosymbiotic bacterium Cardinium. J Evol Biol 20:707–716PubMedCrossRefGoogle Scholar
  109. Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM, Lee SH, Robertson HM, Kennedy RC, Elhaik E, Gerlach D, Kriventseva EV, Elsik CG, Graur D, Hill CA, Veenstra JA, Walenz B, Tubío JMC, Ribeiro JMC, Rozas J, Johnston JS, Reese JT, Popadic A, Tojo M, Raoult D, Reed DL, Tomoyasu Y, Krause E, Mittapalli O, Margam VM, Li H-M, Meyer JM, Johnson RM, Romero-Severson J, Pagel VanZee J, Alvarez-Ponce D, Vieira FG, Aguadé M, Guirao-Rico S, Anzola JM, Yoon KS, Strycharz JP, Unger MF, Christley S, Lobo NF, Seufferheld MJ, Wang NK, Dasch GA, Struchiner CJ, Madey G, Hannick LI, Bidwell S, Joardar V, Caler E, Shao R, Barker SC, Cameron S, Bruggner RV, Regier A, Johnson J, Viswanathan L, Utterback TR, Sutton GG, Lawson D, Waterhouse RM, Venter JC, Strausberg RL, Berenbaum MR, Collins FH, Zdobnov EM, Pittendrigh BR (2010) Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci USA 107:12168–12173PubMedCrossRefGoogle Scholar
  110. Klasson L, Westberg J, Sapountzis P, Nasiund K, Lutnaes Y, Darby AC, Veneti Z, Chen LM, Braig HR, Garrett R, Bourtzis K, Andersson SGE (2009) The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci USA 106:5725–5730PubMedCrossRefGoogle Scholar
  111. Kluth S, Kruess A, Tscharntke T (2002) Insects as vectors of plant pathogens: mutualistic and antagonistic interactions. Oecologia 133:193–199CrossRefGoogle Scholar
  112. Koukou K, Pavlikaki H, Kilias G, Werren JH, Bourtzis K, Alahiotis SN (2006) Influence of antibiotic treatment and Wolbachia curing on sexual isolation among Drosophila melanogaster cage populations. Evolution 60:87–96PubMedGoogle Scholar
  113. Kuechler SM, Dettner K, Kehl S (2010) Molecular characterization and localization of the obligate endosymbiotic bacterium in the birch catkin bug Kleidocerys resedae (Heteroptera: Lygaeidae, Ischnorhynchinae). FEMS Microbiol Ecol 73:408–418Google Scholar
  114. Kuechler SM, Dettner K, Kehl S (2011) Characterization of an obligate intracellular bacterium in the midgut epithelium of the bulrush bug Chilacis typhae (Heteroptera, Lygaeidae, Artheneinae). Appl Environ Microbiol 77:2869–2876PubMedCrossRefGoogle Scholar
  115. Kuijper B, Pen I (2010) The evolution of haplodiploidy by male-killing endosymbionts: importance of population structure and endosymbiont mutualisms. J Evol Biol 23:40–52PubMedCrossRefGoogle Scholar
  116. Lamelas A, Gosalbes MJ, Manzano-Marin A, Pereto J, Moya A, Latorre A (2011) Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont. PLoS Genet 7(11):e1002357. doi:10.1371/journal.pgen.1002357
  117. Lamelas A, Perez-Brocal V, Gomez-Valero L, Gosalbes MJ, Moya A, Latorre A (2008) Evolution of the secondary symbiont “Candidatus Serratia symbiotica” in aphid species of the subfamily Lachninae. Appl Environ Microbiol 74:4236–4240PubMedCrossRefGoogle Scholar
  118. Landmann F, Orsi GA, Loppin B, Sullivan W (2009) Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. PLoS Pathog 5(3):e1000343. doi:10.1371/journal.ppat.1000343
  119. Lawrence PO (2005) Morphogenesis and cytopathic effects of the Diachasmimorpha longicaudata entomopoxvirus in host haemocytes. J Insect Physiol 51:221–233PubMedCrossRefGoogle Scholar
  120. Lawrence PO, Akin D (1990) Virus-like particles in the accessory glands of Biosteres longicaudatus. Can J Zool 68:539–546CrossRefGoogle Scholar
  121. Lawrence PO, Matos LF (2005) Transmission of the Diachasmimorpha longicaudata rhabdovirus (DlRhV) to wasp offspring: an ultrastructural analysis. J Insect Physiol 51:235–241PubMedCrossRefGoogle Scholar
