The impacts of endosymbiotic bacteria on insects

Abstract

Symbiotic bacteria are ubiquitous in insect hosts. The host-symbiont interactions vary from obligate to facultative associations depending on their coevoluationary histories. These microbial fauna have a broad array of effects on their hosts. In the case of insects that typically live on limited nutrients, one common role of their obligate endosymbionts (referred to as Primary symbionts) is to supply essential nutrients to their hosts. Among the nutrients provided by symbionts are essential amino acids, vitamins and other potentially beneficial compounds that restricted host diets typically lack. Beyond nutrient provisioning, symbionts have been implicated in the detoxification of dietary compounds and insecticides as well. In a number of insect systems, facultative associations (referred to as Secondary symbionts) contribute to resistance toward natural enemies, provide tolerance to heat shock or impact host transmission of viruses. The parasitic bacterium, Wolbachia, which are widely prevalent in diverse insect taxa, influence host reproductive biology and have an impact on host population dynamics via mechanisms such as cytoplasmic incompatibility (CI), parthenogenesis induction (PI), feminization and male killing. Here we review the current knowledge on the interactions between symbionts and their insects hosts and introduce the symbiont-based approaches that are being investigated to control insect pests.

Keywords

• Plant, insects, endosymbiotic bacteria, symbiosis, pest management

Endosimbiyotik bakterilerin böcekler üzerine etkisi

Abstract

Böceklerde oldukça yaygın olan simbiyotik bakteriler konukçularında çok değişik etkiler göstermektedir. Evrimsel sürece bağlı olarak konukçu simbiyont ilişkileri obligat ya da fakültatif olabilmektedir. Obligat olan primer simbiyontlar bitki özsuyunda bulunmayan temel aminoasitleri, vitaminleri ve faydalı pek çok bileşiği konukçusu olan böceklere sağlamaktadır. Besin sağlamalarının yanı sıra simbiyontların beslenmeyle ilgili bileşiklerin hatta insektisitlerin detoksifikasyonundan sorumlu olduğu gösterilmiştir. Bazı böceklerde doğal düşmanlara karşı gösterilen farklı savunma reaksiyonları fakültatif olan sekonder simbiyontlar ile ilişkilendirilirken bazı simbiyontların sıcaklığa karşı tolerans gösterdiği bilinmektedir. Ayrıca bazı endosimbiyontlar vektör böceklerin virüs taşıma yeteneklerini de etkileyebilmektedir. Öte yandan, böcek takımlarında yaygın olarak bulunan Wolbachia gibi parazitik bakteriler; sitoplazmik uyuşmazlık (CI), partenogenezisin teşvik edilmesi (PI), dişileşme (feminizasyon) ve erkek ölümü gibi mekanizmalarla konukçularının populasyon dinamiklerini etkilerler. Bu derlemede simbiyont konukçu ilişkisi hakkında bilinenler irdelenerek, simbiyontların zararlı mücadelesinde kullanım olanakları tartışılmıştır.

Keywords

• Bitki, böcek, endosimbiyotik bakteriler, simbiyozis, zararlı mücadelesi

References

1. Alam, U., J. Medlock, C. Brelsford, R. Pais, C. Lohs, S. Balmand, J. Carnogursky, A. Heddi, P. Takac, A. Galvani & S. Aksoy, 2011. Wolbachia symbiont infections induce strong cytoplasmic incompatibility in the tsetse fly, Glossina morsitans morsitans. PLoS Pathogens 7, e1002415.
2. Akman Gündüz, E. & A. E. Douglas, 2009. Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc R Soc B, 276: 987-991.
3. Akman, L., A. Yamashita, H. Watanabe, K. Oshima, T. Shiba, M. Hattori & S. Aksoy, 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat Genet, 32: 402-407.
4. Andersen, P. C., B. V. Brodbeck & R. F. Mizell, 1989. Metabolism of amino acids, organic acids and sugars extracted from the xylem fluid of four host plants by adult Homalodisca coagulata. Entomol Exp Appl, 50: 149-159.
5. Bandi, C., M. Sironi, G. Damiani, L. Magrassi, C. A. Nalepa, U. Laudani, & L. Sacchi, 1995. The establishment of intracellular symbiosis in an ancestor of cockroaches and termites. Proc R Soc Lond, 259: 293-299.
