Diversity of proteobacterial endosymbionts in hemlock woolly adelgid (Adelges tsugae) (Hemiptera: Adelgidae) from its native and introduced range

Environmental Microbiology

Volumn 15, Issue 7, 2013, Pages 2043-2062

  von Dohlen, Carol D ^a   Spaulding, Usha ^a,d   Shields, Kathleen ^b,e   Havill, Nathan P ^b   Rosa, Cristina ^c   Hoover, Kelli ^c  

^a UTAH STATE UNIVERSITY   (United States)

^b USDA FOREST SERVICE   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d Idaho Technology Inc   (United States)

^e NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADELGES TSUGAE; ADELGIDAE; BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; BUCHNERA APHIDICOLA; CANDIDATUS SERRATIA SYMBIOTICA; CONIUM; GAMMAPROTEOBACTERIA; HEMIPTERA; HEXAPODA; PROTEOBACTERIA; PSEUDOMONAS; SERRATIA; TSUGA; TSUGA SIEBOLDII;

EID: 84880035611     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12102     Document Type: Article

References (106)

1. Aksoy, S., and Rio, R.V.M. (2005) Interactions among multiple genomes: tsetse, its symbionts and trypanosomes. Insect Biochem Mol Biol 35: 691-698.
2. Ammar, E., and Hogenhout, S.A. (2005) Use of immunofluorescence confocal laser scanning microscopy to study distribution of the bacterium corn stunt spiroplasma in vector leafhoppers (Hemiptera : Cicadellidae) and in host plants. Ann Entomol Soc Am 98: 820-826.
3. Annand, P.N. (1924) A new species of Adelges (Hemiptera, Phylloxeridae). Pan-Pac Entomol 1: 79-82.
4. Annand, P.N. (1928) A Contribution toward A Monograph of the Adelginae (Phylloxeridae) of North America. Palo Alto, CA, USA: Stanford Univ. Press.
5. Ausubel, F.A., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (eds) (1996) Current Protocols in Molecular Biology. New York, USA: John Wiley and Sons.
6. Baumann, P. (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59: 155-189.
7. Baumann, P. (2006) Diversity of prokaryote-insect associations within the Sternorrhyncha (psyllids, whiteflies, aphids, mealybugs. In Insect Symbiosis. Bourtzis, K., and Miller, T.A. (eds). Boca Raton, FL, USA: CRC Press, pp. 1-24.
8. Buchner, P. (1965) Endosymbiosis of Animals with Plant Microorganisms. New York, USA: John Wiley and Sons.
9. Burke, G.R., Normark, B.B., Favret, C., and Moran, N.A. (2009) Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae. Appl Environ Microbiol 75: 5328-5335.
10. Chen, W.J., Tsai, K.H., Cheng, S.L., Huang, C.G., and Wu, W.J. (2005) Using in situ hybridization to detect endosymbiont Wolbachia in dissected tissues of mosquito host. J Med Entomol 42: 120-124.
11. Cheng, Q., and Aksoy, S. (1999) Tissue tropism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol Biol 8: 125-132.
12. Clark, M.A., Moran, N.A., Baumann, P., and Wernegreen, J.J. (2000) Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54: 517-525.
13. Costa, S. (2010) Hemlock woolly adelgid suppression with aerial application of mycotal fungus in a microfactory formulation: can it work? In Fifth Symposium on Hemlock Woolly Adelgid in the Eastern United States. Onken, B., and Reardon, R. (eds). Asheville, NC, USA: USDA Forest Service FHTET-2010-07, p. 32.
14. Dion, E., Polin, S.E., Simon, J.-C., and Outreman, Y. (2011) Symbiont infection affects aphid defensive behaviours. Biol Lett 7: 743-746.
15. Dixon, R.A., Harrison, M.J., and Lamb, C.J. (1994) Early events in the activation of plant defense responses. Annu Rev Phytopathol 32: 479-501.
16. von Dohlen, C.D., Kohler, S., Alsop, S.T., and McManus, W.R. (2001) Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature 412: 433-436.
17. Douglas, A.E., Minto, L.B., and Wilkinson, T.L. (2001) Quantifying nutrient production by the microbial symbionts in an aphid. J Exp Biol 204: 349-358.
18. Dunbar, H.E., Wilson, A.C.C., Ferguson, N.R., and Moran, N.A. (2007) Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol 5: 1006-1015.
19. Fletcher, J., Wayadande, A., Melcher, U., and Ye, F.C. (1998) The phytopathogenic mollicute-insect vector interface: a closer look. Phytopathology 88: 1351-1358.