  122. Leonardo TE (2004) Removal of a specialization-associated symbiont does not affect aphid fitness. Ecol Lett 7:461–468CrossRefGoogle Scholar
  123. Leonardo TE, Muiru GT (2003) Facultative symbionts are associated with host plant specialization in pea aphid populations. Proc R Soc B 270:S209–S212PubMedCrossRefGoogle Scholar
  124. Lewis Z, Champion de Crespigny FE, Sait SM, Tregenza T, Wedell N (2011) Wolbachia infection lowers fertile sperm transfer in a moth. Biol Lett 7:187–189PubMedCrossRefGoogle Scholar
  125. Lewsey MG, Murphy AM, MacLean D, Dalchau N, Westwood JH, Macaulay K, Bennet MH, Moulin M, Hanke DE, Powell G, Smith AG, Carr JP (2010) Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol Plant-Microbe Interact 23:835–845PubMedCrossRefGoogle Scholar
  126. Li S, Falabella P, Giannantonio S, Fanti P, Battaglia D, Digilio MC, Völkl W, Sloggett JJ, Weisser W, Pennacchio F (2002) Pea aphid clonal resistance to the endophagous parasitoid Aphidius ervi. J Insect Physiol 48:971–980PubMedCrossRefGoogle Scholar
  127. Login FH, Balmand S, Vallier A, Vincent-Monegat C, Vigneron A, Weiss-Gayet M, Rochat D, Heddi A (2011) Antimicrobial peptides keep insect endosymbionts under control. Science 334:362–365PubMedCrossRefGoogle Scholar
  128. Lopez-Sanchez MJ, Neef A, Pereto J, Patino-Navarrete R, Pignatelli M, Latorre A, Moya A (2009) Evolutionary convergence and nitrogen metabolism in Blattabacterium strain Bge, primary endosymbiont of the cockroach Blattella germanica. PLoS Genet 5(11):e1000721. doi:10.1371/journal.pgen.1000721
  129. Lukasik P, Hancock EL, Ferrari J, Godfray HCJ (2011) Grain aphid clones vary in frost resistance, but this trait is not influenced by facultative endosymbionts. Ecol Entomol 36:790–793CrossRefGoogle Scholar
  130. Majerus MEN (2003) Sex wars: genes, bacteria and biased sex ratios. Princeton University Press, PrincetonGoogle Scholar
  131. Majerus TM, Majerus ME (2010) Intergenomic arms races: detection of a nuclear rescue gene of male-killing in a ladybird. PLoS Pathog 6(7):e1000987. doi:10.1371/journal.ppat.1000987
  132. Margulis L (1993) Origins of species: acquired genomes and individuality. BioSystems 31(2–3):121–125PubMedCrossRefGoogle Scholar
  133. Margulis L (2009) Genome acquisition in horizontal gene transfer: symbiogenesis and macromolecular sequence analysis. Methods Mol Biol 532:181–191PubMedCrossRefGoogle Scholar
  134. McCutcheon JP, McDonald BR, Moran NA (2009) Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc Natl Acad Sci USA 106:15394–15399PubMedCrossRefGoogle Scholar
  135. McCutcheon JP, Moran NA (2007) Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci USA 104:19392–19397PubMedCrossRefGoogle Scholar
  136. McCutcheon JP, Moran NA (2010) Functional convergence in reduced genomes of bacterial symbionts spanning 200 my of evolution. Genome Biol Evol 2:708–718PubMedGoogle Scholar
  137. McCutcheon JP, von Dohlen CD (2011) An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol 21:1366–1372PubMedCrossRefGoogle Scholar
  138. McLean AHC, van Asch M, Ferrari J, Godfray HCJ (2011) Effects of bacterial secondary symbionts on host plant use in pea aphids. Proc R Soc B 278:760–766PubMedCrossRefGoogle Scholar
  139. Miller WJ, Ehrman L, Schneider D (2010) Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum. PLoS Pathog 6(12):e1001214. doi:10.1371/journal.ppat.1001214
  140. Min K-T, Benzer S (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and death. Proc Nat Acad Sci USA 94:10792–10796PubMedCrossRefGoogle Scholar
