Microbiome diversity of Aphis glycines with extensive superinfection in native and invasive populations

Environmental Microbiology Reports

Volumn 6, Issue 1, 2014, Pages 57-69

  Bansal, Raman ^a   Mian, M A Rouf ^a,b   Michel, Andy P ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; APHID; ARTICLE; BACTERIUM; BIODIVERSITY; CLASSIFICATION; GENETICS; INTRODUCED SPECIES; ISOLATION AND PURIFICATION; JAPAN; MICROBIOLOGY; MICROFLORA; NORTH AMERICA; PHYLOGENY; SOUTH KOREA;

ANIMALS; APHIDS; BACTERIA; BIODIVERSITY; INTRODUCED SPECIES; JAPAN; MICROBIOTA; NORTH AMERICA; PHYLOGENY; REPUBLIC OF KOREA;

EID: 84892664845     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/1758-2229.12108     Document Type: Article

References (112)

1. Acuña, R., Padilla, B.E., Flórez-Ramos, C.P., Rubio, J.D., Herrera, J.C., Benavides, P., etal. (2012) Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc Natl Acad Sci USA 109: 4197-4202.
2. Allen, J.M., Reed, D.L., Perotti, M.A., and Braig, H.R. (2007) Evolutionary relationships of 'Candidatus Riesia spp., ' endosymbiotic Enterobacteriaceae living within hematophagous primate lice. Appl Environ Microbiol 73: 1659-1664.
3. Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.
4. Ateyyat, M. (2008) Culturable bacteria associated with the guts of pea aphid, Acyrthosiphum pisum (Homoptera: Aphididae). J Entomol 5: 167-175.
5. Bai, X., Zhang, W., Orantes, L., Jun, T.-H., Mittapalli, O., Mian, M.A.R., and Michel, A.P. (2010) Combining next-generation sequencing strategies for rapid molecular resource development from an invasive aphid species, Aphis glycines. PLoS ONE 5: e11370.
6. Bansal, R., Hulbert, S., Schemerhorn, B., Reese, J.C., Whitworth, R.J., Stuart, J.J., etal. (2011) Hessian fly-associated bacteria: transmission, essentiality, and composition. PLoS ONE 6: e23170.
7. Bansal, R., Mian, M.R., Mittapalli, O., and Michel, A.P. (2012a) Characterization of a chitin synthase encoding gene and effect of diflubenzuron in soybean aphid, Aphis glycines. Int J Biol Sci 8: 1323-1334.
8. Bansal, R., Mamidala, P., Mian, M.R., Mittapalli, O., and Michel, A.P. (2012b) Validation of reference genes for gene expression studies in Aphis glycines (Hemiptera: Aphididae). J Econ Entomol 105: 1432-1438.
9. Bansal, R., Jun, T., Mian, M., and Michel, A.P. (2013a) Developing host-plant resistance for hemipteran soybean pests: lessons from soybean aphid and stink bugs. In Soybean-Pest Resistance. El-Shemy, H. (ed.). Rijeka, Croatia: InTech, pp. 19-46. ISBN: 978-953-51-0978-5, doi: 10.5772/54597.
10. Bansal, R., Mian, M., and Michel, A.P. (2013b) Identification of novel sources of host plant resistance to known soybean aphid biotypes. J Econ Entomol 106: 1479-1485.
11. Bansal, R., Mian, M., Mittapalli, O., and Michel, A.P. (2013c) Molecular characterization and expression analysis of soluble trehalase gene in Aphis glycines, a migratory pest of soybean. Bull Entomol Res 103: 286-295.
12. Bartosch, S., Fite, A., Macfarlane, G.T., and McMurdo, M.E. (2004) Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol 70: 3575-3581.
13. Baumann, P., Baumann, L., Lai, C.Y., Rouhbakhsh, D., Moran, N.A., and Clark, M.A. (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu Rev Microbiol 49: 55-94.
14. Behar, A., Jurkevitch, E., and Yuval, B. (2008) Bringing back the fruit into fruit fly-bacteria interactions. Mol Ecol 17: 1375-1386.
15. Belda, E., Pedrola, L., Peretó, J., Martínez-Blanch, J.F., Montagud, A., etal. (2011) Microbial diversity in the midguts of field and lab-reared populations of the European Corn Borer Ostrinia nubilalis. PLoS ONE 6: e21751.