6. Bandi, C., A. Dunn, G. Hurst & T. Rigaud, 2001. Inherited microorganisms, sex-specific virulence and reproductive parasitism. Trends Parasitol, 17: 88-94.
7. Bakri, A., K. Mehta & D. Lance, 2005. Sterilizing insects with ionizing radiation, pp. 233-268 In V. A. Dyck, J. Hendrichs, and A. S. Robinson [eds.], Sterile Insect Technique, Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht.
8. Baumann, L. & P. Baumann, 2005. Cospeciation between the primary endosymbionts of mealybugs and their hosts. Curr Microbiol, 50: 84-87.

9. Baumann, P., 2005.Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects Annu Rev Microbiol, 59: 155-189.
10. Beard, C. B., S. L.O’Neill, R. B. Tesh, F. F. Richards & S. Aksoy, 1993. Modification of arthropod vector competence via symbiotic bacteria. Parasitol Today, 9: 179-183.
11. Becerra, J. X., G. X. Venable & V. Saeidi, 2015. Wolbachia-free Heteropterans do not produce defensive chemicals or alarm pheromones. Journal of Chemical Ecology, 1-9.
12. Beckage, N., 1998. Parasitoids and Polydnaviruses. Bioscience, 48: 305-311.
13. Bosquee, E., E. Haubruge & F. Francis, 2012. The 7th Congress of the International Symbiosis Society. July 2012, Krakow, Poland.
14. Broderick, N. A., K. F. Raffa & J. Handelsman, 2006. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. PNAS, 103: 15196-15199.
15. Breeuwer, J. A. J., R. Stouthamer, S. M. Barns, D. A. Pelletier, W. G.Weisburg & J. H. Werren, 1992. Phylogeny of cytoplasmic incompatibility microorganisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16S ribosomal DNA sequences. Insect Molec Biol, 1: 25-36.
16. Brumin, M., S. Kontsedalov & M. Ghanim, 2011. Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci, 18: 57-66.
17. Brumin, M., M. Levy & M. Ghanim, 2012. Transovarial Transmission of Rickettsia spp. and Organ-Specific Infection of the Whitefly Bemisia tabaci. Applied and Environmental Microbiology, 78(16): 5565-5574.
18. Buchner, P., 1965. Endosymbiosis of animals with plant microorganisms. New York: John Wiley. 909 p.
19. Carroll, G., 1988. Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology, 69: 2-9.
20. Chen, X. A., S. Li & S. Aksoy,1999. Concordant evolution of a symbiont with its host insect species: Molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J Mol Evol, 48: 49-58.
21. Chen, D-Q., C. B.Montllor & A. H. Purcell, 2000. Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, the blue alfalfa aphid, A. kondoi. Entomol Exp Appl, 95: 315-323.
22. Chiel, E., Y. Gottlieb, M. Inbar, E. Zchori-Fein & M. Ghanim, 2007. Distribution of secondary symbionts in Israeli populations of Bemisia tabaci. Bull Entomol Res, 97: 407-413.
23. Chouaia, B, P. Rossi, M. Montagna, I. Ricci, E. Crotti, C. Damiani, S. Epis, I. Faye, N. Sagnon, A. Alma, G.Favia, D. Daffonchio & C. Bandi, 2010. Molecular evidence for multiple infections as revealed by typing of Asaia bacterial symbionts of four mosquito species. Appl Environ Microbiol, 76: 7444-7450.
24. Clark, M. A., N. A. Moran, P. Baumann & J. J. Wernegreen, 2000. Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution, 54: 517-525.
25. Collins, S. R., C. W. Weldon, C. Banos & P. W. Taylor, 2008. Effects of irradiation dose rate on quality and sterility of Queensland fruit flies, Bactrocera tryoni (Froggatt). Journal of Applied Entomology, 132 (5): 398-405.
26. Cook, P. E., C. J. Mc Meniman & S. L. O’Neill, 2008. Modifying insect population age structure to control vector-borne disease. Adv Exp Med Biol, 627: 126-140.
27. Currie, C. R, 2001. A community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis. Annu Rev Microbiol, 55: 357-80.
28. Dedeine, F., F. Vavre, F. Fleury, B. Loppin, M. E. Hochberg & M. Boulétreau, 2001. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proceedings of the National Academy of Sciences, 98(11): 6247-6252.
