Microbial Ecology

, Volume 70, Issue 1, pp 287–297 | Cite as

Dynamics of the Endosymbiont Rickettsia in an Insect Pest

  • Bodil N. Cass
  • Rachel Yallouz
  • Elizabeth C. Bondy
  • Netta Mozes-Daube
  • A. Rami Horowitz
  • Suzanne E. Kelly
  • Einat Zchori-Fein
  • Martha S. Hunter
Invertebrate Microbiology

Abstract

A new heritable bacterial association can bring a fresh set of molecular capabilities, providing an insect host with an almost instantaneous genome extension. Increasingly acknowledged as agents of rapid evolution, inherited microbes remain underappreciated players in pest management programs. A Rickettsia bacterium was tracked sweeping through populations of an invasive whitefly provisionally described as the “B” or “MEAM1” of the Bemisia tabaci species complex, in the southwestern USA. In this population, Rickettsia provides strong fitness benefits and distorts whitefly sex ratios under laboratory conditions. In contrast, whiteflies in Israel show few apparent fitness benefits from Rickettsia under laboratory conditions, only slightly decreasing development time. A survey of B. tabaci B samples revealed the distribution of Rickettsia across the cotton-growing regions of Israel and the USA. Thirteen sites from Israel and 22 sites from the USA were sampled. Across the USA, Rickettsia frequencies were heterogeneous among regions, but were generally very high, whereas in Israel, the infection rates were lower and declining. The distinct outcomes of Rickettsia infection in these two countries conform to previously reported phenotypic differences. Intermediate frequencies in some areas in both countries may indicate a cost to infection in certain environments or that the frequencies are in flux. This suggests underlying geographic differences in the interactions between bacterial symbionts and this serious agricultural pest.

Keywords

Whitefly Bemisia tabaci Middle East-Asia Minor 1 (MEAM1) Bemisia argentifolii B biotype Diagnostic PCR 

Supplementary material

248_2015_565_MOESM1_ESM.docx (59 kb)
ESM 1(DOCX 59 kb)
248_2015_565_MOESM2_ESM.docx (344 kb)
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248_2015_565_MOESM3_ESM.docx (282 kb)
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References