20. Foottit, R.G., Maw, H.E.L., Havill, N., Ahern, R.G., and Montgomery, M.E. (2009) DNA barcodes to identify species and explore diversity in the Adelgidae (Insecta: Hemiptera: Aphidoidea). Mol Ecol Resour 9: 188-195.
21. Fuchs, B.M., Wallner, G., Beisker, W., Schwippl, I., Ludwig, W., and Amann, R. (1998) Flow cytometric analysis of the in situ accessibility of Escherichia coli 16S rRNA for fluorescently labeled oligonucleotide probes. Appl Environ Microbiol 64: 4973-4982.
22. Fukatsu, T., Watanabe, K., and Sekiguchi, Y. (1998) Specific detection of intracellular symbiotic bacteria of aphids by oligonucleotide-probed in situ hybridization. Appl Entomol Zool 33: 461-472.
23. Gehrer, L., and Vorburger, C. (2012) Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Lett 8: 613-615.
24. Gómez, S., Orians, C., and Preisser, E. (2012) Exotic herbivores on a shared native host: tissue quality after individual, simultaneous, and sequential attack. Oecologia 169: 1015-1024.
25. Gomez-Valero, L., Soriano-Navarro, M., Perez-Brocal, V., Heddi, A., Moya, A., Garcia-Verdugo, J.M., and Latorre, A. (2004) Coexistence of Wolbachia with Buchnera aphidicola and a secondary symbiont in the aphid Cinara cedri. J Bacteriol 186: 6626-6633.
26. Gonda-King, L., Radville, L., and Preisser, E.L. (2012) False ring formation in eastern hemlock branches: impacts of hemlock woolly adelgid and elongate hemlock scale. Environ Entomol 41: 523-531.
27. Grant, J.F., Hakeem, A., Wiggins, G., Rhea, R., and Lambdin, P.L. (2010) Assessment of introduced predator species against hemlock woolly adelgid on eastern hemlock using whole-tree canopy enclosures. In Fifth Symposium on Hemlock Woolly Adelgid in the Eastern United States. Onken, B., and Reardon, R. (eds). Asheville, NC, USA: USDA Forest Service FHTET-2010-07, pp. 53-55.
28. Grimaldi, D., and Engel, M.S. (2005) Evolution of the Insects. Cambridge, UK: Cambridge University Press.
29. Gruwell, M.E., Morse, G.E., and Normark, B.B. (2007) Phylogenetic congruence of armored scale insects (Hemiptera: Diaspididae) and their primary endosymbionts from the phylum Bacteroidetes. Mol Phylogenet Evol 44: 267-280.
30. Hansen, A.K., and Moran, N.A. (2011) Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc Natl Acad Sci USA 108: 2849-2854.
31. Hansen, A.K., Jeong, G., Paine, T.D., and Stouthamer, R. (2007) Frequency of secondary symbiont infection in an invasive psyllid relates to parasitism pressure on a geographic scale in California. Appl Environ Microbiol 73: 7531-7535.
32. Haracsi, L. (1938) Beiträge zur Biologie der Blattläuse. Nat For Exper 1-4: 47-53.
33. Havill, N.P., and Foottit, R.G. (2007) Biology and evolution of Adelgidae. Annu Rev Entomol 52: 325-349.
34. Havill, N.P., Montgomery, M.E., Yu, G.Y., Shiyake, S., and Caccone, A. (2006) Mitochondrial DNA from hemlock woolly adelgid (Hemiptera : Adelgidae) suggests cryptic speciation and pinpoints the source of the introduction to eastern North America. Ann Entomol Soc Am 99: 195-203.
35. Heie, O.E. (1987) Paleontology and phylogeny. In Aphids Their Biology, Natural Enemies and Control. Minks, A.K., and Harrewijn, P. (eds). Amsterdam, the Netherlands: Elsevier, pp. 367-391.
36. Heie, O.E., and Pike, E.M. (1996) Reassessment of the taxonomic position of the fossil aphid family Canadaphididae based on two additional specimens of Canadaphis carpenteri (Hemiptera: Aphidinea). Eur J Entomol 93: 617-622.
37. van den Heuvel, J.F.J., Verbeek, M., and van der Wilk, F. (1994) Endosymbiotic bacteria associated with circulative transmission of potato leafroll virus by Myzus persicae. J Gen Virol 75: 2559-2565.
38. Himler, A.G., Adachi-Hagimori, T., Bergen, J.E., Kozuch, A., Kelly, S.E., Tabashnik, B.E., etal. (2011) Rapid Spread of a bacterial symbiont in aninvasive whitefly Is driven by fitness benefits and female bias. Science 332: 254-256.