29. Douglas, A. E., 1988. Sulfate utilization in an aphid symbiosis. Insect Biochem, 18: 599-605.
30. Douglas, A. E, 1989. Mycetocyte symbiosis in insects. Biological Reviews, 64: 409-434.
31. Douglas, A. E. & W. A. Prosser, 1992. Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. J Insect Physiol, 38: 565-568.
32. Douglas, A. E., 2006. Phloem-sap feeding by animals: problems and solutions. J Exp Bot, 57: 747-54.
33. Douglas, A. E., 2011. Lessons from studying insect symbioses. Cell Host Microbe, 10: 359-367.
34. Downie, D. A. & P. . Gullan, 2005. Phylogenetic congruence of mealybugs and their primary endosymbionts. J Evol Biol, 18: 315-324.
35. Dunbar, H. E., A. C. Wilson, N. R. Ferguson & N. A. Moran, 2007. Aphid thermal tolerance is governed by a point mutation in bacterial symbionts.PLoS Biol., 5: 1006-1015.
36. Dunn, A. M., M. J. Hatcher, R. S. Terry & C. Tofts, 1995. Evolutionary ecology of vertically transmitted parasites, transovarial transmission of a microsporidian sex ratio distorter in , Gammarus duebeni. Parasitology, 111: 91-109.
37. Faeth, S. H.,& K.E. Hammon, 1997. Fungal endophytes in oak trees. I. Long-term patterns of abundance and associations with leafminers. Ecology, 78 (3): 810-819.
38. Farikou, O., S. Thevenon, F. Njiokou, F. Allal, G. Cuny & A. Geiger, 2011. Genetic diversity and population structure of the secondary symbiont of tsetse flies, Sodalis glossinidius, in sleeping sickness foci in Cameroon. PLoS Negl Trop Dis, 5(8): e1281.
39. Febvay, G., I. Liadouze, J. Guillaud & G. Bonnot, 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.
40. Ferrari, J., A. C. Darby, T. J. Daniell, H. C. Godfray & A. E. Douglas, 2004. Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecological Entomology, 29: 60-65.
41. Frantz, A., V. Calcagno, L. Mieuzet, M. Plantegenest & J. C. Simon, 2009. Complex trait differentiation between hostpopulations of the pea aphid Acyrthosiphon pisum (Harris): implications for the evolution of ecological specialisation. Biol J Linn Soc, 97: 718-727.
42. Gehring, C. A. & T. G. Whitham, 1994. Interactions between aboveground herbivores and the mycorrhizal mutualists of plants. Trends Ecol & Evol, 9: 251-255.
43. Ghanim, M. & S. Kontsedalov, 2009. Susceptibility to insecticides in the Q biotype of Bemisia tabaci is correlated with bacterial symbiont densities. Pest Manag Sci, 65(9): 939-942.
44. Gosalbes, M. J., A. Latorre, A. Lamelas & A. Moya, 2010. Genomics of intracellular symbionts in insects. International Journal of Medical Microbiology, 300: 271-278.
45. Gottlieb, Y., E. Zchori-Fein, N. Mozes-Daube, S. Kontsedalov, M. Skaljac & M. Brumin, 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. Journal of Virology, 84: 9310-9317.
46. Gruwell, M. E., G. E. Morse & B. B. Normark, 2007. Phylogenetic congruence of armored scale insects (Hemiptera: Diaspididae) and their primary endosymbionts from the phylum Bacteroidetes. Mol Phylogenet Evol, 44: 267- 280.
47. Harmon, J. P., N. A. Moran & A. R. Ives, 2009. Species response to environmental change: impacts of food web interactions and evolution.Science, 323: 1347-1350.
48. Harris, H. L., L. J. Brennan, B. A. Keddie & H. R. Braig, 2010. Bacterial symbionts in insects: balancing life and death. Symbiosis, 51: 37-53.
49. van den Heuvel, J. F., M. Verbeek & F. van der Wilk, 1994. Endosymbiotic bacteria associated with circulative transmission of potato leafroll virus by Myzus persicae. J Gen Virol, 75: 2559-2565.
50. Hofstetter, R. W., J. T. Cronin, K. D. Klepzig, J. C. Moser & M. P. Ayres, 2006a. Antagonisms, mutualisms and commensalisms affect outbreak dynamics of the southern pine beetle. Oecologia, 147(4): 679-691.