  141. Moran NA, Degnan PH, Santos SR, Dunbar HE, Ochman H (2005a) The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci USA 102:16919–16926PubMedCrossRefGoogle Scholar
  142. Moran NA, Dunbar HE (2006) Sexual acquisition of beneficial symbionts in aphids. Proc Natl Acad Sci USA 103:12803–12806PubMedCrossRefGoogle Scholar
  143. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190PubMedCrossRefGoogle Scholar
  144. Moran NA, McLaughlin HJ, Sorek R (2009) The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323:379–382PubMedCrossRefGoogle Scholar
  145. Moran NA, Tran P, Gerardo NM (2005b) Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum bacteroidetes. Appl Environ Microbiol 71:8802–8810PubMedCrossRefGoogle Scholar
  146. Moreira D, Lòpez Garcia P (2009) Ten reasons to exclude viruses from tree of life. Nat Rev Microbiol 7:306–311PubMedGoogle Scholar
  147. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, Rocha BC, Hall-Mendelin S, Day A, Riegler M, Hugo LE, Johnson KN, Kay BH, McGraw EA, van den Hurk AF, Ryan PA, O’Neill SL (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139:1268–1278PubMedCrossRefGoogle Scholar
  148. Müller CB, Williams IS, Hardie J (2001) The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecol Entomol 26:330–340CrossRefGoogle Scholar
  149. Murphy N, Banks JC, Whitfield JB, Austin AD (2008) Phylogeny of the parasitic microgastroid subfamilies (Hymenoptera: Braconidae) based on sequence data from seven genes, with an improved time estimate of the origin of the lineage. Mol Phylogenet Evol 47:378–395PubMedCrossRefGoogle Scholar
  150. Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, Hattori M (2006) The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314:267PubMedCrossRefGoogle Scholar
  151. Nakanishi K, Hoshino M, Nakai M, Kunimi Y (2008) Novel RNA sequences associated with late male killing in Homona magnanima. Proc R Soc B 275:1249–1254PubMedCrossRefGoogle Scholar
  152. Narita S, Kageyama D, Nomura M, Fukatsu T (2007) Unexpected mechanism of symbiont-induced reversal of insect sex: feminizing Wolbachia continuously acts on the butterfly Eurema hecabe during larval development. Appl Environ Microbiol 73:4332–4341PubMedCrossRefGoogle Scholar
  153. Nazzi F, Brown SP, Annoscia D, Del Piccolo F, Di Prisco G, Varricchio P, Della Vedova G, Cattonaro F, Caprio E, Pennacchio F (2012) Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog 8(6):e1002735. doi:10.1371/journal.ppat.1002735 PubMedCrossRefGoogle Scholar
  154. Negri I, Pellecchia M, Mazzoglio PJ, Patetta A, Alma A (2006) Feminizing Wolbachia in Zyginidia pullula (Insecta, Hemiptera), a leafhopper with an XX/X0 sex-determination system. Proc Biol Sci 273:2409–2416PubMedCrossRefGoogle Scholar
  155. Newton ILG, Bordenstein SR (2011) Correlations between bacterial ecology and mobile DNA. Curr Microbiol 62:198–208PubMedCrossRefGoogle Scholar
  156. Normark BB (2004) Haplodiploidy as an outcome of coevolution between male-killing cytoplasmic elements and their hosts. Evolution 58:790–798PubMedGoogle Scholar
  157. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304PubMedCrossRefGoogle Scholar
  158. Oliver KM, Campos J, Moran NA, Hunter MS (2008) Population dynamics of defensive symbionts in aphids. Proc R Soc B 275:293–299PubMedCrossRefGoogle Scholar
  159. Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts of aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55:247–266PubMedCrossRefGoogle Scholar
  160. Oliver KM, Degnan PH, Hunter MS, Moran NA (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325:992–994PubMedCrossRefGoogle Scholar
  161. Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100:1803–1807PubMedCrossRefGoogle Scholar
