Bacterial symbionts in insects or the story of communities affecting communities

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1569, 2011, Pages 1389-1400

  Ferrari, Julia ^a   Vavre, Fabrice ^b,c  

^a UNIVERSITY OF YORK   (United Kingdom)

^b UNIVERSITÉ LYON 1   (France)

^c LABORATOIRE DE BIOMÉTRIE ET BIOLOGIE EVOLUTIVE   (France)

Author keywords

Community genetics; Ecological communities; Heritable symbionts; Insects; Reproductive manipulation; Secondary symbionts

Indexed keywords

BACTERIUM; GENE FLOW; GENETIC VARIATION; HERITABILITY; HORIZONTAL TRANSMISSION; HOST PLANT; HOST-SYMBIONT INTERACTION; INSECT; NATURAL ENEMY; PHENOTYPE;

ANIMALIA; BACTERIA (MICROORGANISMS); HEXAPODA;

EID: 79953740341     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0226     Document Type: Review

References (114)

1. Douglas, A. E. 1998 Nutritional interactions in insect- microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43, 17-37. (doi:10.1146/annurev.ento.43.1.17)
2. Brownlie, J. C. & Johnson, K. N. 2009 Symbiontmediated protection in insect hosts. Trends Microbiol. 17, 348-354. (doi:10.1016/j.tim.2009.05.005)
3. Haine, E. R. 2008 Symbiont-mediated protection. Proc. R. Soc. B 275, 353-361. (doi:10.1098/rspb.2007.1211)
4. Engelstädter, J. & Hurst, G. D. D. 2009 The ecology and evolution of microbes that manipulate host reproduction. Annu. Rev. Ecol. Evol. Syst. 40, 127-149. (doi:10.1146/annurev.ecolsys.110308.120206)
5. Fleury, F., Vavre, F., Ris, N., Fouillet, P. & Bouletreau, M. 2000 Physiological cost induced by the maternallytransmitted endosymbiont Wolbachia in the Drosophilaparasitoid Leptopilina heterotoma. Parasitology 121, 493-500. (doi:10.1017/S0031182099006599)
6. Oliver, K. M., Moran, N. A. & Hunter, M. S. 2006 Costs and benefits of a superinfection of facultative symbionts in aphids. Proc. R. Soc. B 273, 1273-1280. (doi:10.1098/rspb.2005.3436)
7. Baumann, P. 2005 Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59, 155-189. (doi:10.1146/annurev. micro.59.030804.121041)
8. Moran, N. A., McCutcheon, J. P. & Nakabachi, A. 2008 Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42, 165-190. (doi:10.1146/ annurev.genet.41.110306.130119)
9. Akman Gündüz, E. & Douglas, A. E. 2009 Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc. R. Soc. B 276, 987-991. (doi:10.1098/rspb. 2008.1476)
10. Moran, N. A., Tran, P. & 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. (doi:10.1128/AEM.71.12.8802-8810.2005)
11. Nakabachi, A., Yamashita, A., Toh, H., Ishikawa, H., Dunbar, H. E., Moran, N. A. & Hattori, M. 2006 The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314, 267-267. (doi:10.1126/ science.1134196)
12. Pal, C., Papp, B., Lercher, M. J., Csermely, P., Oliver, S. G. & Hurst, L. D. 2006 Chance and necessity in the evolution of minimal metabolic networks. Nature 440, 667-670. (doi:10.1038/nature04568)
13. Tamas, I., Klasson, L., Canbäck, B., Näslund, A. K., Eriksson, A. S., Wernegreen, J. J., Sandström, J. P., Moran, N. A. & Andersson, S. G. E. 2002 50 million years of genomic stasis in endosymbiotic bacteria. Science 296, 2376-2379. (doi:10.1126/science.1071278)