51. Hofstetter, R. W., K. D. Klepzig, J. C. Moser & M. P. Ayres, 2006b. Seasonal dynamics of mites and fungi and their interaction with southern pine beetle. Environ Entomol, 35(1): 22-30.
52. Horowitz, A. R., S. Kontsedalov & I. Ishaaya, 2004. Dynamics of resistance to the neonicotinoids acetamiprid and thiamethoxam in Bemisia tabaci (Homoptera: Aleyrodidae). Journal of Economic Entomology, 97: 2051-2056.
53. Horowitz, A. R., S. Kontsedalov, V. Khasdan & I. Ishaaya, 2005. Biotypes B and Q of Bemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance. Archives of Insect Biochemistry and Physiology, 58: 216-225.
54. Hosokawa, T.,Y. Kikuchi, N. Nikoh, M. Shimada & T. Fukatsu, 2006. Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biology, 4: 1841-1851.
55. Hosokawa, T., Y. Kikuchi, M. Shimada & T. Fukatsu, 2007. Obligate symbiont involved in pest status of host insect. Proc R Soc B, 274: 1979-1984.
56. Hurst, G. D. D., F.M. Jiggins, J. H. G. von der Schulenburg, D. Bertrand, S. A. West, I. I. Goriacheva, I. A. Zakharov, J. H. Werren, R. Stouthamer & M. E. N. Majerus, 1999. Male killing Wolbachia in two species of insect. Proc R Soc Lond B, 266: 735-740.
57. Hurst, G. D. D., A. P. Johnson, J. H. G. von der Schulenburg & Y. Fuyama, 2000. Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics, 156: 699-709.
58. Jaenike, J., 1980. Host specialization in phytophagous insects. Annu Rev Ecol Syst, 21: 243-273.
59. Jiang, Y. X., C. de Blas, I. D. Bedford, G. Nombela & M. Muñiz, 2004. Effect of Bemisia tabaci biotype in the transmission of tomato yellow leaf curl sardinia virus (TYLCSV-ES) between tomato and common weeds. Span J Agric Res, 2: 115-119.
60. Jousselin, E., Y. Desdevises & A. Coeur d'Acier, 2009.Fine-scale cospeciation between Brachycaudus and Buchnera aphidicola: bacterial genome helps define species and evolutionary relationships in aphids. Proc Biol Sci, 276: 187-196.
61. Kikuchi, Y., M. Hayatsu, T. Hosokawa, A. Nagayama, K. Tago & T. Fukatsu, 2012. Symbiont-mediated insecticide resistance. Proceedings of the National Academy of Sciences of the United States of America, 109: 8618- 8622.
62. Kliot, A. & M. Ghanim, 2013. The role of bacterial chaperones in the circulative transmission of plant viruses by Insect Vectors. Viruses, 5(6): 1516-1535.
63. Kontsedalov, S. Zchori-Fein, E. Chiel, E. Gottlieb, Y. Inbar & M. Ghanim, 2008. The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Management Science, 64: 789-792.
64. Kumano, N., F. Kawamura, D. Haraguchi & T. Kohama, 2008a. Irradiation does not affect field dispersal ability in the West Indian sweetpotato weevil, Euscepes postfasciatus. Entomologia Experimentalis et Applicata, 130 (1): 63-72.
65. Kumano N., D. Haraguchi & T. Kohama, 2008b. Effect of irradiation on mating performance and mating ability in the West Indian sweetpotato weevil, Euscepes postfasciatus. Entomologia Experimentalis et Applicata, 127: 229-236.
66. Li, Z. X., H. Z. Lin & X. P. Guo, 2007. Prevalence of Wolbachia infection in Bemisia tabaci. Curr Microbiol, 54: 467- 471.
67. Li, M., J. Hu, F. C. Xu & S. S. Liu, 2010. Transmission of Tomato yellow leaf curl virus by two invasive biotypes and a Chinese indigenous biotype of the whitefly Bemisia tabaci. International Journal of Pest Management, 56: 275- 280.
68. Liu, L., X. L. Huang, R. L. Zhang, L. Y. Jiang & G. X. Qiao, 2013. Phylogenetic congruence between Mollitrichosiphum (Aphididae: Greenideinae) and Buchnera indicates insect-bacteria parallel evolution. Syst Entomol, 38: 81-92.
69. Lozier, J. D., G. K. Roderick & N. J. Mills, 2009. Molecular markers reveal strong geographic, but not host associated, genetic differentiation in Aphidius transcaspicus, a parasitoid of the aphid genus Hyalopterus. Bull Entomol Res, 99: 83-96.