16. Blackburn, M.B., Gunderson-Rindal, D.E., Weber, D.C., Martin, P.A.W., and Farrar, R.R.J. (2008) Enteric bacteria of field-collected Colorado potato beetle larvae inhibit growth of the entomopathogens Photorhabdus temperata and Beauveria bassiana. Biol Control 46: 434-441.
17. Cárcer, D.A., Denman, S.E., McSweeney, C., and Morrison, M. (2011) Evaluation of subsampling-based normalization strategies for tagged high-throughput sequencing data sets from gut microbiomes. Appl Environ Microbiol 77: 8795-8798.
18. Chandrasena, D., DiFonzo, C., and Byrne, A. (2011) An aphid-dip bioassay to evaluate susceptibility of soybean aphid (Hemiptera: Aphididae) to pyrethroid, organophosphate, and neonicotinoid insecticides. J Econ Entomol 104: 1357-1363.
19. Chao, A. (1984) Non-parametric estimation of the number of classes in a population. Scand J Stat 11: 265-270.
20. Chao, A.M., Ma, M.C., and Yang, M.C.K. (1993) Stopping rules and estimation for recapture debugging with unequal failure rates. Biometrika 80: 193-201.
21. Chiel, E., Gottlieb, Y., Zchori-Fein, E., Mozes-Daube, N., Katzir, N., Inbar, M., etal. (2007) Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bull Entomol Res 97: 407-413.
22. Chiozza, M.V., O'Neal, M.E., and MacIntosh, G.C. (2010) Constitutive and induced differential accumulation of amino acid in leaves of susceptible and resistant soybean plants in response to the soybean aphid (hemiptera: aphididae). Environ Entomol 39: 856-864.
23. Darby, A.C., and Douglas, A.E. (2003) Elucidation of the transmission patterns of an insect borne bacterium. Appl Environ Microbiol 69: 4403-4407.
24. Davis, J.A., and Radcliffe, E.B. (2008) The importance of an invasive aphid species in vectoring a persistently transmitted potato virus: Aphis glycines is a vector of Potato leafroll virus. Plant Dis 92: 1515-1523.
25. De Vries, E.J., Van der Wurff, A.W.G., Jacobs, G., and Breeuwer, J.A.J. (2008) Onion thrips, Thrips tabaci, have gut bacteria that are closely related to the symbionts of the western flower thrips, Frankliniella occidentalis. J Insect Sci 8: 1-11.
26. Dergousoff, S.J., and Chilton, N.B. (2010) Detection of a new Arsenophonus-type bacterium in Canadian populations of the Rocky Mountain wood tick. Dermacentor andersoni. Exp Appl Acarol 52: 85-91.
27. Dillon, R.J., and Charnley, A.K. (1995) Chemical barriers to gut infection in the desert locust: In vivo production of antimicrobial phenols associated with the bacterium Pantoea agglomerans. J Inv Path 66: 72-75.
28. Dillon, R.J., Vennard, C.T., Buckling, A., and Charnley, A.K. (2005) Diversity of locust gut bacteria protects against pathogen invasion. Ecol Lett, 8: 1291-1298.
29. Douglas, A.E. (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria. Buchnera Ann Rev Entomol 43: 17-37.
30. Doyle, J.J., and Doyle, J.L. (1987) A rapid DNA isolation procedure from small quantities of fresh leaf tissues. Phytochem Bull 19: 11-15.
31. 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: e96.
32. Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
33. Excoffier, L., Smouse, P.E., and Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479-491.
34. Febvay, G., Liadouze, I., Guillaud, J., and Bonnot, G. (1995) Analysis of energetic amino acid metabolism in Acyrthosiphon pisum: a multidimensional approach to amino acid metabolism in aphids. Arch Insect Biochem Physiol 29: 45-69.
35. Feldhaar, H. (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36: 533-543.
36. Fellous, S., Duron, O., and Rousset, F. (2011) Adaptation due to symbionts and conflicts between heritable agents of biological information. Nat Rev Gen 12: 663.
37. Feng, W., Wang, X.Q., Zhou, W., Liu, G.Y., and Wan, Y.J. (2011) Isolation and characterization of lipase-producing bacteria in the intestine of the silkworm, Bombyx mori, reared on different forage. J Insect Sci 11: 1-10.
38. Ferrari, J., Darby, A.C., Daniell, T.J., Godfray, H.C.J., and Douglas, A.E. (2004) Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol Entomol 29: 60-65.
39. Ferrari, J., West, J.A., Via, S., and Godfray, H.C.J. (2012) Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution 66: 375-390.