14. Hosokawa, T., Kikuchi, Y., Shimada, M. & Fukatsu, T. 2007 Obligate symbiont involved in pest status of host insect. Proc. R. Soc. B 274, 1979-1984. (doi:10.1098/ rspb.2007.0620)
15. Tomokuni, M. 1993 A field guide to Japanese bugs. Tokyo, Japan: Zenkoku Noson Kyoiku Kyokai.
16. Dunbar, H. E., Wilson, A. C. C., Ferguson, N. R. & Moran, N. A. 2007 Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol. 5, 1006-1015. (doi:10.1371/journal.pbio.0050096)
17. Harmon, J. P., Moran, N. A. & Ives, A. R. 2009 Species response to environmental change: impacts of food web interactions and evolution. Science 323, 1347-1350. (doi:10.1126/science.1167396)
18. Pais, R., Lohs, C., Wu, Y. N., Wang, J. W. & Aksoy, S. 2008 The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly. Appl. Environ. Microbiol. 74, 5965-5974. (doi:10.1128/AEM.00741-08)
19. Wang, J. W., Wu, Y. N., Yang, G. X. & Aksoy, S. 2009 Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Proc. Natl Acad. Sci. USA 106, 12 133-12 138. (doi:10.1073/pnas.0901226106)
20. Feldhaar, H., Straka, J., Krischke, M., Berthold, K., Stoll, S., Mueller, M. J. & Gross, R. 2007 Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol. 5, 48. (doi:10. 1186/1741-7007-5-48)
21. de Souza, D. J., Bezier, A., Depoix, D., Drezen, J. M. & Lenoir, A. 2009 Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah. BMC Microbiol. 9, 29. (doi:10. 1186/1471-2180-9-29)
22. Moran, N. A. & Dunbar, H. E. 2006 Sexual acquisition of beneficial symbionts in aphids. Proc. Natl Acad. Sci. USA 103, 12803-12806. (doi:10.1073/pnas. 0605772103)
23. Russell, J. A., Latorre, A., Sabater-Munoz, B., Moya, A. & Moran, N. A. 2003 Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol. Ecol. 12, 1061-1075. (doi:10.1046/j.1365-294X.2003.01780.x)
24. Sandström, J. P., Russell, J. A.,White, J. P. & Moran, N. A. 2001 Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol. Ecol. 10, 217-228. (doi:10.1046/j.1365-294X.2001.01189.x)
25. Janson, E.M., Stireman, J. O., Singer, M. S. & Abbot, P. 2008 Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification. Evolution 62, 997-1012. (doi:10.1111/j.1558-5646.2008.00348.x)
26. Oliver, K. M., Degnan, P. H., Burke, G. R. & Moran, N. A. 2010 Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu. Rev. Entomol. 55, 247-266. (doi:10.1146/ annurev-ento-112408-085305)
27. Oliver, K. M., Russell, J. A., Moran, N. A. & Hunter, M. S. 2003 Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl Acad. Sci. USA 100, 1803-1807. (doi:10.1073/pnas.0335320100)
28. Degnan, P. H. & Moran, N. A. 2008 Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage. Mol. Ecol. 17, 916-929. (doi:10.1111/j.1365-294X.2007.03616.x)
29. Moran, N. A., Degnan, P. H., Santos, S. R., Dunbar, H. E. & Ochman, H. 2005 The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc. Natl Acad. Sci. USA 102, 16 919-16 926. (doi:10.1073/pnas.0507029102)
30. Oliver, K. M., Degnan, P. H., Hunter, M. S. & Moran, N. A. 2009 Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325, 992-994. (doi:10.1126/science.1174463)
31. Oliver, K. M., Campos, J., Moran, N. A. & Hunter, M. S. 2008 Population dynamics of defensive symbionts in aphids. Proc. R. Soc. B 275, 293-299. (doi:10.1098/ rspb.2007.1192)