  162. O’Neill SL, Karr TL (1990) Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348:178–180PubMedCrossRefGoogle Scholar
  163. Pannebakker BA, Loppin B, Elemans CP, Humblot L, Vavre F (2007) Parasitic inhibition of cell death facilitates symbiosis. Proc Natl Acad Sci USA 104:213–215PubMedCrossRefGoogle Scholar
  164. Pannebakker BA, Pijnacker LP, Zwaan BJ, Beukeboom LW (2004) Cytology of Wolbachia-induced parthenogenesis in Leptopilina clavipes (Hymenoptera: Figitidae). Genome 47:299–303PubMedCrossRefGoogle Scholar
  165. Pannebakker BA, Schidlo NS, Boskamp GJ, Dekker L, van Dooren TJ, Beukeboom LW, Zwaan BJ, Brakefield PM, van Alphen JJ (2005) Sexual functionality of Leptopilina clavipes (Hymenoptera: Figitidae) after reversing Wolbachia-induced parthenogenesis. J Evol Biol 18:1019–1028PubMedCrossRefGoogle Scholar
  166. Patot S, Martinez J, Allemand R, Gandon S, Varaldi J, Fleury F (2010) Prevalence of a virus inducing behavioural manipulation near species range border. Mol Ecol 19:2995–3007PubMedCrossRefGoogle Scholar
  167. Pennacchio F, Strand MR (2006) Evolution of developmental strategies in parasitic Hymenoptera. Annu Rev Entomol 51:233–258PubMedCrossRefGoogle Scholar
  168. Perera S, Li Z, Pavlik L, Arif B (2010) Entomopoxviruses. In: Asgari S, Johnson K (eds) Insect virology. Caister Academic, Norfolk, pp 83–102Google Scholar
  169. Perlman SJ, Magnus SA, Copley CR (2010) Pervasive associations between Cybaeus spiders and the bacterial symbiont Cardinium. J Invert Pathol 103:150–155CrossRefGoogle Scholar
  170. Perrot-Minnot MJ, Cheval B, Migeon A, Navajas M (2002) Contrasting effects of Wolbachia on cytoplasmic incompatibility and fecundity in the haplodiploid mite Tetranychus urticae. J Evol Biol 15:808–817CrossRefGoogle Scholar
  171. Pijls JWAM, van Steenbergen HJ, van Alphen JJM (1996) Asexuality cured: the relations and differences between sexual and asexual Apoanagyrus diversicornis. Heredity 76:506–513CrossRefGoogle Scholar
  172. Poinsot D, Bourtzis K, Markakis G, Savakis C, Mercot H (1998) Wolbachia transfer from Drosophila melanogaster into D. simulans: host effect and cytoplasmic incompatibility relationships. Genetics 150:227–237PubMedGoogle Scholar
  173. Poinsot D, Charlat S, Mercot H (2003) On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts. BioEssays 25:259–265PubMedCrossRefGoogle Scholar
  174. Rancés E, Ye YH, Woolfit M, McGraw EA, O’Neill SL (2012) The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog 8(2):e1002548. doi:10.1371/journal.ppat.1002548 PubMedCrossRefGoogle Scholar
  175. Renault S (2012) RNA viruses in parasitoid wasps. In: Beckage NE, Drezen JM (eds) Parasitoid viruses. Elsevier, Amsterdam, pp 193–201CrossRefGoogle Scholar
  176. Renault S, Bigot S, Lemesle M, Sizaret P-Y, Bigot Y (2003) The cypovirus Diadromus pulchellus DpRV-2 is sporadically associated with the endoparasitoid wasp D. pulchellus and modulates the defence mechanisms of pupae of the parasitized leek-moth Acrolepiopsis assectella. J Gen Virol 84:1799–1807PubMedCrossRefGoogle Scholar
  177. Renault S, Stasiak K, Federici BA, Bigot Y (2005) Commensal and mutualistic relationships of reoviruses with their parasitoid wasp hosts. J Insect Physiol 51:137–146PubMedCrossRefGoogle Scholar
  178. Rigaud T, Juchault P (1995) Success and failure of horizontal transfers of feminizing Wolbachia endosymbionts in woodlice. J Evol Biol 8:249–255CrossRefGoogle Scholar
  179. Rigaud T, Moreau J (2004) A cost of Wolbachia-induced sex reversal and female-biased sex ratios: decrease in female fertility after sperm depletion in a terrestrial isopod. Proc R Soc B 271:1941–1946PubMedCrossRefGoogle Scholar