40. Frentiu, F.D., Robinson, J., Young, P.R., McGraw, E.A., and O'Neill, S.L. (2010) Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PLoS ONE 5: e13398.
41. Garbeva, P., Van Veen, J.A., and Van Elsas, J.D. (2003) Predominant Bacillus spp. in agricultural soil under different management regimes detected via PCR-DGGE. Microb Ecol 45: 302-316.
42. Gil, R., Latorre, A., and Moya, A. (2004) Bacterial endosymbionts of insects: insights from comparative genomics. Environ Microbiol 6: 1109-1122.
43. Grenier, A.M., Nardon, C., and Rahbé, Y. (1994) Observations on the micro-organisms occurring in the gut of the pea aphid Acyrthosiphon pisum. Entomol Exp Appl 70: 91-96.
44. Hail, D., Lauzìere, I., Dowd, S.E., and Bextine, B.O. (2011) Culture independent survey of the microbiota of the glassy-winged sharpshooter (Homalodisca vitripennis) using 454 pyrosequencing. Environ Entomol 40: 23-29.
45. 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.
46. Heimpel, G.E., Frelich, L.E., Landis, D.A., Hopper, K.R., Hoelmer, K.A., Sezen, Z., etal. (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol Invasions 12: 2913-2931.
47. Heuer, H., and Smalla, K. (1997) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) for studying soil microbial communities. In Modern Soil Microbiology. Van Elsas, J.D., Trevors, J.T., and Wellington, E.M.H. (eds). New York, USA: Marcel Dekker, pp. 353-373.
48. Hill, C.B., Li, Y., and Hartman, G.L. (2004) Resistance to the soybean aphid in soybean germplasm. Crop Sci 44: 98-106.
49. Hill, C.B., Crull, L., Herman, T., Voegtlin, D.J., and Hartman, G.L. (2010) A new soybean aphid (Hemiptera: Aphididae) biotype identified. J Econ Entomol 103: 509-515.
50. Hill, J.H., Alleman, R., Hogg, D.B., and Grau, C.R. (2001) First report of transmission of Soybean mosaic virus and Alfalfa mosaic virus by Aphis glycines in the New World. Plant Dis 85: 561.
51. Hill, C.B., Chirumamilla, A., and Hartman, G.L. (2012). Resistance and virulence in the soybean-Aphis glycines interaction. Euphytica 186: 635-646.
52. 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 an invasive whitefly is driven by fitness benefits and female bias. Science 332: 254-256.
53. Hirsch, J., Strohmeier, S., Pfannkuchen, M., and Reineke, A. (2012) Assessment of bacterial endosymbiont diversity in Otiorhynchus spp. (Coleoptera: Curculionidae) larvae using a multitag 454 pyrosequencing approach. BMC Microbiol 12 (Suppl. 1): S6.
54. Hodgson, E.W., McCornack, B.P., Tilmon, K., and Knodel, J.J. (2012) Management recommendations for soybean aphid (Hemiptera: Aphididae) in the United States. J Integ Pest Manage 3: E1-E10.
55. Hosokawa, T., Kikuchi, Y., Shimada, M., and Fukatsu, T. (2007) Obligate symbiont involved in pest status of host insect. Proc R Soc Lond B 274: 1979-1984.
56. Hosokawa, T., Koga, R., Kikuchi, Y., Meng, X.Y., and Fukatsu, T. (2010) Wolbachia as a bacteriocyte associated nutritional mutualist. Proc Natl Acad Sci USA 107: 769-774.
57. Huse, S.M., Welch, D.M., Morrison, H.G., and Sogin, M.L. (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12: 1889-1898.
58. Jaenike, J., Unckless, R., Cockburn, S.N., Boelio, L.M., and Perlman, S.J. (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329: 212-215.
59. Kim, H., Hoelmer, K.A., Lee, W., Kwon, Y.-D., and Lee, S. (2010) Molecular and morphological identification of the soybean aphid and other aphis species on the primary host Rhamnus davurica in Asia. Ann Entomol Soc Am 103: 532-543.
60. Lane, D.J. (1991) 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics. Stackebrandt, E., and Goodfellow, M. (eds). New York, USA: John Wiley & Sons, Inc., pp. 115-175.
61. Liu, J., Wu, K., Hopper, K.R., and Zhao, K. (2004) Population dynamics of Aphis glycines (Homoptera: Aphididae) and its natural enemies in soybean in northern China. Ann Entomol Soc Am 97: 235-239.