32. Ferrari, J., Darby, A. C., Daniell, T. J., Godfray, H. C. J. & Douglas, A. E. 2004 Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol. Entomol. 29, 60-65. (doi:10.1111/j. 1365-2311.2004.00574.x)
33. Guay, J.-F., Boudreault, S., Michaud, D. & Cloutier, C. 2009 Impact of environmental stress on aphid clonal resistance to parasitoids: role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid. J. Insect Physiol. 55, 919-926. (doi:10. 1016/j.jinsphys.2009.06.006)
34. von Burg, S., Ferrari, J., Müller, C. B. & Vorburger, C. 2008 Genetic variation and covariation of susceptibility to parasitoids in the aphid Myzus persicae-no evidence for trade-offs. Proc. R. Soc. B 275, 1089-1094. (doi:10. 1098/rspb.2008.0018)
35. Vorburger, C., Gehrer, L. & Rodriguez, P. 2010 A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol. Lett. 6, 109-111. (doi:10.1098/rsbl.2009.0642)
36. Fytrou, A., Schofield, P. G., Kraaijeveld, A. R. & Hubbard, S. F. 2006 Wolbachia infection suppresses both host defence and parasitoid counter-defence. Proc. R. Soc. B 273, 791-796. (doi:10.1098/rspb.2005.3383)
37. Scarborough, C. L., Ferrari, J. & Godfray, H. C. J. 2005 Aphid protected from pathogen by endosymbiont. Science 310, 1781-1781. (doi:10.1126/science.1120180)
38. Currie, C. R., Scott, J. A., Summerbell, R. C. & Malloch, D. 1999 Fungus-growing ants use antibioticproducing bacteria to control garden parasites. Nature 398, 701-704. (doi:10.1038/19519)
39. Kaltenpoth, M., Gottler, W., Herzner, G. & Strohm, E. 2005 Symbiotic bacteria protect wasp larvae from fungal infestation. Curr. Biol. 15, 475-479. (doi:10.1016/j.cub.2004.12.084)
40. Scott, J. J., Oh, D. C., Yuceer, M. C., Klepzig, K. D., Clardy, J. & Currie, C. R. 2008 Bacterial protection of beetle-fungus mutualism. Science 322, 63. (doi:10.1126/science.1160423)
41. Hedges, L. M., Brownlie, J. C., O'Neill, S. L. & Johnson, K. N. 2008 Wolbachia and virus protection in insects. Science 322, 702-702. (doi:10.1126/science.1162418)
42. 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)
43. Osborne, S. E., Leong, Y. S., O'Neill, S. L. & Johnson, K. N. 2009 Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog. 5, e1000656. (doi:10.1371/journal.ppat.1000656)
44. Gil-Turnes, M. S. & Fenical, W. 1992 Embryos of Homarus americanus are protected by epibiotic bacteria. Biol. Bull. 182, 105-108. (doi:10.2307/1542184)
45. Gil-Turnes, M.S.,Hay, M.E.& Fenical, W. 1989Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 246, 116-118. (doi:10. 1126/science.2781297)
46. Haine, E. R., Boucansaud, K. & Rigaud, T. 2005 Conflict between parasites with different transmission strategies infecting an amphipod host. Proc. R. Soc. B 272, 2505-2510. (doi:10.1098/rspb.2005.3244)
47. Ferrari, J., Via, S. & Godfray, H. C. J. 2008 Population differentiation and genetic variation in performance on eight hosts in the pea aphid complex. Evolution 62, 2508-2524. (doi:10.1111/j.1558-5646.2008.00468.x)
48. Peccoud, J., Ollivier, A., Plantegenest, M. & Simon, C. 2009 A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proc. Natl Acad. Sci. USA 106, 7495-7500. (doi:10.1073/pnas.0811117106)
49. Via, S. 1991 The genetic structure of host plant adaptation in a spatial patchwork-demographic variability among reciprocally transplanted pea aphid clones. Evolution 45, 827-852. (doi:10.2307/2409692)