  1. 1.
    Azad AF, Beard CB (1998) Rickettsial pathogens and their arthropod vectors. Emerg Infect Dis 4:179–186. doi:10.3201/eid0402.980205 PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Biere A, Tack AJM (2013) Evolutionary adaptation in three-way interactions between plants, microbes and arthropods. Funct Ecol 27:646–660. doi:10.1111/1365-2435.12096 CrossRefGoogle Scholar
  3. 3.
    Bing XL, Ruan YM, Rao Q, Wang XW, Liu SS (2013) Diversity of secondary endosymbionts among different putative species of the whitefly Bemisia tabaci. Insect Sci 20:194–206. doi:10.1111/j.1744-7917.2012.01522.x PubMedCrossRefGoogle Scholar
  4. 4.
    Bing XL, Yang J, Zchori-Fein E, Wang XW, Liu SS (2013) Characterization of a newly discovered symbiont in the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Appl Environ Microbiol 79:569–575. doi:10.1128/AEM.03030-12 PubMedCentralPubMedCrossRefGoogle Scholar
  5. 5.
    Boykin LM, Shatters RG Jr, Rosell RC, McKenzie CL, Bagnall RA, De Barro P, Frohlich DR (2007) Global relationships of Bemisia tabaci (Hemiptera: Aleyrodidae) revealed using Bayesian analysis of mitochondrial COI DNA sequences. Mol Phylogenet Evol 44:1306–1319. doi:10.1016/j.ympev.2007.04.020 PubMedCrossRefGoogle Scholar
  6. 6.
    Brown JK, Frohlich DR, Rosell RC (1995) The sweetpotato or silverleaf whiteflies: Biotypes of Bemisia tabaci or a species complex. Annu Rev Entomol 40:511–534. doi:10.1146/annurev.en.40.010195.002455 CrossRefGoogle Scholar
  7. 7.
    Brumin M, Kontsedalov S, Ghanim M (2011) Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci 18:57–66. doi:10.1111/j.1744-7917.2010.01396.x CrossRefGoogle Scholar
  8. 8.
    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 Biol Sci 279:1791–1796. doi:10.1098/rspb.2011.2095 PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Caspi-Fluger A, Inbar M, Mozes-Daube N, Mouton L, Hunter MS, Zchori-Fein E (2011) Rickettsia 'in' and 'out': two different localization patterns of a bacterial symbiont in the same insect species. PLoS One 6:e21096. doi:10.1371/journal.pone.0021096 PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Chiel E, Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Katzir N, Inbar M, Ghanim M (2007) Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bull Entomol Res 97:407–413. doi:10.1017/S0007485307005159 PubMedCrossRefGoogle Scholar
  11. 11.
    Chiel E, Inbar M, Mozes-Daube N, White JA, Hunter MS, Zchori-Fein E (2009) Assessments of fitness effects by the facultative symbiont Rickettsia in the sweetpotato whitefly (Hemiptera: Aleyrodidae). Ann Entomol Soc Am 102:413–418. doi:10.1603/008.102.0309 CrossRefGoogle Scholar
  12. 12.
    Chiel E, Zchori-Fein E, Inbar M, Gottlieb Y, Adachi-Hagimori T, Kelly SE, Asplen MK, Hunter MS (2009) Almost there: transmission routes of bacterial symbionts between trophic levels. PLoS One 4:e4767. doi:10.1371/journal.pone.0004767 PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Chu D, Cong B, Zhang YJ, Xu BY, Wu QJ, Zhu GR (2005) Detection and phylogenetic analysis of Wolbachia in different Bemisia tabaci biotypes. Acta Entomol Sinica 48:518–525Google Scholar
  14. 14.
    Chu D, Gao CS, De Barro P, Zhang YJ, Wan FH, Khan IA (2011) Further insights into the strange role of bacterial endosymbionts in whitefly. Bemisia tabaci: comparison of secondary symbionts from biotypes B and Q in China. Bull Entomol Res 101:477–486. doi:10.1017/S0007485311000083 PubMedCrossRefGoogle Scholar
  15. 15.
    Davis MJ, Ying ZT, Brunner BR, Pantoja A, Ferwerda FH (1998) Rickettsial relative associated with papaya bunchy top disease. Curr Microbiol 36:80–84. doi:10.1007/s002849900283 PubMedCrossRefGoogle Scholar
  16. 16.
    De Barro P, Ahmed MZ (2011) Genetic networking of the Bemisia tabaci cryptic species complex reveals pattern of biological invasions. PLoS One 6:e25579. doi:10.1371/journal.pone.0025579 PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    De Barro PJ, Liu SS, Boykin LM, Dinsdale AB (2010) Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19. doi:10.1146/annurev-ento-112408-085504 CrossRefGoogle Scholar