62. Liu, L., Li, L., Liu, J., Hu, Y., Liu, Z., Guo, L., and Liu, J. (2013) Coinfection of Dermacentor silvarum Olenev (Acari: Ixodidae) by Coxiella-like, Arsenophonus-like, and Rickettsia-like symbionts. Appl Environ Microbiol 79: 2450-2454.
63. Liu, S., Chougule, N.P., Vijayendran, D., and Bonning, B.C. (2012) Deep sequencing of the transcriptomes of soybean aphid and associated endosymbionts. PLoS ONE 7: e45161.
64. McCornack, B.P., Ragsdale, D.W., and Venette, R.C. (2004) Demography of soybean aphid (Homoptera: Aphididae) at summer temperatures. J Econ Entomol 97: 854-861.
65. McCutcheon, J.P., and Moran, N.A. (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10: 13-26.
66. Magurran, A.E. (1988) Ecological Diversity and Its Measurement. Princeton, NJ, USA: Princeton University Press.
67. Martin, A.P. (2002) Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl Environ Microbiol 68: 3673-3682.
68. Mian, M.A.R., Hammond, R.B., and Martin, S.K. (2008) New plant introductions with resistance to the soybean aphid. Crop Sci 48: 1055-1061.
69. Michel, A.P., Zhang, W., and Mian, M.A.R. (2010) Genetic diversity and differentiation among laboratory and field populations of the soybean aphid, Aphis glycines. Bull Entomol Res 100: 727-734.
70. Michel, A.P., Mittapalli, O., and Mian, M.A.R. (2011) Evolution of soybean aphid biotypes: understanding and managing virulence to host-plant resistance. In Soybean: Molecular Aspects of Breeding. Sudaric, A. (ed.). Vienna, Austria: InTech Publishing, pp. 355-372.
71. Moran, N.A. (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci USA 104: 8627-8633.
72. Moran, N.A., Munson, M.A., Baumann, P., and Ishikawa, H. (1993) A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc R Soc Lond B Biol Sci 253: 167-171.
73. Moran, N.A., McCutcheon, J.P., and Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165-190.
74. Muyzer, G., De Waal, E.C., and Uitterlinden, A.G. (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700.
75. Nachappa, P., Levy, J., Pierson, E., and Tamborindeguy, C. (2011) Diversity of endosymbionts in the potato psyllid, Bactericera cockerelli (Triozidae), vector of zebra chip disease of potato. Curr Microbiol 62: 1510-1520.
76. Ohnesorg, W.J., Johnson, K.D., and O'neal, M.E. (2009) Impact of reduced-risk insecticides on soybean aphid and associated natural enemies. J Econ Entomol 102: 1816-1826.
77. Oliver, K.M., Moran, N.A., and Hunter, M.S. (2006) Costs and benefits of a superinfection of facultative symbionts in aphids. Proc R Soc B Biol Sci 273: 1273-1280.
78. Oliver, K.M., Campos, J., Moran, N.A., and Hunter, M.S. (2008) Population dynamics of defensive symbionts in aphids. Proc R Soc B 275: 293-299.
79. Oliver, K.M., Degnan, P.H., Burke, G.R., and Moran, N.A. (2010) Facultative symbionts of aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55: 247-266.
80. Palavesam, A., Guerrero, F.D., Heekin, A.M., Wang, J., Dowd, S.E., Sun, Y., etal. (2012) Pyrosequencing-based analysis of the microbiome associated with the horn fly, Haematobia irritans. PLoS ONE 7: e44390.
81. Perotti, M.A., Allen, J.M., Reed, D.L., and Braig, H.R. (2007) Host-symbiont interactions of the primary endosymbiont of human head and body lice. FASEB J 21: 1058-1066.
82. Pruesse, E., Quast, C., Knittel, K., Fuchs, B., Ludwig, W., Peplies, J., and Glöckner, F.O. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
83. Ragsdale, D.W., Voegtlin, D.J., and O'Neil, R.J. (2004) Soybean aphid biology in North America. Ann Entomol Soc Am 97: 204-208.
84. Ragsdale, D.W., Landis, D.A., Brodeur, J., Heimpel, G.E., and Desneux, N. (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56: 375-399.
85. Rani, A., Sharma, A., Rajagopal, R., Adak, T., and Bhatnagar, R.K. (2009) Bacterial diversity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi-an Asian malarial vector. BMC Microbiol 9: 96.