70. MacDonald, S. J., G. H. Thomas & A. E. Douglas, 2011. Genetic and metabolic determinants of nutritional phenotype in an insect-bacterial symbiosis. Molecular Ecology, 20: 2073-2084.
71. Martínez-Torres, D., C. Buades, A. Latorre & A. Moya, 2001. Molecular systematics of aphids and their primary endosymbionts. Mol Phylogenetics and Evolution, 20: 437-449.
72. Mattson, W. J., 1980. Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst, 11: 119-161.
73. Min, K. T. & S. Benzer, 1997. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and death. Proc. Nat. Acad. Sc. USA, 94: 10792-10796.
74. Mittler, T. E., 1971. Some effects on the aphid Myzus persicae of ingesting antibiotics incorporated into artificial diets. Journal of Insect Physiology, 17: 1333-1347.
75. Montllor, C., A. Maxmen & A. H. Purcell, 2002. Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress.Ecol Entomol, 27: 189-195.
76. Moran, N. A, 1992. The evolution of life cycles in aphids. Annual Review of Entomology, 37: 321-348.
77. Moran, N. A., M. A. Munson, P. Baumann & H. Ishikawa, 1993. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc RSoc Lond B, 253: 167-171.
78. Moran, N. A. & P. Baumann, 1994. Phylogenetics of cytoplasmically inherited micro-organisms of arthropods. Trends Ecol Evol, 9: 15-20.
79. Moran, N. A.& A. Telang, 1998. Bacteriocyte-associated symbionts of insects: a variety of insect groups harbor ancient prokaryotic endosymbionts. Bioscience, 48: 295-304.
80. Moran, N. A. & P. Baumann, 2000. Bacterial endosymbionts in animals. Current Opinions in Microbiology, 3: 270- 275.
81. Morin, S., M. Ghanim, M. Zeidan, H. Czosnek, M. Verbeek & J. F. J. M. van den Heuvel,1999. A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaciis implicated in the circulative transmission of tomato yellow leaf curl virus.Virology, 256: 75-84.
82. Munson, M. A., P. Baumann & M. G. Kinsey, 1991. Buchnera gen. nov. and Buchnera aphidicola sp. nov., a taxon consisting of the mycetocyte-associated, primary endosymbionts of aphids. Int J Syst Bacteriol, 41(4): 566- 568.
83. Nakabachi, A., S. Shigenobu, N. Sakazume, T. Shiraki & Y. Hayashizaki, 2005. Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera. Proc Natl Acad Sci USA, 102: 5477-82.
84. Nikoh, N.& A. Nakabachi, 2009. Aphids acquired symbiotic genes via lateral gene transfer. BMC Biol, 7: 12.
85. Nováková, E. & N. A. Moran, 2012. Diversification of genes for carotenoid biosynthesis in aphids following an ancient transfer from a fungus. Mol Biol Evol, 29: 313-323.
86. Nováková, E., V. Hypša, J. Klein, R. G. Foottit, C. D. von Dohlen & N. A. Moran, 2013. Reconstructing the phylogeny of aphids (Hemiptera: Aphididae) using DNA of the obligate symbiont Buchnera aphidicola. Mol Phylogenet Evol, 68: 42-54.
87. Oliver, K. M., J. A. Russell, N. A. Moran & M. S. Hunter, 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA, 100: 1803-1807.
88. Oliver, K. M, N. A. Moran & M. S. Hunter, 2005. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA, 102: 12 -12
89. O'Neill, S. L., R. Giordano, A. M. E. Colbert, T. L. Karr & H. M. Robertson, 1992. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA, 94: 2699-2702.
90. Pais, R., C. Lohs, Y. Wu, J. Wang & S. Aksoy, 2008. The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly. Appl Environ Microb, 74: 5965- 5974.
91. Peccoud, J., J. C. Simon, H. J. McLaughlin & N. A. Moran, 2009. Post-Pleistocene radiation of the pea aphid complex revealed by rapidly evolving endosymbionts. Proc Natl Acad Sci USA, 106 (38): 16315-16320.
92. Perez-Brocal, V., R. Gil, S. Ramos, A. Lamelas, M. Postigo, J. M. Michelena, F. J. Silva, A. Moya & A. Latorre, 2006. A small microbial genome: the end of a long symbiotic relationship? Science, 314: 312-313.