  18. 18.
    De Barro PJ, Scott KD, Graham GC, Lange CL, Schutze MK (2003) Isolation and characterization of microsatellite loci in Bemisia tabaci. Mol Ecol Notes 3:40–43. doi:10.1046/j.1471-8286.2003.00344.x CrossRefGoogle Scholar
  19. 19.
    Deguine JP, Ferron P, Russell D (2008) Sustainable pest management for cotton production. A review. Agron Sustain Devel 28:113–137. doi:10.1007/978-90-481-2666-8_27 CrossRefGoogle Scholar
  20. 20.
    Dennehy TJ, Degain BA, Harpold VS, Brown JK, Morin S, Fabrick JA, Byrne FJ, Nichols RL (2005) New challenges to management of whitefly resistance to insecticides in Arizona. The University of Arizona Co-operative Extension Report, Tucson, AZGoogle Scholar
  21. 21.
    Dickey AM, Osborne LS, Shatters RG Jr, Hall PA, Mckenzie CL (2013) Population genetics of invasive Bemisia tabaci (Hemiptera: Aleyrodidae) cryptic species in the United States based on microsatellite markers. J Econ Entomol 106:1355–1364. doi:10.1603/EC12512 PubMedCrossRefGoogle Scholar
  22. 22.
    Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev Camb Philos Soc 64:409–434PubMedCrossRefGoogle Scholar
  23. 23.
    Duplouy A, Hurst GDD, O’Neill SL, Charlat S (2010) Rapid spread of a male-killing Wolbachia in the butterfly Hypolimnas bolina. J Evol Biol 23:231–235. doi:10.1111/j.1420-9101.2009.01891.x PubMedCrossRefGoogle Scholar
  24. 24.
    Everett KDE, Thao ML, Horn M, Dyszynski GE, Baumann P (2005) Novel chlamydiae in whiteflies and scale insects: endosymbionts 'Candidatus Fritschea bemisiae' strain Falk and 'Candidatus Fritschea eriococci' strain Elm. Int J Syst Evol Microbiol 55:1581–1587. doi:10.1099/ijs. 0.63454-0 PubMedCrossRefGoogle Scholar
  25. 25.
    Ferrari J, Scarborough CL, Godfray HCJ (2007) Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids. Oecologia 153:323–329. doi:10.1007/s00442-007-0730-2 PubMedCrossRefGoogle Scholar
  26. 26.
    Fournier PE, Raoult D (2007) Identification of rickettsial isolates at the species level using multi-spacer typing. BMC Microbiol 7:72. doi:10.1186/1471-2180-7-72 PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Frohlich DR, Torres-Jerez I, Bedford ID, Markham PG, Brown JK (1999) A phylogeographical analysis of the Bemisia tabaci species complex based on mitochondrial DNA markers. Mol Ecol 8:1683–1691. doi:10.1046/j.1365-294x.1999.00754.x PubMedCrossRefGoogle Scholar
  28. 28.
    Ghanim M, Kontsedalov S (2009) Susceptibility to insecticides in the Q biotype of Bemisia tabaci is correlated with bacterial symbiont densities. Pest Manag Sci 65:939–942. doi:10.1002/ps.1795 PubMedCrossRefGoogle Scholar
  29. 29.
    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 76:2589–2599. doi:10.1128/AEM. 03154-09 PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, Tzuri G, Horowitz AR, Belausov E, Mozes-Daube N, Kontsedalov S, Gershon M, Gal S, KatZir N, Zchori-Fein E (2006) Identification and localization of a Rickettsia sp in Bemisia tabaci (Homoptera : Aleyrodidae). Appl Environ Microbio 72:3646–3652. doi:10.1128/AEM.72.5.3646–3652.2006 CrossRefGoogle Scholar
  31. 31.
    Gottlieb Y, Ghanim M, Gueguen G, Kontsedalov S, Vavre F, Fleury F, Zchori-Fein E (2008) Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB J 22:2591–2599. doi:10.1096/fj.07-101162 PubMedCrossRefGoogle Scholar
  32. 32.
    Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Kontsedalov S, Skaljac M et al (2010) The transmission efficiency of tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. J Virol 84:9310–9317. doi:10.1128/JVI. 00423-10 PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Gueguen G, Vavre F, Gnankine O, Peterschmitt M, Charif D, Chiel E, Gottlieb Y, Ghanim M, Zchori-Fein E, Fleury F (2010) Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Mol Ecol 19:4365–4378. doi:10.1111/j.1365-294X.2010.04775.x PubMedCrossRefGoogle Scholar
  34. 34.
    Hagimori T, Abe Y, Date S, Miura K (2006) The first finding of a Rickettsia bacterium associated with parthenogenesis induction among insects. Curr Microbiol 52:97–101. doi:10.1007/s00284-005-0092-0 PubMedCrossRefGoogle Scholar
  35. 35.
    Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702. doi:10.1126/science.1162418 PubMedCrossRefGoogle Scholar
  36. 36.
    Henry LM, Peccoud J, Simon J, Hadfield JD, Maiden MJC, Ferrari J, Godfray HCJ (2013) Horizontally transmitted symbionts and host colonization of ecological niches. Curr Biol 23:1713–1717. doi:10.1016/j.cub.2013.07.029 PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Hequet E, Henneberry TJ (2007) Sticky cotton - causes, impacts and prevention. United States Department of Agriculture Agricultural Research Service Technical Bulletin No. 1915Google Scholar
  38. 38.
    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 332:254–256. doi:10.1126/science.1199410 PubMedCrossRefGoogle Scholar
  39. 39.
    Hoffman AA, Clancy DJ, Merton E (1994) Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster. Genetics 136:993–999Google Scholar
  40. 40.
    Hoffmann AA, Hercus M, Dagher H (1998) Population dynamics of the Wolbachia infection causing cytoplasmic incompatibility in Drosophila melanogaster. Genetics 148:221–231PubMedCentralPubMedGoogle Scholar
  41. 41.
    Hoffmann AA, Turelli M, Harshman LG (1990) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126:933–948PubMedCentralPubMedGoogle Scholar
  42. 42.
    Hornett EA, Engelstädter J, Hurst GD (2009) Hidden cytoplasmic incompatibility alters the dynamics of male-killer/host interactions. J Evol Biol 23:479–487. doi:10.1111/j.1420-9101.2009.01872.x PubMedCrossRefGoogle Scholar
  43. 43.
    Horowitz AR, Denholm I, Gorman K, Ceñís JL, Kontsedalov S, Ishaaya I (2003) Biotype Q of Bemisia tabaci identified in Israel. Phytoparasitica 31:94–98CrossRefGoogle Scholar
  44. 44.
    Horowitz AR, Ishaaya I (2014) Dynamics of biotypes B and Q of the whitefly Bemisia tabaci and their impact on insecticide resistance. Pest Manag Sci 70:1568–1572. doi:10.1002/ps.3752 PubMedCrossRefGoogle Scholar
  45. 45.
    Horowitz AR, Weintraub PG, Ishaaya I (1998) Status of pesticide resistance in arthropod pests in Israel. Phytoparasitica 26:231–240. doi:10.1007/BF02981438 CrossRefGoogle Scholar
  46. 46.
    Jansen VA, Turelli M, Godfray HC (2008) Stochastic spread of Wolbachia. Proc Biol Sci 275:2769–2776. doi:10.1098/rspb.2008.0914 PubMedCentralPubMedCrossRefGoogle Scholar
  47. 47.
    Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212–215. doi:10.1126/science.1188235 PubMedCrossRefGoogle Scholar
  48. 48.
    Jones DR (2003) Plant viruses transmitted by whiteflies. Eur J Plant Pathol 109:195–219. doi:10.1023/A:1022846630513 CrossRefGoogle Scholar
  49. 49.
    Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. doi:10.1093/molbev/mst010 PubMedCentralPubMedCrossRefGoogle Scholar
  50. 50.
    Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont-mediated insecticide resistance. Proc Natl Acad Sci U S A 109:8618–8622. doi:10.1073/pnas.1200231109 PubMedCentralPubMedCrossRefGoogle Scholar
  51. 51.
    Kikuchi Y, Hosokawa T, Fukatsu T (2007) Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol 73:4308–4316. doi:10.1128/AEM. 00067-07 PubMedCentralPubMedCrossRefGoogle Scholar
  52. 52.
    Kontsedalov S, Zchori-Fein E, Chiel E, Gottlieb Y, Inbar M, Ghanim M (2008) The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Manag Sci 64:789–792. doi:10.1002/ps.1595 PubMedCrossRefGoogle Scholar
  53. 53.
    Kriesner P, Hoffmann AA, Lee SF, Turelli M, Weeks AR (2013) Rapid sequential spread of two Wolbachia variants in Drosophila simulans. PLoS Pathog 9:e1003607. doi:10.1371/journal.ppat.1003607 PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.
    Lawson ET, Mousseau TA, Klaper R, Hunter MD, Werren JH (2001) Rickettsia associated with male-killing in a buprestid beetle. Heredity 86:497–505. doi:10.1046/j.1365-2540.2001.00848.x PubMedCrossRefGoogle Scholar
  55. 55.
    Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. doi:10.1006/meth.2001.1262 PubMedCrossRefGoogle Scholar
  56. 56.
    Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the World’s worst invasive alien species: a selection from the global invasive species database. The IUCN Invasive Species SpecialistGroup, AucklandGoogle Scholar