86. Rochelle, P.A., Will, J.A.K., Fry, J.C., Jenkins, G.J.S., Parkers, R.J., Turley, C.M., and Weightman, A.J. (1995) Extraction and amplification of 16S rRNA genes from deep marine sediments and seawater to assess bacterial community diversity. In Nucleic Acids in the Environment. Trevors, J.T., and Elsas, J.D. (eds). Berlin, Germany: Springer-Verlag, pp. 219-239.
87. Russell, J.A., Weldon, S., Smith, A.H., Kim, K.L., Hu, Y., Lukasik, P., etal. (2013) Uncovering symbiont-driven genetic diversity across North American pea aphids. Mol Ecol 22: 2045-2059.
88. Rutledge, C.E., O'Neil, R.J., Fox, T.B., and Landis, D.A. (2004) Soybean aphid predators and their use in integrated pest management. Ann Entomol Soc Am 97: 240-248.
89. Sandström, J., and Moran, N.A. (1999) How nutritionally imbalanced is phloem sap for aphids? Entomol Exp Appl 91: 203-210.
90. Sandström, J., and Moran, N.A. (2001) Amino acid budgets in three aphid species using the same host plant. Physiol Entomol 26: 202-211.
91. Sandström, J., and Pettersson, J. (1994) Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. J Insect Physiol 40: 947-955.
92. 15N-labeled glutamine. Zool Sci 19: 787-791.
93. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., etal. (2009) Introducing mothur: Open source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
94. Shigenobu, S., Watanabe, H., Hattori, M., Sasaki, Y., and Ishikawa, H. (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407: 81-86.
95. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
96. Teixeira, L., Ferreira, Á., and Ashburner, M. (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6: e1000002.
97. The International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 8: e1000313.
98. Trowbridge, R.E., Dittmar, K., and Whiting, M.F. (2006) Identification and phylogenetic analysis of Arsenophonus- and Photorhabdus-type bacteria from adult Hippoboscidae and Streblidae (Hippoboscoidea). J Invertebr Pathol 91: 64-68.
99. Tsuchida, T., Koga, R., Shibao, H., Matsumoto, T., and Fukatsu, T. (2002) Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol Ecol 11: 2123-2135.
100. Tsuchida, T., Koga, R., and Fukatsu, T. (2004) Host plant specialization governed by facultative symbiont. Science 303: 1989-1989.
101. Tsuchida, T., Koga, R., and Fukatsu, T. (2009) Endosymbiont that broadens food plant range of host insect. In Insect Symbiosis, Vol. 3. Bourtzis, K., and Miller, T. (eds). Boca Raton, FL, USA: CRC Press, pp. 123-141.
102. 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.
103. Venette, R.C., and Ragsdale, D.W. (2004) Assessing the invasion by soybean aphid (Homoptera: Aphididae): where will it end? Ann Entomol Soc Am 97: 219-226.
104. Weeks, A.R., Turelli, M., Harcombe, W.R., Reynolds, K.T., and Hoffmann, A.A. (2007) From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5: e114.
105. Werren, J.H., and Windsor, D.M. (2000) Wolbachia infection frequency in insects: evidence of a global equilibrium? Proc R Soc Lond B Biol Sci 267: 1277-1285.
106. Werren, J.H., Baldo, L., and Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741-751.
107. White, J.R., Nagarajan, N., and Pop, M. (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5: e1000352.
108. Wille, B., and Hartman, G.L. (2009) Two species of symbiotic bacteria present in the soybean aphid (Hemiptera: Aphididae). Environ Entomol 38: 110-115.
109. Wilson, A.C., Ashton, P.D., Calevro, F., 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.
110. Wilson, K.H., Blitchington, R.B., and Greene, R.C. (1990) Amplification of bacterial-16S ribosomal DNA with polymerase chain-reaction. J Clin Microbiol 28: 1942-1946.
111. Wulff, J.A., Buckman, K.A., Wu, K., Heimpel, G.E., and White, J.A. (2013) The endosymbiont Arsenophonus is widespread in soybean aphid, Aphis glycines, but does not provide protection from parasitoids or a fungal pathogen. PLoS ONE 8: e62145.
112. Xiang, H., Wei, G.-F., Jia, S., Huang, J., Miao, X.-X., etal. (2006) Microbial communities in the larval midgut of laboratory and field populations of cotton bollworm (Helicoverpa armigera). Can J Microbiol 52: 1085-1092.