  180. Riparbelli MG, Giordano R, Ueyama M, Callaini G (2012) Wolbachia-mediated male killing is associated with defective chromatin remodeling. PLoS One 7(1):e30045. doi:10.1371/journal.pone.0030045
  181. Rodriguero MS, Confalonieri VA, Guedes JV, Lanteri AA (2010) Wolbachia infection in the tribe Naupactini (Coleoptera, Curculionidae): association between thelytokous parthenogenesis and infection status. Insect Mol Biol 19:631–640PubMedCrossRefGoogle Scholar
  182. Roossinck MJ (2005) Symbiosis versus competition in plant virus evolution. Nature Rev Microbiol 3:917–924CrossRefGoogle Scholar
  183. Ros VI, Breeuwer JA (2009) The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni. Heredity 102:413–422PubMedCrossRefGoogle Scholar
  184. Ross L, Pen I, Shuker DM (2010) Genomic conflict in scale insects: the causes and consequences of bizarre genetic systems. Biol Rev 85:807–828PubMedGoogle Scholar
  185. Rossignol PA et al (1985) Enhanced mosquito blood-finding success on parasitemic host: evidence for vector-parasite mutualism. Proc Natl Acad Sci USA 82:7725–7727PubMedCrossRefGoogle Scholar
  186. Russell JA, Latorre A, Sabater-Munoz B, Moya A, Moran NA (2003) Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol 12:1061–1075PubMedCrossRefGoogle Scholar
  187. Russell JA, Moran NA (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc R Soc B 273:603–610PubMedCrossRefGoogle Scholar
  188. Russell JE, Stouthamer R (2011) The genetics and evolution of obligate reproductive parasitism in Trichogramma pretiosum infected with parthenogenesis-inducing Wolbachia. Heredity 106:58–67PubMedCrossRefGoogle Scholar
  189. Ryabov EV, Keane G, Naish N, Evered C, Winstanley D (2009) Densovirus induces winged morphs in asexual clones of the rosy apple aphid, Dysaphis plantaginea. Proc Natl Acad Sci USA 21:8465–8470CrossRefGoogle Scholar
  190. Ryan F (2002) Darwin’s blind spot. Houghton Miffin, BostonGoogle Scholar
  191. Ryu JH, Ha EM, Lee WJ (2010) Innate immunity and gut-microbe mutualism in Drosophila. Dev Comp Immunol 34:369–376PubMedCrossRefGoogle Scholar
  192. Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14(3):225–274CrossRefGoogle Scholar
  193. Sapp J (1994) Evolution by association. A history of symbiosis. Oxford University Press, New YorkGoogle Scholar
  194. Sapp J (2009) The new foundations of evolution. On the tree of life. Oxford University Press, New YorkGoogle Scholar
  195. Scarborough CL, Ferrari J, Godfray HCJ (2005) Aphid protected from pathogen by endosymbiont. Science 310:1781PubMedCrossRefGoogle Scholar
  196. Serbus LR, Casper-Lindley C, Landmann F, Sullivan W (2008) The genetics and cell biology of Wolbachia-host interactions. Annu Rev Genet 42:683–707PubMedCrossRefGoogle Scholar
  197. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp APS. Nature 407:81–86PubMedCrossRefGoogle Scholar
  198. Shigenobu S, Wilson ACC (2011) Genomic revelations of a mutualism: the pea aphid and its obligate bacterial symbiont. Cell Mol Life Sci 68:1297–1309PubMedCrossRefGoogle Scholar
  199. Sicard M, Chevalier F, De Vlechouver M, Bouchon D, Greve P, Braquart-Varnier C (2010) Variations of immune parameters in terrestrial isopods: a matter of gender, aging and Wolbachia. Naturwissenschaften 97:819–826PubMedCrossRefGoogle Scholar
  200. Silverman N, Paquette N (2008) The right resident bugs. Science 319:734–735PubMedCrossRefGoogle Scholar
  201. Siozios S, Sapountzis P, Ioannidis P, Bourtzis K (2008) Wolbachia symbiosis and insect immune response. Insect Sci 15:89–100CrossRefGoogle Scholar