39. Hogenhout, S.A., Oshima, K., Ammar el, D., Kakizawa, S., Kingdom, H.N., and Namba, S. (2008) Phytoplasmas: bacteria that manipulate plants and insects. Mol Plant Pathol 9: 403-423.
40. Hosokawa, T., Kikuchi, Y., Nikoh, N., Shimada, M., and Fukatsu, T. (2006) Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol 4: e337.
41. Hosokawa, T., Kikuchi, Y., Shimada, M., and Fukatsu, T. (2007) Obligate symbiont involved in pest status of host insect. Proc R Soc Lond B Biol Sci 274: 1979-1984.
42. Joseph, S.V., Hanula, J.L., Braman, S.K., and Byrne, F.J. (2011) Effects of fertilizer and low rates of imidacloprid on Adelges tsugae (Hemiptera: Adelgidae). J Econ Entomol 104: 868-878.
43. Kellner, R.L.L. (2002) Interspecific transmission of Paederus endosymbionts: relationship to the genetic divergence among the bacteria associated with pederin biosynthesis. Chemoecology 12: 133-138.
44. Kikuchi, Y., Meng, X.Y., and Fukatsu, T. (2005) Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera : Alydidae). Appl Environ Microbiol 71: 4035-4043.
45. Kikuchi, Y., Hosokawa, T., and 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.
46. Kikuchi, Y., Hosokawa, T., and Fukatsu, T. (2011) An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J 5: 446-460.
47. Kikuchi, Y., Hayatsu, M., Hosokawa, T., Nagayama, A., Tago, K., and Fukatsu, T. (2012) Symbiont-mediated insecticide resistance. Proc Natl Acad Sci USA 109: 8618-8622.
48. Komminoth, P. (1996) Detection of mRNA in tissue sections using DIG-labeled RNA and oligonucleotide probes. In Nonradioactive in situ Hybridization Application Manual. Grünewald-Janho, S., Keesey, J., Leous, M., van Miltenburg, R., and Schroeder, C. (eds). Mannheim, Germany: Boehringer Mannheim GmbH, Biochemica, pp. 126-135.
49. Kwon, M.O., Wayadande, A.C., and Fletcher, J. (1999) Spiroplasma citri movement into the intestines and salivary glands of its leafhopper vector, Circulifer tenellus. Phytopathology 89: 1144-1151.
50. Lambert, J.D., and Moran, N.A. (1998) Deleterious mutations destabilize ribosomal RNA in endosymbiotic bacteria. Proc Natl Acad Sci USA 95: 4458-4462.
51. Lamelas, A., Perez-Brocal, V., Gomez-Valero, L., Gosalbes, M.J., Moya, A., and Latorre, A. (2008) Evolution of the secondary symbiont 'Candidatus Serratia symbiotica' in aphid species of the subfamily Lachninae. Appl Environ Microbiol 74: 4236-4240.
52. Lamelas, A., Gosalbes, M.J., Manzano-Marin, A., Pereto, J., Moya, A., and Latorre, A. (2011) Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont. PLoS Genet 7: e1002357.
53. McClure, M.S., and Cheah, C.A.S. (1999) Reshaping the ecology of invading populations of hemlock woolly adelgid, Adelges tsugae (Homoptera: Adelgidae), in eastern North America. Biol Invasions 1: 247-254.
54. McCutcheon, J.P., and von Dohlen, C.D. (2011) An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol 21: 1366-1372.
55. McCutcheon, J.P., and Moran, N.A. (2010) Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol 2: 708-718.
56. Marzorati, M., Alma, A., Sacchi, L., Pajoro, M., Palermo, S., Brusetti, L., etal. (2006) A novel Bacteroidetes symbiont is localized in Scaphoideus titanus, the insect vector of flavescence dorée in Vitis vinifera. Appl Environ Microbiol 72: 1467-1475.
57. Medina, R.F., Nachappa, P., and Tamborindeguy, C. (2011) Differences in bacterial diversity of host-associated populations of Phylloxera notabilis Pergande (Hemiptera: Phylloxeridae) in pecan and water hickory. J Evol Biol 24: 761-771.
58. Mitsuhashi, W., Saiki, T., Wei, W., Kawakita, H., and Sato, M. (2002) Two novel strains of Wolbachia coexisting in both species of mulberry leafhoppers. Insect Mol Biol 11: 577-584.
59. Montllor, C.B., Maxmen, A., and Purcell, A.H. (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27: 189-195.
60. Moran, N.A. (1996) Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci USA 93: 2873-2878.
61. Moran, N.A. (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci USA 104: 8627-8633.