50. Frantz, A., Calcagno, V., Mieuzet, L., Plantegenest, M. & Simon, J. C. 2009 Complex trait differentiation between host-populations of the pea aphid Acyrthosiphon pisum (Harris): implications for the evolution of ecological specialisation. Biol. J. Linn. Soc. 97, 718-727. (doi:10.1111/j.1095-8312.2009.01221.x)
51. Leonardo, T. E. & Muiru, G. T. 2003 Facultative symbionts are associated with host plant specialization in pea aphid populations. Proc. R. Soc. Lond. B 270, S209-S212. (doi:10.1098/rsbl.2003.0064)
52. Simon, J. C., Carre, S., Boutin, M., Prunier-Leterme, N., Sabater-Munoz, B., Latorre, A. & Bournoville, R.2003 Host-based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts. Proc. R. Soc. Lond. B 270, 1703-1712. (doi:10.1098/rspb.2003.2430)
53. Tsuchida, T., Koga, R., Shibao, H., Matsumoto, T. & Fukatsu, T. 2002 Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol. Ecol. 11, 2123-2135. (doi:10.1046/j.1365-294X.2002.01606.x)
54. Ferrari, J., Scarborough, C. L. & Godfray, H. C. J. 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)
55. Leonardo, T. E. 2004 Removal of a specialization-associated symbiont does not affect aphid fitness. Ecol. Lett. 7, 461-468. (doi:10.1111/j.1461-0248.2004.00602.x)
56. McLean, A. H. C., van Asch, M., Ferrari, J. & Godfray, H. C. J. 2011 Effects of bacterial secondary symbionts on host plant use in pea aphids. Proc. R. Soc. B 278, 760-766. (doi:10.1098/rspb.2010.1654)
57. Tsuchida, T., Koga, R. & Fukatsu, T. 2004 Host plant specialization governed by facultative symbiont. Science 303, 1989-1989. (doi:10.1126/science.1094611)
58. van den Heuvel, J. F. J. M., Verbeek, M. & van der Wilk, F. 1994 Endosymbiotic bacteria associated with circulative transmission of potato leafroll virus by Myzus persicae. J. Gen. Virol. 75, 2559-2565. (doi:10.1099/0022-1317-75-10-2559)
59. Morin, S., Ghanim, M., Zeidan, M., Czosnek, H., Verbeek, M. & van den Heuvel, J. F. J. M. 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. (doi:10.1006/viro.1999.9631)
60. Akad, F., Eybishtz, A., Edelbaum, D., Gorovits, R., Dar-Issa, O., Iraki, N. & Czosnek, H. 2007 Making a friend from a foe: expressing a GroEL gene from the whitefly Bemisia tabaci in the phloem of tomato plants confers resistance to tomato yellow leaf curl virus. Arch. Virol. 152, 1323-1339. (doi:10.1007/s00705- 007-0942-0)
61. Edelbaum, D., Gorovits, R., Sasaki, S., Ikegami, M. & Czosnek, H. 2009 Expressing a whitefly GroEL protein in Nicotiana benthamiana plants confers tolerance to tomato yellow leaf curl virus and cucumber mosaic virus, but not to grapevine virus A or tobacco mosaic virus. Arch. Virol. 154, 399-407. (doi:10.1007/ s00705-009-0317-9)
62. Montllor, C. B., Maxmen, A. & Purcell, A. H. 2002 Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol. Entomol. 27, 189-195. (doi:10.1046/j.1365-2311.2002.00393.x)
63. Leonardo, T. E. & Mondor, E. B. 2006 Symbiont modifies host life-history traits that affect gene flow. Proc. R. Soc. B 273, 1079-1084. (doi:10.1098/rspb.2005.3408)
64. Herzog, J., Muller, C. B. & Vorburger, C. 2007 Strong parasitoid-mediated selection in experimental populations of aphids. Biol. Lett. 3, 667-669. (doi:10.1098/ rsbl.2007.0362)