  57. 57.
    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. doi:10.1111/ele.12031 PubMedCrossRefGoogle Scholar
  58. 58.
    Luttrell RG, Fitt GP, Ramalho FS, Sugonyaev ES (1994) Cotton pest management: part 1. A worldwide perspective. Annu Rev Entomol 9:517–526CrossRefGoogle Scholar
  59. 59.
    McKenzie CL, Hodges G, Osborne LS, Byrne FJ, Shatters RG Jr (2009) Distribution of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in Florida—investigating the Q invasion. J Econ Entomol 102:670–676. doi:10.1603/029.102.0227 PubMedCrossRefGoogle Scholar
  60. 60.
    Mitchell J, Carter L, Munk D, Klonsky K, Hutmacher R, Shrestha A, DeMoura R, Wroble J (2012) Conservation tillage systems for cotton advance in the San Joaquin Valley. Calif Agric 66:108–115. doi:10.3733/ca.v066n03p108 CrossRefGoogle Scholar
  61. 61.
    Morag N, Klement E, Saroya Y, Lensky I, Gottlieb Y (2012) Prevalence of the symbiont Cardinium in Culicoides (Diptera: Ceratopogonidae) vector species is associated with land surface temperature. FASEB J 26:4025–4034. doi:10.1096/fj.12-210419 PubMedCrossRefGoogle Scholar
  62. 62.
    Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190. doi:10.1146/annurev.genet.41.110306.130119 PubMedCrossRefGoogle Scholar
  63. 63.
    Naranjo SE, Ellsworth PC (2009) Fifty years of the integrated control concept: moving the model and implementation forward in Arizona. Pest Manag Sci 65:1267–1286. doi:10.1002/ps.1861 PubMedCentralPubMedCrossRefGoogle Scholar
  64. 64.
    Nirgianaki A, Banks GK, Frohlich DR, Veneti Z, Braig HR, Miller TA, Bedford ID, Markham PG, Savakis C, Bourtzis K (2003) Wolbachia infections of the whitefly Bemisia tabaci. Curr Microbiol 47:93–101. doi:10.1007/s00284-002-3969-1 PubMedCrossRefGoogle Scholar
  65. 65.
    Oliveira MRV, Henneberry TJ, Anderson P (2001) History, current status, and collaborative research projects for Bemisia tabaci. Crop Prot 20:709–723. doi:10.1016/S0261-2194(01)00108-9 CrossRefGoogle Scholar
  66. 66.
    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 U S A 102:12795–12800. doi:10.1073/pnas.0506131102 PubMedCentralPubMedCrossRefGoogle Scholar
  67. 67.
    Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci U S A 100:1803–1807. doi:10.1073/pnas.0335320100 PubMedCentralPubMedCrossRefGoogle Scholar
  68. 68.
    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:e1000656. doi:10.1371/journal.ppat.1000656 PubMedCentralPubMedCrossRefGoogle Scholar
  69. 69.
    Perlman SJ, Hunter MS, Zchori-Fein E (2006) The emerging diversity of Rickettsia. Proc Biol Sci 273:2097–2106. doi:10.1098/rspb.2006.3541 PubMedCentralPubMedCrossRefGoogle Scholar
  70. 70.
    Perlman SJ, Kelly SE, Hunter MS (2008) Population biology of cytoplasmic incompatibility: maintenance and spread of Cardinium symbionts in a parasitic wasp. Genetics 178:1003–1011. doi:10.1534/genetics.107.083071 PubMedCentralPubMedCrossRefGoogle Scholar
  71. 71.
    Perring TM (2001) The Bemisia tabaci species complex. Crop Prot 20:725–737. doi:10.1016/S0261-2194(01)00109-0 CrossRefGoogle Scholar
  72. 72.
    Riegler M, Sidhu M, Miller WJ, O’Neill SL (2005) Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr Biol 15:1428–1433. doi:10.1016/j.cub.2005.06.069 PubMedCrossRefGoogle Scholar
  73. 73.
    R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/.
  74. 74.
    Roux V, Rydkina E, Eremeeva M, Raoult D (1997) Citrate synthase gene comparison, a new tool for phylogenetic analysis, and its application for the Rickettsiae. Int J Syst Bacteriol 47:252–261. doi:10.1099/00207713-47-2-252 PubMedCrossRefGoogle Scholar
  75. 75.
    Russell JA, Moran NA (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc Biol Sci 273:603–610. doi:10.1098/rspb.2005.3348 PubMedCentralPubMedCrossRefGoogle Scholar
  76. 76.
    Scarborough CL, Ferrari J, Godfray HC (2005) Aphid protected from pathogen by endosymbiont. Science 310:1781. doi:10.1126/science.1120180 PubMedCrossRefGoogle Scholar
  77. 77.