  202. Snook RR, Cleland SY, Wolfner MF, Karr TL (2000) Offsetting effects of Wolbachia infection and heat shock on sperm production in Drosophila simulans: analyses of fecundity, fertility and accessory gland proteins. Genetics 155:167–178PubMedGoogle Scholar
  203. Stasiak K, Renault S, Federici BA, Bigot Y (2005) Characteristics of pathogenic and mutualistic relationships of ascoviruses in field populations of parasitoid wasps. J Insect Physiol 51:103–115PubMedCrossRefGoogle Scholar
  204. Stout MJ, Thaler JS, Thomma BPHJ (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu Rev Entomol 51:663–689PubMedCrossRefGoogle Scholar
  205. Stouthamer R (1997) Wolbachia-induced parthenogenesis. In: O’Neill SL, Hoffmann AA, Werren JH (eds) Influential passengers: inherited microorganisms and arthropod reproduction. Oxford University Press, Oxford, pp 102–122Google Scholar
  206. Stouthamer R, van Tilborg M, de Jong JH, Nunney L, Luck RF (2001) Selfish element maintains sex in natural populations of a parasitoid wasp. Proc R Soc B 268:617–622PubMedCrossRefGoogle Scholar
  207. Strand MR (2010) Polydnaviruses. In: Asgari S, Johnson K (eds) Insect virology. Caister Academic, Norfolk, pp 171–197Google Scholar
  208. Strand MR (2012) Polydnavirus gene products that interact with the host immune system. In: Beckage NE, Drezen JM (eds) Parasitoid viruses. Elsevier, Amsterdam, pp 149–161CrossRefGoogle Scholar
  209. Sugimoto TN, Ishikawa Y (2012) A male-killing Wolbachia carries a feminizing factor and is associated with degradation of the sex-determining system of its host. Biol Lett 8:412–415PubMedCrossRefGoogle Scholar
  210. Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC, Boca RatonGoogle Scholar
  211. Tamas I, Klasson L, Canback B, Naslund AK, Eriksson AS, Wernegreen JJ, Sandstrom JP, Moran NA, Andersson SGE (2002) 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376–2379PubMedCrossRefGoogle Scholar
  212. Tamas I, Wernegreen JJ, Nystedt B, Kauppinen SN, Darby AC, Gomez-Valero L, Lundin D, Poole AM, Andersson SGE (2008) Endosymbiont gene functions impaired and rescued by polymerase infidelity at poly(A) tracts. Proc Natl Acad Sci USA 105:14934–14939PubMedCrossRefGoogle Scholar
  213. Telschow A, Flor M, Kobayashi Y, Hammerstein P, Werren JH (2007) Wolbachia-induced unidirectional cytoplasmic incompatibility and speciation: mainland-island model. PLoS One 2(8):e701. doi:10.1371/journal.pone.0000701
  214. Telschow A, Hammerstein P, Werren JH (2005) The effect of Wolbachia versus genetic incompatibilities on reinforcement and speciation. Evolution 59:1607–1619PubMedGoogle Scholar
  215. Terry RS, Smith JE, Sharpe RG, Rigaud T, Littlewood DT, Ironside JE, Rollinson D, Bouchon D, MacNeil C, Dick JT, Dunn AM (2004) Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proc R Soc B 271:1783–1789PubMedCrossRefGoogle Scholar
  216. Thomma BPHJ, Penninckx IAMA, Broekaert WF, Cammue BPA (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13:63–68PubMedCrossRefGoogle Scholar
  217. Toft C, Andersson SGE (2010) Evolutionary microbial genomics: insights into bacterial host adaptation. Nat Rev Genet 11:465–475PubMedCrossRefGoogle Scholar
  218. Toju H, Fukatsu T (2011) Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Mol Ecol 20:853–868PubMedCrossRefGoogle Scholar
  219. Toju H, Hosokawa T, Koga R, Nikoh N, Meng XY, Kimura N, Fukatsu T (2010) “Candidatus Curculioniphilus buchneri”, a novel clade of bacterial endocellular symbionts from weevils of the genus Curculio. Appl Environ Microbiol 76:275–282PubMedCrossRefGoogle Scholar
