Nine facultative endosymbionts in aphids. A review

[en] Aphids are frequently engaged in mutualistic associations with endosymbionts. Symbionts are bacterial or fungal microorganisms that can be obligate or facultative to aphids. Research showed facultative (or secondary) symbionts have numerous effects on their host aphids such as resistance to heat shock, parasitoids and fungus etc., which may consequently promote a co-evolution between symbionts and hosts. However, this symbiotic relation may be affected by several factors, such as the ability of symbionts to spread from aphids to others within and across populations, and the cost of infections for hosts. Moreover, aphid-symbionts interactions may be affected by aphid living environment such as its host plant, the presence of natural enemies or the temperature. Here we firstly described the functions of nine facultative symbionts (Serratia symbiotica, Hamiltonella defensa, Regiella insecticola, Rickettsia, Rickettsiella, PAXS (pea aphid X-type symbiont), Spiroplasma, Wolbachia and Arsenophonus) studied in aphids one by one, and discussed the associations between these symbionts and aphids, plants and environment. We aim to have a better knowledge of the roles the facultative symbionts play in aphid biology, ecology and evolution, which we believe can provide new inspirations for aphid control.

Research Center/Unit :

TERRA Teaching and Research Centre - TERRA

Disciplines :

Entomology & pest control
Microbiology
Environmental sciences & ecology

Author, co-author :

Guo, Jianqing ; Université de Liège - ULiège > Doct. sc. agro. & ingé. biol. (Paysage)

Hatt, Séverin ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs

He, Kanglai; Chinese Academy of Agricultural Sciences > Institute of Plant Protection > State Key Laboratory for Biology of Plant Diseases and Insect Pests

Chen, Julian; Chinese Academy of Agricultural Sciences > Institute of Plant Protection > State Key Laboratory for Biology of Plant Diseases and Insect Pests

Francis, Frédéric ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs

Wang, Zhenying; Chinese Academy of Agricultural Sciences > Institute of Plant Protection > State Key Laboratory for Biology of Plant Diseases and Insect Pests

Language :

English

Title :

Nine facultative endosymbionts in aphids. A review

Publication date :

2017

Journal title :

Journal of Asia-Pacific Entomology

ISSN :

1226-8615

eISSN :

1876-7990

Publisher :

Elsevier

Volume :

Pages :

794-801

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

http://www.sciencedirect.com/science/article/pii/S1226861517300262

Funders :

CARE AgricultureIsLife (University of Liège)
Opening Fund of State Key Laboratory for Biology of Plant Diseases and Insect Pests (SKLOF201601)

Available on ORBi :