    Schneider DI, Garschall KI, Parker AG, Abd-Alla AM, Miller WJ (2013) Global Wolbachia prevalence, titer fluctuations and their potential of causing cytoplasmic incompatibilities in tsetse flies and hybrids of Glossina morsitans subgroup species. J Invertebr Pathol 112(Suppl):S104–S115. doi:10.1016/j.jip.2012.03.024 PubMedCentralPubMedCrossRefGoogle Scholar
  78. 78.
    Sloan DB, Moran NA (2012) Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biol Lett 8:986–989. doi:10.1098/rsbl.2012.0664 PubMedCentralPubMedCrossRefGoogle Scholar
  79. 79.
    Stamatakis A (2006) RAxML-VI-HPC: maximum Likelihood based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. doi:10.1093/bioinformatics/btl446 PubMedCrossRefGoogle Scholar
  80. 80.
    Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029 PubMedCentralPubMedCrossRefGoogle Scholar
  81. 81.
    Tay WT, Evans GA, Boykin LM, De Barro PJ (2012) Will the real Bemisia tabaci please stand up? PLoS One 7:e50550. doi:10.1371/journal.pone.0050550 PubMedCentralPubMedCrossRefGoogle Scholar
  82. 82.
    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 CrossRefGoogle Scholar
  83. 83.
    Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989. doi:10.1126/science.1094611 PubMedCrossRefGoogle Scholar
  84. 84.
    Turelli M, Hoffmann AA (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353:440–442. doi:10.1038/353440a0 PubMedCrossRefGoogle Scholar
  85. 85.
    Turelli M, Hoffmann AA (1995) Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140:1319–1338PubMedCentralPubMedGoogle Scholar
  86. 86.
    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. doi:10.1111/j.1558-5646.2011.01485.x PubMedCrossRefGoogle Scholar
  87. 87.
    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. doi:10.1111/j.1558-5646.2009.00660.x PubMedCrossRefGoogle Scholar
  88. 88.
    Weeks AR, Breeuwer JA (2003) A new bacterium from the Cytophaga–Flavobacterium–Bacteroides phylum that causes sex ratio distortion. In: Bourtzis K, Miller TA (eds) Insect symbiosis. CRC Press Boca Raton, FL, pp 165–176. doi:10.1201/9780203009918.ch11 CrossRefGoogle Scholar
  89. 89.
    Werren JH, Hurst GDD, Zhang W, Breeuwer JA, Stouthamer R, Majerus ME (1994) Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata). J Bacteriol 176:388–394PubMedCentralPubMedGoogle Scholar
  90. 90.
    Wolfgang A, Markus R, Dimitrios A, Christian S (2009) Evidence for low-titre infections in insect symbiosis: Wolbachia in the bark beetle Pityogenes chalcographus (Coleoptera, Scolytinae). Environ Microbiol 11:1923–1933. doi:10.1111/j.1462-2920.2009.01914.x PubMedCrossRefGoogle Scholar
  91. 91.
    Xie J, Butler S, Sanchez G, Mateos M (2014) Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps. Heredity 112:399–408. doi:10.1038/hdy.2013.118 PubMedCentralPubMedCrossRefGoogle Scholar
  92. 92.
    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 wasp-attacked fly survivors. Evol Ecol 53:1065–1079. doi:10.1007/s10682-010-9453-7 PubMedCentralPubMedCrossRefGoogle Scholar
  93. 93.
    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. doi:10.1371/journal.pone.0012149 PubMedCentralPubMedCrossRefGoogle Scholar
  94. 94.
    Zchori-Fein E, Brown JK (2002) Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera : Aleyrodidae). Ann Entomol Soc Am 95:711–718. doi:10.1603/0013-8746(2002)095[0711:DOPAWB]2.0.CO;2 CrossRefGoogle Scholar
  95. 95.
    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. doi:10.1371/journal.pone.0038544 PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Bodil N. Cass
    • 1
  • Rachel Yallouz
    • 2
  • Elizabeth C. Bondy
    • 3
  • Netta Mozes-Daube
    • 2
  • A. Rami Horowitz
    • 4
    • 5
  • Suzanne E. Kelly
    • 3
  • Einat Zchori-Fein
    • 2
  • Martha S. Hunter
    • 3
  1. 1.Graduate Interdisciplinary Program in Entomology and Insect ScienceUniversity of ArizonaTucsonUSA
  2. 2.Department of EntomologyNewe Ya’ar Research CenterRamat YishayIsrael
  3. 3.Department of EntomologyUniversity of ArizonaTucsonUSA
  4. 4.Department of Entomology, AROGilat Research CenterMobile Post NegevIsrael
  5. 5.Department of EntomologyKatif Research CenterSedot NegevIsrael

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