  220. Tram U, Sullivan W (2002) Role of delayed nuclear envelope breakdown and mitosis in Wolbachia induced cytoplasmic incompatibility. Science 296:1124–1126Google Scholar
  221. Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989PubMedCrossRefGoogle Scholar
  222. 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 11:2123–2135PubMedCrossRefGoogle Scholar
  223. Turelli M (1994) Evolution of incompatibility-inducing microbes and their hosts. Evolution 48:1500–1513CrossRefGoogle Scholar
  224. Vala F, Egas M, Breeuwer JA, Sabelis MW (2004) Wolbachia affects oviposition and mating behaviour of its spider mite host. J Evol Biol 17:692–700PubMedCrossRefGoogle Scholar
  225. Varaldi J, Boulétreau M, Fleury F (2005) Cost induced by viral particles manipulating superparasitism behaviour in the parasitoid Leptopilina boulardi. Parasitology 131:161–168PubMedCrossRefGoogle Scholar
  226. Varaldi J, Patot S, Nardin M, Gandon S (2009) A virus-shaping reproductive strategy in a Drosophila parasitoid. Adv Parasitol 70:333–363PubMedCrossRefGoogle Scholar
  227. Varaldi J, Martinez J, Patot S, Lepetit D, Fleury F, Gandon S (2012) An inherited virus manipulating the behavior of its parasitoid host: epidemiology and evolutionary consequences. In: Beckage NE, Drezen JM (eds) Parasitoid viruses. Elsevier, Amsterdam, pp 203–214CrossRefGoogle Scholar
  228. Vavre F, de Jong JH, Stouthamer R (2004) Cytogenetic mechanism and genetic consequences of thelytoky in the wasp Trichogramma cacoeciae. Heredity 93:592–596PubMedCrossRefGoogle Scholar
  229. Veneti Z, Bentley JK, Koana T, Braig HR, Hurst GD (2005) A functional dosage compensation complex required for male killing in Drosophila. Science 307:1461–1463PubMedCrossRefGoogle Scholar
  230. Veneti Z, Clark ME, Karr TL, Savakis C, Bourtzis K (2004) Heads or tails: host-parasite interactions in the Drosophila-Wolbachia system. Appl Environ Microbiol 70:5366–5372PubMedCrossRefGoogle Scholar
  231. Villarreal LP (2005) Viruses and the evolution of life. ASM, Washington DCGoogle Scholar
  232. Vogel KJ, Moran NA (2011) Sources of variation in dietary requirements in an obligate nutritional symbiosis. Proc R Soc B 278:115–121PubMedCrossRefGoogle Scholar
  233. Volkoff AN, Jouan V, Urbach S, Samain S, Bergoin M, Wincker P, et al (2010) Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. PLoS Pathog 6, e1000923. doi: 10.1371/journal.ppat.1000923
  234. Vorburger C, Gehrer L, Rodriguez P (2010) A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol Lett 6:109–111PubMedCrossRefGoogle Scholar
  235. Wang Y, Jehle JA (2009) Nudiviruses and other large, double-stranded circular DNA viruses of invertebrates: new insights on an old topic. J Invertebr Pathol 101:187–193PubMedCrossRefGoogle Scholar
  236. Webb B, Strand MR (2005) The biology and genomics of polydnaviruses. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science, vol 6. Elsevier, Amsterdam, pp 323–360CrossRefGoogle Scholar
  237. Weeks AR, Breeuwer JA (2001) Wolbachia-induced parthenogenesis in a genus of phytophagous mites. Proc Biol Sci 268:2245–2251PubMedCrossRefGoogle Scholar
  238. Weeks AR, Marec F, Breeuwer JAJ (2001) A mite species that consists entirely of haploid females. Science 292:2479–2482PubMedCrossRefGoogle Scholar
  239. Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA (2007) From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5(5):e114. doi:10.1371/journal.pbio.0050114
  240. Weinert LA, Werren JH, Aebi A, Stone GN, Jiggins FM (2009) Evolution and diversity of Rickettsia bacteria. BMC Biol 7:6. doi:10.1186/1741-7007-7-6