62. Moran, N.A., and Degnan, P.H. (2006) Functional genomics of Buchnera and the ecology of aphid hosts. Mol Ecol 15: 1251-1261.
63. Moran, N.A., Tran, P., and Gerardo, N.M. (2005) Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl Environ Microbiol 71: 8802-8810.
64. Moran, N.A., McCutcheon, J.P., and Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165-190.
65. Morin, S., Ghanim, M., Zeidan, M., Czosnek, H., Verbeek, M., and van den Heuvel, J. (1999) A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaci is implicated in the circulative transmission of tomato yellow leaf curl virus. Virology 256: 75-84.
66. Munson, M.A., Baumann, P., Clark, M.A., Baumann, L., Moran, N.A., Voegtlin, D.J., and Campbell, B.C. (1991) Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol 173: 6321-6324.
67. Murray, R.G., and Stackebrandt, E. (1995) Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol 45: 186-187.
68. Nylander, J.A.A. (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
69. Oliver, K.M., Moran, N.A., and Hunter, M.S. (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102: 12795-12800.
70. Oliver, K.M., Degnan, P.H., Burke, G.R., and Moran, N.A. (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55: 247-266.
71. Olsen, R.T., and Bentz, S.E. (2010) Breeding novel hemlock hybrids with resistance to hemlock woolly adelgid. In Fifth Symposium on Hemlock Woolly Adelgid in the Eastern United States. Onken, B., and Reardon, R. (eds). Asheville, NC, USA: USDA Forest Service FHTET-2010-07, pp. 91-92.
72. Orwig, D.A. (2008) Ecological and management implications of hemlock logging in Massachusetts. In Fourth Symposium on Hemlock Woolly Adelgid in the Eastern United States. Onken, B., and Reardon, R. (eds). Hartford, CT, USA: USDA Forest Service FHTET-2008-01, pp. 112-113.
73. Piel, J., Hofer, I., and Hui, D.Q. (2004) Evidence for a symbiosis island involved in horizontal acquisition of pederin biosynthetic capabilities by the bacterial symbiont of Paederus fuscipes beetles. J Bacteriol 186: 1280-1286.
74. Profft, J. (1937) Beiträge zur Symbiose der Aphiden und Psylliden. Z Morphol Oekol Tiere 32: 289-326.
75. Radville, L., Chaves, A., and Preisser, E. (2011) Variation in plant defense against invasive herbivores: evidence for a hypersensitive response in eastern hemlocks (Tsuga canadensis). J Chem Ecol 37: 592-597.
76. Rambaut, A., and Drummond, A.J. (2009) Tracer v1.5, [WWW document]. URL http://beast.bio.ed.ac.uk/Tracer.
77. Ronquist, F., and Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
78. Ross, D.W., Grubin, S.M., Kohler, G.R., and Wallin, K.F. (2010) Evaluation of Leucopis species (Diptera: Chamaemyiidae) from the PNW as potential biological controls for the hemlock woolly adelgid. In Fifth Symposium on Hemlock Woolly Adelgid in the Eastern United States. Onken, B., and Reardon, R. (eds). Asheville, NC, USA: USDA Forest Service FHTET-2010-07, p. 32.
79. Russell, J.A., and Moran, N.A. (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc R Soc Lond B Biol Sci 273: 603-610.
80. Sauer, C., Stackebrandt, E., Gadau, J., Holldobler, B., and Gross, R. (2000) Systematic relationships and cospeciation of bacterial endosymbionts and their carpenter ant host species: proposal of the new taxon Candidatus Blochmannia gen. nov. Int J Syst Evol Microbiol 50: 1877-1886.
81. Scarborough, C.L., Ferrari, J., and Godfray, H.C.J. (2005) Aphid protected from pathogen by endosymbiont. Science 310: 1781.
82. Shields, K.S., and Hirth, R.T. (2005) Bacterial endosymbionts of Adelges tsugae Annand: Potential targets for biocontrol? Third Symposium on Hemlock Woolly Adelgid in the Eastern United States. Onken, B., and Reardon, R. (eds). Asheville, NC, USA: USDA Forest Service, FHTET-2005-01, pp. 357-359.
83. Souto, D., Luther, T., and Chianese, B. (1996) Past and current status of HWA in eastern and Carolina hemlock stands. In Proceedings of the First Hemlock Woolly Adelgid Review. Salom, S.M., Tignor, T.C., and Reardon, R.C. (eds). Morgantown, WV, USA: USDA Forest Service, pp. 9-15.