93. Raina, H. S., V. Rawal, S. Singh, G. Daimei, M. Shakarad & R. Rajagopal, 2015. Elimination of Arsenophonus and decrease in the bacterial symbionts diversity by antibiotic treatment leads to increase in fitness of whitefly, Bemisia tabaci. Infection, Genetics and Evolution, 32: 224-230.
94. Rausher, M. D, 2001. Co-evolution and plant resistance to natural enemies. Nature, 411: 857-864.
95. Rispe, C., M. Kutsukake, V. Doublet, S. Hudaverdian, F. Legeai, J. C. Simon, D. Tagu & T. Fukatsu, 2008. Large gene family expansion and variable selective pressures for cathepsin B in aphids. Mol Biol Evol, 25. 5-17.
96. Sakurai, H.,Y. Murakami, T. Kohama & T. Teruya, 2000a. Sterilizing mechanism of γ-radiation in the female of West Indian sweet potato weevil, Euscepes fasciatus. Res Bull Fac Agric, Gifu Univ. 65: 13-20.
97. Sakurai, H., Y. Murakami, H. Utimura, T. Kohama & T. Teruya, 2000b. Sterilizing mechanism of gamma-radiation in the male of West Indian Sweet Potato weevil, Euscepes postfasciatus. Res Bull Fac Agric, Gifu Univ. 65: 5-12.
98. Sánchez-Campos, S., J. Navas-Castillo, R. Camero, C. Soria, J. A. Díaz & E. Moriones, 1999. Displacement of tomato yellow leaf curl virus (TYLCV)-Sr by TYLCV-Is in tomato epidemics in Spain. Phytopathology, 89: 1038-1043.
99. Sandström, J.& J.Pettersson, 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.
100. Sandström, J. P. & N.A. Moran, 2001. Amino acid budgets in three aphid species using the same host plant. Physiological Entomology, 26(3): 202-211.
101. Sandström, J. P. & N. A. Moran, 2001. Amino acid budgets in three aphid species using the same host plant. Physiological Entomology, 26: 202-211.
102. Sapp, J., 1994. Evolution by Association: a History of Symbiosis. Oxford University Press, Oxford, United Kingdom.
103. Scarborough, C. L., J. Ferrari & H. C. J. Godfray, 2005. Aphid protected from pathogen by endosymbiont. Science, 310: 1781-1781.
104. Schoonhoven, L. M., J. J. A. Van Loon & M. Dicke, 2005. Insect-plant Biology, 2nd edn. Oxford University Press, Oxford.
105. Schröder, D., H. Deppisch, M. Obermayer, G. Krohne, E. Stackebrandt, B. Holldobler, W. Goebel & R. Gross, 1996. Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): Systematics, evolution and ultrastructural characterization. Mol Microbiol, 21: 479-489.
106. Shigenobu, S., H. Watanabe, M. Hattori, Y. Sakaki & H. Ishikawa, 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp APS. Nature, 407: 81-86.
107. Shoemaker, D. D., V. Katju & J. Jaenike, 1999. Wolbachia and the evolution of reproductive isolation between Drosophila recens and Drosophila subquinaria. Evolution, 53: 1157-1164.
108. Singer, M. C. & C. S. McBride, 2010. Multitrait, host-associated divergence among sets of butterfly populations: implications for reproductive isolation and ecological speciation. Evolution, 64: 921-933.
109. Sinkins, S. P., H. R. Braig & S. L. O'Neill, 1995a. Wolbachia pipientis: bacterial density and unidirectional cytoplasmic incompatibility between infected populations of Aedes albopictus. Exp Parasit, 81: 284-291.
110. Sinkins, S. P., H. R. Braig & S. L. O'Neill, 1995b. Wolbachia superinfections and the expression of cytoplasmic incompatibility. Proc Soc Lond Biol, 261: 325-330.
111. Six, D. L. & T. D. Paine, 1998. Effects of mycangial fungi and host tree species on progeny survival and emergence of Dendroctonus ponderosae (Coleoptera: Scolytidae). Environmental Entomology, 27 (6): 1393-1401.
112. Slansky, F.& J.M. Jr., Scriber, 1985. Food consumption and utilization. In: Kerkut, G. A., Gilbert, L. I. (Eds.), Comprehensive Insect Physiology, Biochemistry, and Pharmacology. Pergamon Press, Oxford, pp. 87-163.