  241. Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42:587–609PubMedCrossRefGoogle Scholar
  242. Werren JH (1998) Wolbachia and speciation. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, Oxford, pp 245–260Google Scholar
  243. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751PubMedCrossRefGoogle Scholar
  244. Werren JH, Beukeboom LW (1998) Sex determination, sex ratios and genetic conflict. Annu Rev Ecol Syst 29:233–261CrossRefGoogle Scholar
  245. Werren JH, O’Neil S (1997) The evolution of heritable symbionts. In: O’Neil S, Hoffmann AA, Werren JH (eds) Influential passengers: inherited microorganisms and arthropod reproduction. Oxford University Press, New York, pp 1–41Google Scholar
  246. Werren JH, Richards S, Desjardins CA et al (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327:343–348PubMedCrossRefGoogle Scholar
  247. Werren JH, Zhang W, Guo LR (1995) Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc R Soc Lond B Biol Sci 261:55–63CrossRefGoogle Scholar
  248. Wetterwald C, Roth T, Kaeslin M, Annaheim M, Wespi G, Heller M, Mäser P, Roditi I, Pfister-Wilhelm R, Bézier A, Gyapay G, Drezen JM, Lanzrein B (2010) Identification of bracovirus particle proteins and analysis of their transcript levels at the stage of virion formation. J Gen Virol 91:2610–2619PubMedCrossRefGoogle Scholar
  249. White JA (2011) Caught in the act: rapid, symbiont-driven evolution. BioEssays 33:823–829PubMedCrossRefGoogle Scholar
  250. White JA, Kelly SE, Perlman SJ, Hunter MS (2009) Cytoplasmic incompatibility in the parasitic wasp Encarsia inaron: disentangling the roles of Cardinium and Wolbachia symbionts. Heredity 102:483–489PubMedCrossRefGoogle Scholar
  251. Whitfield JB (2002) Estimating the age of the polydnavirus/braconid wasp symbiosis. Proc Natl Acad Sci USA 99:7508–7513PubMedCrossRefGoogle Scholar
  252. Wong ZS, Hedges LM, Brownlie JC, Johnson KN (2011) Wolbachia-mediated antibacterial protection and immune gene regulation in Drosophila. PLoS ONE 6(9):e25430. doi:10.1371/journal.pone.0025430 PubMedCrossRefGoogle Scholar
  253. Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875PubMedCrossRefGoogle Scholar
  254. Zchori-Fein E, Perlman SJ (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 13:2009–2016PubMedCrossRefGoogle Scholar
  255. Zeh JA, Zeh DW (2006) Male-killing Wolbachia in a live-bearing arthropod: brood abortion as a constraint on the spread of a selfish microbe. J Invert Pathol 92:33–38CrossRefGoogle Scholar
  256. Zera AJ, Denno RF (1997) Physiology and ecology of dispersal polymorphism in insects. Annu Rev Entomol 42:207–230PubMedCrossRefGoogle Scholar
  257. Zheng Y, Ren PP, Wang JL, Wang YF (2011a) Wolbachia-induced cytoplasmic incompatibility is associated with decreased Hira expression in male Drosophila. PLoS One 6(4):e19512. doi:10.1371/journal.pone.0019512
  258. Zheng Y, Wang JL, Liu C, Wang CP, Walker T, Wang YF (2011b) Differentially expressed profiles in the larval testes of Wolbachia infected and uninfected Drosophila. BMC Genomics 12:595. doi:10.1186/1471-2164-12-595

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Jennifer A. White
    • 1
  • Massimo Giorgini
    • 2
  • Michael R. Strand
    • 3
  • Francesco Pennacchio
    • 4
  1. 1.Department of EntomologyUniversity of KentuckyLexingtonUSA
  2. 2.Istituto per la Protezione delle Piante, CNRPorticiItaly
  3. 3.Department of EntomologyUniversity of GeorgiaAthensUSA
  4. 4.Dipartimento di Agraria Laboratorio di Entomologia “E. Tremblay”Università di Napoli “Federico II”PorticiItaly

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