since 18 June 2017

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Bibliography

Asplen, M.K., Bano, N., Brady, C.M., Desneux, N., Hopper, K.R., Malouines, C., Oliver, K.M., White, J.A., Heimpel, G.E., Specialisation of bacterial endosymbionts that protect aphids from parasitoids. Ecol. Entomol. 39:6 (2014), 736–739.
Augustinos, A.A., Santos-Garcia, D., Dionyssopoulou, E., Moreira, M., Papapanagiotou, A., Scarvelakis, M., Doudoumis, V., Ramos, S., Aguiar, A.F., Borges, P.A.V. et al., Detection and characterization of Wolbachia infections in natural populations of aphids: is the hidden diversity fully unraveled?. PLoS One 6 (2011), 1–10.
Baumann, P., Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59 (2005), 155–189.
Burke, G.R., Moran, N.A., Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol. Evol. 3 (2011), 195–208.
Castañeda, L.E., Sandrock, C., Vorburger, C., Variation and covariation of life history traits in aphids are related to infection with the facultative bacterial endosymbiont Hamiltonella defensa. Biol. J. Linn. Soc. 100 (2010), 237–247.
Cayetano, L., Vorburger, C., Symbiont-conferred protection against Hymenopteran parasitoids in aphids: how general is it?. Ecol. Entomol. 40 (2015), 85–93.
Cayetano, L., Rothacher, L., Simon, J.C., Vorburger, C., Cheaper is not always worse: strongly protective isolates of a defensive symbiont are less costly to the aphid host. P. Roy. Soc. B-Biol. Sci., 282(1799), 2015, 20142333.
Chen, D.Q., Purcell, A.H., Occurrence and transmission of facultative endosymbionts in aphids. Curr. Microbiol. 34 (1997), 220–225.
Chen, D.Q., Campbell, B.C., Purcell, A.H., A new Rickettsia from a herbivorous insect, the pea aphid Acyrthosiphon pisum (Harris). Curr. Microbiol. 33 (1996), 123–128.
Chen, D.Q., Montllor, C.B., Purcell, A.H., Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi. Entomol. Exp. Appl. 95 (2000), 315–323.
Cordaux, R., Pacesfessy, M., Raimond, M., Michelsalzat, A., Zimmer, M., Bouchon, D., Molecular characterization and evolution of arthropod-pathogenic Rickettsiella bacteria. Appl. Environ. Microbiol. 73:15 (2007), 5045–5047.
Costopoulos, K., Kovacs, J., Kamins, A., Gerardo, N., Aphid facultative symbionts reduce survival of the predatory lady beetle Hippodamia convergens. BMC Ecol. 14 (2014), 80–91.
Darby, A.C., Birkle, L.M., Turner, S.L., Douglas, A.E., An aphid-borne bacterium allied to the secondary symbionts of whitefly. FEMS Microbiol. Ecol. 36 (2001), 43–50.
De Clerck, C., Tsuchida, T., Massart, S., Lepoivre, P., Francis, F., Jijakli, M.H., Combination of genomic and proteomic approaches to characterize the symbiotic population of the banana aphid (Hemiptera: Aphididae). Environ. Entomol. 43 (2014), 29–36.
De Clerck, C., Fujiwara, A., Joncour, P., Léonard, S., Félix, M.-L., Francis, F., Jijakli, M.H., Tsuchida, T., Massart, S., A metagenomic approach from aphid's hemolymph sheds light on the potential roles of co-existing endosymbionts. Microbiome 3 (2015), 1–11.
Degnan, P.H., Moran, N.A., Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage. Mol. Ecol. 17 (2008), 916–929.
Degnan, P.H., Moran, N.A., Diverse phage-encoded toxins in a protective insect endosymbiont. Appl. Environ. Microbiol. 74 (2008), 6782–6791.
Dion, E., Zélé, F., Simon, J.C., Outreman, Y., Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts. J. Evol. Biol. 24 (2011), 741–750.
Donald, K.J., Clarke, H.V., Mitchell, C., Cornwell, R.M., Hubbard, S.F., Karley, A.J., Protection of pea aphids associated with coinfecting bacterial symbionts persists during superparasitism by a braconid wasp. Microb. Ecol. 71:1 (2016), 1–4.
Douglas, A., Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43 (1998), 17–37.
Douglas, A.E., FranÇois, C.L.M.J., Minto, L.B., Facultative ‘secondary’ bacterial symbionts and the nutrition of the pea aphid, Acyrthosiphon pisum. Physiol. Entomol. 31:3 (2006), 262–269.
Duron, O., Arsenophonus insect symbionts are commonly infected with APSE, a bacteriophage involved in protective symbiosis. FEMS Microbiol. Ecol. 90 (2014), 184–194.
Dykstra, H.R., Weldon, S.R., Martinez, A.J., White, J.A., Hopper, K.R., Heimpel, G.E., Asplen, M.K., Oliver, K.M., Factors limiting the spread of the protective symbiont Hamiltonella defensa in Aphis craccivora aphids. Appl. Environ. Microbiol. 80 (2014), 5818–5827.
Elsik, C.G., The pea aphid genome sequence brings theories of insect defense into question. Genome Biol. 11 (2010), 1–3.
Ferrari, J., Darby, A.C., Daniell, T.J., Godfray, H.C.J., Douglas, A.E., Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol. Entomol. 29 (2004), 60–65.
Ferrari, J., Scarborough, C., Godfray, H.C., Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids. Oecologia 153 (2007), 323–329.
Ferrari, J., West, J.A., Via, S., Godfray, H.C.J., Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution 66 (2012), 375–390.
Frantz, A., Calcagno, V., Mieuzet, L., Plantegenest, M., Simon, J.C., 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 (2009), 718–727.
Fukatsu, T., Endosymbiosis of aphids with microorganisms: a model case of dynamic endosymbiotic evolution. Plant Species Biol. 9 (1994), 145–154.
Fukatsu, T., Nikoh, N., Kawai, R., Koga, R., The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta: Homoptera). Appl. Environ. Microbiol. 66 (2000), 2748–2758.
Fukatsu, T., Tsuchida, T., Nikoh, N., Koga, R., Spiroplasma symbiont of the pea aphid, Acyrthosiphon pisum (Insecta: Homoptera). Appl. Environ. Microbiol. 67 (2001), 1284–1291.