84. Spaulding, A.W., and von Dohlen, C.D. (2001) Psyllid endosymbionts exhibit patterns of co-speciation with hosts and destabilizing substitutions in ribosomal RNA. Insect Mol Biol 10: 57-67.
85. Spaulding, H., and Rieske, L. (2010) The aftermath of an invasion: structure and composition of Central Appalachian hemlock forests following establishment of the hemlock woolly adelgid, Adelges tsugae. Biol Invasions 12: 3135-3143.
86. Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
87. Stamatakis, A., Hoover, P., and Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57: 758-771.
88. Steffan, A.W. (1968) Evolution und Systematik der Adelgidae (Homoptera: Aphidina): eine Verwandtschaftsanalyse auf vorwiegend ethologischer zytologischer und karyologischer Grundlage. Zoologica 115: 1-139.
89. Stenger, D.C., Sisterson, M.S., and French, R. (2010) Population genetics of Homalodisca vitripennis reovirus validates timing and limited introduction to California of its invasive insect host, the glassy-winged sharpshooter. Virology 407: 53-59.
90. Sunnucks, P., and Hales, D.F. (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13: 510-524.
91. Swofford, D. (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4.0 b 10.
92. Tamas, I., Klasson, L., Canback, B., Naslund, A.K., Eriksson, A.S., Wernegreen, J.J., etal. (2002) 50 million years of genomic stasis in endosymbiotic bacteria. Science 296: 2376-2379.
93. Thao, M.L., Moran, N.A., Abbot, P., Brennan, E.B., Burckhardt, D.H., and Baumann, P. (2000) Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl Environ Microbiol 66: 2898-2905.
94. Thomopoulos, G.N., Neophytou, E.P., and Limberithomopoulos, S. (1991) Rickettsiae-like structures in the larval salivary-gland cells of Drosophila auraria. J Morphol 207: 17-21.
95. Toenshoff, E.R., Gruber, D., and Horn, M. (2012a) Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts. Environ Microbiol 14: 1284-1295.
96. Toenshoff, E.R., Penz, T., Narzt, T., Collingro, A., Schmitz-Esser, S., Pfeiffer, S., etal. (2012b) Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae). ISME J 6: 384-396.
97. Toh, H., Weiss, B.L., Perkin, S.A.H., Yamashita, A., Oshima, K., Hattori, M., and Aksoy, S. (2006) Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res 16: 149-156.
98. Tsuchida, T., Koga, R., and Fukatsu, T. (2004) Host plant specialization governed by facultative symbiont. Science 303: 1989-1989.
99. Tsuchida, T., Koga, R., Sakurai, M., and Fukatsu, T. (2006) Facultative bacterial endosymbionts of three aphid species, Aphis craccivora, Megoura crassicauda and Acyrthosiphon pisum, sympatrically found on the same host plants. Appl Entomol Zool (Jpn) 41: 129-137.
100. Tsuchida, T., Koga, R., Matsumoto, S., and Fukatsu, T. (2011) Interspecific symbiont transfection confers a novel ecological trait to the recipient insect. Biol Lett 7: 245-248.
101. Vorwerk, S., Martinez-Torres, D., and Forneck, A. (2007) Pantoea agglomerans-associated bacteria in grape phylloxera (Daktulosphaira vitifoliae, Fitch). Agric For Entomol 9: 57-64.
102. Wernegreen, J.J. (2002) Genome evolution in bacterial endosymbionts of insects. Nat Rev Genet 3: 850-861.
103. Wilson, A.C.C., Ashton, P.D., Calevro, F., Charles, H., Colella, S., Febvay, G., etal. (2010) Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol Biol 19: 249-258.
104. Young, R.F., Shields, K.S., and Berlyn, G.P. (1995) Hemlock woolly adelgid (Homoptera: Adelgidae): stylet bundle insertion and feeding sites. Ann Entomol Soc Am 88: 827-835.
105. Zarda, B.A., and Schleifer, K. (1996) Identification of single cells using DIG-labeled oligonucleotides. In Nonradioactive in situ Hybridization Application Manual. Mannheim, Germany: Boehringer Mannheim GmbH, Biochemica, pp. 119-121.
106. Zwickl, D.J. (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD Dissertation. Austin, TX, USA: The University of Texas at Austin.