65. Hughes, A. R., Inouye, B. D., Johnson, M. T. J., Underwood, N. & Vellend, M. 2008 Ecological consequences of genetic diversity. Ecol. Lett. 11, 609-623. (doi:10.1111/j.1461-0248.2008.01179.x)
66. Oliver, K. M., Moran, N. A. & Hunter, M. S. 2005 Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc. Natl Acad. Sci. USA 102, 12 795-12 800. (doi:10.1073/pnas.0506131102)
67. Boto, L. 2010 Horizontal gene transfer in evolution: facts and challenges. Proc. R. Soc. B 277, 819-827. (doi:10.1098/rspb.2009.1679)
68. Koonin, E. V. 2009 The Origin at 150: is a new evolutionary synthesis in sight? Trends Genet. 25, 473-475. (doi:10.1016/j.tig.2009.09.007)
69. Hurst, G. D. D. & Darby, A. C. 2009 The inherited microbiota of arthropods, and their importance inunderstanding resistance and immunity. In Insect infection and immunity-evolution, ecology, and mechanisms (eds J. Rolff & S. E. Reynolds), pp. 119-136. Oxford, UK: Oxford University Press.
70. Darby, A. C., Choi, J. H., Wilkes, T., Hughes, M. A., Werren, J. H., Hurst, G. D. D. & Colbourne, J. K.2010 Characteristics of the genome of Arsenophonus nasoniae, son-killer bacterium of the wasp Nasonia. Insect Mol. Biol. 19, 75-89. (doi:10.1111/j.1365-2583.2009.00950.x)
71. Wade, M. J. & Goodnight, C. J. 2006 Cyto-nuclear epistasis: two-locus random genetic drift in hermaphroditic and dioecious species. Evolution 60, 643-659.
72. Ros, V. I. D. & Hurst, G. D. D. 2009 Lateral gene transfer between prokaryotes and multicellular eukaryotes: ongoing and significant? BMC Biol. 7, 20. (doi:10.1186/1741-7007-7-20)
73. Duron, O.,Bouchon, D., Boutin, S., Bellamy, L., Zhou, L., Engelstädter, J. & Hurst, G. D. 2008 The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol. 6, 27. (doi:10.1186/1741-7007-6-27)
74. Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A. & Werren, J. H. 2008 How many species are infected with Wolbachia?-a statistical analysis of current data. FEMS Microbiol. Lett. 281, 215-220. (doi:10.1111/j.1574-6968.2008.01110.x)
75. Charlat, S., Reuter, M., Dyson, E. A., Hornett, E. A., Duplouy, A., Davies, N., Roderick, G. K., Wedell, N. & Hurst, G. D. D. 2007 Male-killing bacteria trigger a cycle of increasing male fatigue and female promiscuity. Curr. Biol. 17, 273-277. (doi:10.1016/j.cub.2006.11.068)
76. Slothouber Galbreath, J. G. M., Smith, J. E., Terry, R. S., Becnel, J. J. & Dunn, A. M. 2004 Invasion success of Fibrillanosema crangonycis, n.sp., n.g.: a novel vertically transmitted microsporidian parasite from the invasive amphipod host Crangonyx pseudogracilis. Int. J. Parasitol. 34, 235-244. (doi:10.1016/j.ijpara.2003.10.009)
77. Engelstädter, J. & Hurst, G. D. D. 2007 The impact of male-killing bacteria on host evolutionary processes. Genetics 175, 245-254. (doi:10.1534/genetics.106.060921)
78. Rigaud, T. & Juchault, P. 1992 Genetic-control of the vertical transmission of a cytoplasmic sex factor in Armadillidium vulgare Latr (Crustacea, Oniscidea). Heredity 68, 47-52. (doi:10.1038/hdy.1992.6)
79. Rigaud, T. & Juchault, P. 1993 Conflict between feminizing sex-ratio distorters and an autosomal masculinizing gene in the terrestrial isopod Armadillidium vulgare Latr. Genetics 133, 247-252.