113. Sloan, D. B. & N. A. Moran, 2012. Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biol Lett, 8: 986- 989.
114. Spaulding, A. W. & C. D. von Dohlen, 1998. Phylogenetic characterization and molecular evolution of bacterial endosymbionts i n psyllids (Hemiptera: Sternorrhyncha). Mol Biol Evol, 15: 1506-1513.
115. Spaulding, A. W. & C. D. von Dohlen, 2001. Psyllid endosymbionts exhibit patterns of co-speciation with hosts and destabilizing substitutions in ribosomal RNA. Insect Mol Biol,10: 57-67.
116. Stoll, S.,H. Feldhaar & R. Gross, 2009. Transcriptional profiling of the endosymbiont Blochmannia floridanus during different developmental stages of its holometabolous ant host. Environ Microbiol, 11: 877-888.
117. Stouthamer, R., R. F. Luck & W. D. Hamilton, 1990. Antiobiotics cause parthenogenetic Trichogramma (Hymenoptera: Trichogrammatidae) to revert to sex. Proceedings of the National Academy of Sciences USA, 87: 2424–2427.
118. Stouthamer, R., J. A. Breeuwer, R. F. Luck & J. H. Werren, 1993. Molecular identification of microorganisms associated with parthenogenesis. Nature, 361: 66-68.
119. Stouthamer, R., 1997. Wolbachia-induced parthenogenesis. In: Influential passengers. Inherited Microorganisms and Arthropod Reproduction (S. L. O'Neill, A. A. Hoffmann & J. H. Werren, eds), pp. 102-124. Oxford University Press, Oxford.
120. Stouthamer, R., J. A. J. Breeuwer & G. D. D. Hurst, 1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol, 53: 71-102.
121. Su, Q., X. M. Zhou & Y. J. Zhang, 2013. Symbiont-mediated functions in insect hosts. Communicative & Integrative Biology, 6: e23804.
122. The International Aphid Genomics Consortium, 2010. Genome Sequence of the Pea Aphid Acyrthosiphon pisum. PLoS Biol, 8(2): e1000313.
123. Turelli, M., A. A. Hoffmann & S. W. McKechnie, 1992. Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulan spopulations. Genetics,132: 713-723.
124. Vorburger, C., C. Sandrock, A. Gouskov, L.E. Castañeda & J. Ferrari, 2009. Genotypic variation and the role of defensive endosymbionts in an all-parthenogenetic host-parasitoid interaction. Evolution. 63: 1439-1450.
125. Wade, M. J. & N. W. Chang, 1995. Increased male fertility in Tribolium confusum beetles after infection with the intracellular parasite Wolbachia. Nature, 373: 72-74.
126. Weiss, B. & S. Aksoy, 2011. Microbiome influences on insect host vector competence. Trends Parasitol, 27: 514-522.
127. Werren, J. H., 1997.Biology of Wolbachia. Ann Rev Entom, 42: 587-609.
128. Wilcox, J. L., H. E. Dunbar, R. D. Wolfinger & N. A. Moran, 2003. Consequences of reductive evolution for gene expression in an obligate endosymbiont. Mol Microbiol, 48: 1491-1500. Wilson, D. S. & E. Sober, 1989. "Reviving the Superorganism", Journal of Theoretical Biology, 136: 337-356.
129. Wilson, D. S. & E. Sober, 1989. Reviving the superorganism. Journal of Theoretical Biology, 136 (3): 337–356.
130. Wu, D., S. C. Daugherty, S. E. Van Aken, G. H. Pai, K. L. Watkins, H. Khouri, L. J. Tallon, J. M. Zaborsky, H. Dunbar & P.L. Tran, 2006. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol, 4: e188.
131. Zabalou, S., M. Riegler, M. Theodorakopoulou, C. Stauffer, C. Savakis & K. Bourtzis, 2004. Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proc Natl Acad Sci USA, 101: 15042-15045.
132. Zhang, F., X. Li, Y. Zhang, B. Coates, X. Zhou & D. Cheng, 2015. Bacterial symbionts, Buchnera, and starvation on wing dimorphism in English grain aphid, Sitobion avenae (F.)(Homoptera: Aphididae). Frontiers in Physiology, 6: 155.
133. Zilber-Rosenberg, I. & E. Rosenberg, 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiology Reviews, 32(5): 723-735.