80. Hornett, E. A., Charlat, S., Duplouy, A. M. R., Davies, N., Roderick, G. K.,Wedell, N. & Hurst, G. D. D. 2006 Evolution of male-killer suppression in a natural population. PLoS Biol. 4, 1643-1648. (doi:10.1371/journal. pbio.0040283)
81. Charlat, S., Hornett, E. A., Fullard, J. H., Davies, N., Roderick, G. K., Wedell, N. & Hurst, G. D. D. 2007 Extraordinary flux in sex ratio. Science 317, 214-214. (doi:10.1126/science.1143369)
82. Hornett, E. A., Charlat, S., Wedell, N., Jiggins, C. D. & Hurst, G. D. D. 2009 Rapidly shifting sex ratio across a species range. Curr. Biol. 19, 1628-1631. (doi:10.1016/ j.cub.2009.07.071)
83. Huigens, M. E. & Stouthamer, R. 2003 Parthenogenesis associated with Wolbachia. In Insect symbiosis (eds K. Bourtzis & T. A. Miller), pp. 247-266. Boca Raton, FL: CRC Press.
84. Engelstädter, J. & Telschow, A. 2009 Cytoplasmic incompatibility and host population structure. Heredity 103, 196-207. (doi:10.1038/hdy.2009.53)
85. Telschow, A., Hammerstein, P. & Werren, J. H. 2002 The effect of Wolbachia on genetic divergence between populations: models with two-way migration. Am. Nat. 160, S54-S66. (doi:10.1086/342153)
86. Greischar, M. A. & Koskella, B. 2007 A synthesis of experimental work on parasite local adaptation. Ecol. Lett. 10, 418-434. (doi:10.1111/j.1461-0248.2007.01028.x)
87. van Alphen, J. J. M. & Visser, M. E. 1990 Superparasitism as an adaptive strategy for insect parasitoids. Annu. Rev. Entomol. 35, 59-79. (doi:10.1146/annurev.en.35.010190.000423)
88. Sirot, E. & Krivan, V. 1997 Adaptive superparasitism and host-parasitoid dynamics. Bull. Math. Biol. 59, 23-41. (doi:10.1007/BF02459469)
89. Varaldi, J., Fouillet, P., Ravallec, M., Lopez-Ferber, M., Bouletreau, M. & Fleury, F. 2003 Infectious behavior in a parasitoid. Science 302, 1930-1930. (doi:10.1126/ science.1088798)
90. Patot, S., Martinez, J., Allemand, R., Gandon, S., Varaldi, J. & Fleury, F. 2010 Prevalence of a virus inducing behavioural manipulation near species range border. Mol. Ecol. 19, 2995-3007.
91. Patot, S., Lepetit, D., Charif, D., Varaldi, J. & Fleury, F. 2009 Molecular detection, penetrance, and transmission of an inherited virus responsible for behavioral manipulation of an insect parasitoid. Appl. Environ. Microbiol. 75, 703-710. (doi:10.1128/AEM.01778-08)
92. Gandon, S., Rivero, A. & Varaldi, J. 2006 Superparasitism evolution: adaptation or manipulation? Am. Nat. 167, E1-E22. (doi:10.1086/498398)
93. Varaldi, J., Patot, S., Nardin, M. & Gandon, S. 2009 A virus-shaping reproductive strategy in a Drosophila parasitoid. Adv. Parasitol. 70, 333-363. (doi:10.1016/ S0065-308X(09)70013-2)
94. Prenter, J., MacNeil, C., Dick, J. T. A. & Dunn, A. M. 2004 Roles of parasites in animal invasions. Trends Ecol. Evol. 19, 385-390. (doi:10.1016/j.tree.2004.05.002)
95. Darby, A. C., Birkle, L. M., Turner, S. L. & Douglas, A. E. 2001 An aphid-borne bacterium allied to the secondary symbionts of whitefly. FEMS Microbiol. Ecol. 36, 43-50. (doi:10.1111/j.1574-6941.2001.tb00824.x)
96. 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)
97. Gueguen, G. et al. 2010 Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Mol. Ecol. 19, 4365-4376. (doi:10.1111/j.1365-294x.2010.04775.x)
98. Vautrin, E. & Vavre, F. 2009 Interactions between vertically transmitted symbionts: cooperation or conflict? Trends Microbiol. 17, 95-99. (doi:10.1016/j.tim.2008.12.002)
99. Wade, M. J. 2007 The co-evolutionary genetics of ecological communities. Nat. Rev. Genet. 8, 185-195. (doi:10.1038/nrg2031)
100. Mouton, L., Dedeine, F., Henri, H., Bouletreau, M., Profizi, N. & Vavre, F. 2004 Virulence, multiple infections and regulation of symbiotic population in the Wolbachia-Asobara tabida symbiosis. Genetics 168, 181-189. (doi:10.1534/genetics.104.026716)
101. Chiel, E., Gottlieb, Y., Zchori-Fein, E., Mozes-Daube, N., Katzir, N., Inbar, M. & Ghanim, M. 2007 Biotypedependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bull. Entomol. Res. 97, 407-413. (doi:10.1017/S0007485307005159)
102. Goto, S., Anbutsu, H. & Fukatsu, T. 2006 Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Appl. Environ. Microbiol. 72, 4805-4810. (doi:10.1128/AEM.00416-06)
103. Koga, R., Tsuchida, T. & Fukatsu, T. 2003 Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc. R. Soc. Lond. B 270, 2543-2550. (doi:10.1098/ rspb.2003.2537)
104. Sakurai, M., Koga, R., Tsuchida, T., Meng, X. Y. & Fukatsu, T. 2005 Rickettsia symbiont in the pea aphid Acyrthosiphon pisum: novel cellular tropism, effect on host fitness, and interaction with the essential symbiont Buchnera. Appl. Environ. Microbiol. 71, 4069-4075. (doi:10.1128/AEM.71.7.4069-4075.2005)
105. Vautrin, E., Genieys, S., Charles, S. & Vavre, F. 2008 Do vertically transmitted symbionts co-existing in a single host compete or cooperate? A modelling approach. J. Evol. Biol. 21, 145-161. (doi:10.1111/j.1420-9101.2007.01460.x)
106. Mouton, L., Henri, H., Bouletreau, M. & Vavre, F.2003 Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Mol. Ecol. 12, 3459-3465. (doi:10.1046/j.1365-294X.2003.02015.x)
107. Brandvain, Y., Barker, M. S. & Wade, M. J. 2007 Gene co-inheritance and gene transfer. Science 315, 1685-1685. (doi:10.1126/science.1134789)
108. Wu, D. et al. 2006 Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 4, 1079-1092. (doi:10.1371/journal. pbio.0040188)
109. Woyke, T. et al. 2006 Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443, 950-955. (doi:10.1038/nature05192)
110. Gosalbes, M. J., Lamelas, A., Moya, A. & Latorre, A. 2008 The striking case of tryptophan provision in the cedar aphid Cinara cedri. J. Bacteriol. 190, 6026-6029. (doi:10.1128/JB.00525-08)
111. Perez-Brocal, V., Gil,R., Ramos, S., Lamelas, A., Postigo, M.,Michelena, J. M., Silva, F. J., Moya, A. & Latorre, A. 2006 A small microbial genome: the end of a long symbiotic relationship? Science 314, 312-313. (doi:10.1126/ science.1130441)
112. McMeniman, C. J., Lane, R. V., Cass, B. N., Fong, A. W. C., Sidhu, M., Wang, Y. F. & O'Neill, S. L. 2009 Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323, 141-144. (doi:10.1126/science.1165326)
113. Turley, A. P., Moreira, L. A., O'Neill, S. L. & McGraw, E. A. 2009 Wolbachia infection reduces blood-feeding success in the dengue fever mosquito, Aedes aegypti. PLoS Neglect. Trop. Dis. 3, e516. (doi:10.1371/journal. pntd.0000516)
114. Kambris, Z., Cook, P. E., Phuc, H. K. & Sinkins, S. P. 2009 Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 326, 134-136. (doi:10.1126/science1177531)