Gehrer, L., Vorburger, C., Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol. Lett. 8 (2012), 613–615.
Gerardo, N.M., Altincicek, B., Anselme, C., Atamian, H., Barribeau, S.M., De Vos, M., Duncan, E.J., Evans, J.D., Gabaldón, T., Ghanim, M., Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol., 11, 2010, R21.
Gherna, R.L., Werren, J.H., Weisburg, W., Cote, R., Woese, C.R., Mandelco, L., Brenner, D.J., Notes: Arsenophonus nasoniae gen. nov., sp. nov., the causative agent of the son-killer trait in the parasitic wasp Nasonia vitripennis. Int. J. Syst. Bacteriol. 41 (1991), 563–565.
Gil, R., Sabater-Muñoz, B., Latorre, A., Silva, F.J., Moya, A., Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life. Proc. Natl. Acad. Sci. 99 (2002), 4454–4458.
Gómez-Valero, L., Soriano-Navarro, M., Pérez-Brocal, V., Heddi, A., Moya, A., García-Verdugo, J.M., Latorre, A., Coexistence of Wolbachia with Buchnera aphidicola and a secondary symbiont in the aphid Cinara cedri. J. Bacteriol. 186 (2004), 6626–6633.
Gross, R., Vavre, F., Heddi, A., Hurst, G.D.D., Zchori-Fein, E., Bourtzis, K., Immunity and symbiosis. Mol. Microbiol. 73:5 (2009), 751–759.
Guay, J.F., Boudreault, S., Michaud, D., Cloutier, C., 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 (2009), 919–926.
Hadfield, S.J., Axton, J.M., Reproduction: germ cells colonized by endosymbiotic bacteria. Nature, 402, 1999, 482.
Haine, E.R., Symbiont-mediated protection. P. Roy. Soc. B-Biol. Sci. 275 (2008), 353–361.
Henry, L.M., Peccoud, J., Simon, J.C., Hadfield, J.D., Maiden, M.J.C., Ferrari, J., Godfray, H.C.J., Horizontally transmitted symbionts and host colonization of ecological niches. Curr. Biol. 23 (2013), 1713–1717.
Hertig, M., The Rickettsia, Wolbachia pipientis (gen. et sp.n.) and associated inclusions of the mosquito, Culex pipiens. Parasitology 28 (1936), 453–486.
Heyworth, E.R., Ferrari, J., A facultative endosymbiont in aphids can provide diverse ecological benefits. J. Evol. Biol. 28 (2015), 1753–1760.
Hrček, J., McLean, A.H.C., Godfray, H.C.J., Symbionts modify interactions between insects and natural enemies in the field. J. Anim. Ecol., 2016, 10.1111/1365-2656.12586.
Huger, A.M., Skinner, S.W., Werren, J.H., Bacterial infections associated with the son-killer trait in the parasitoid wasp Nasonia (= Mormoniella) vitripennis (Hymenoptera: Pteromalidae). J. Invertebr. Pathol. 46:3 (1985), 272–280.
Jaenike, J., Population genetics of beneficial heritable symbionts. Trends Ecol. Evol. 27 (2012), 226–232.
Janson, E.M., Stireman, J.O., Singer, M.S., Abbot, P., Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification. Evolution 62 (2008), 997–1012.
Janzen, D.H., Coevolution of mutualism between ants and acacias in Central America. Evolution 20 (1966), 249–275.
Jeyaprakash, A., Hoy, M.A., Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol. Biol. 9 (2000), 393–405.
Jiggins, F.M., Hurst, G.D.D., Jiggins, C.D., v.d. Schulenburg, J.H.G., Majerus, M.E.N., The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium. Parasitology 120 (2000), 439–446.
Jousselin, E., Cœur d'Acier, A., Vanlerberghe-Masutti, F., Duron, O., Evolution and diversity of Arsenophonus endosymbionts in aphids. Mol. Ecol. 22 (2013), 260–270.
Koga, R., Tsuchida, T., Fukatsu, T., Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. P. Roy. Soc. B-Biol. Sci. 270 (2003), 2543–2550.
Koga, R., Tsuchida, T., Sakurai, M., Fukatsu, T., Selective elimination of aphid endosymbionts: effects of antibiotic dose and host genotype, and fitness consequences. FEMS Microbiol. Ecol. 60 (2007), 229–239.
Lamelas, A., Pérez-Brocal, V., Gómez-Valero, L., Gosalbes, M.J., Moya, A., Latorre, A., Evolution of the secondary symbiont “Candidatus Serratia symbiotica” in aphid species of the subfamily Lachninae. Appl. Environ. Microbiol. 74 (2008), 4236–4240.
Lamelas, A., Gosalbes, M.J., Manzano-Marín, A., Peretó, J., Moya, A., Latorre, A., Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont. PLoS Genet., 7, 2011, e1002357.
Laughton, A.M., Fan, M.H., Gerardo, N.M., The combined effects of bacterial symbionts and ageing on life history traits in the pea aphid, Acyrthosiphon pisum. Appl. Environ. Microbiol. 80 (2013), 470–477.
Laughton, A.M., Garcia, J.R., Gerardo, N.M., Condition-dependent alteration of cellular immunity by secondary symbionts in the pea aphid, Acyrthosiphon pisum. J. Insect Physiol. 86 (2016), 17–24.
Leclair, M., Polin, S., Jousseaume, T., Simon, J.C., Sugio, A., Morlière, S., Fukatsu, T., Tsuchida, T., Outreman, Y., Consequences of coinfection with protective symbionts on the host phenotype and symbiont titres in the pea aphid system. Insect Sci, 2016, 10.1111/1744-7917.12380.
Leclair, M., Pons, I., Mahéo, F., Morlière, S., Simon, J.C., Outreman, Y., Diversity in symbiont consortia in the pea aphid complex is associated with large phenotypic variation in the insect host. Evol. Ecol. 30:5 (2016), 925–941.
Leonardo, T.E., Removal of a specialization-associated symbiont does not affect aphid fitness. Ecol. Lett. 7 (2004), 461–468.
Leonardo, T.E., Mondor, E.B., Symbiont modifies host life-history traits that affect gene flow. P. Roy. Soc. B-Biol. Sci. 273 (2006), 1079–1084.
Leonardo, T.E., Muiru, G.T., Facultative symbionts are associated with host plant specialization in pea aphid populations. P. Roy. Soc. B-Biol. Sci. 270:Suppl. 2 (2003), S209–S212.
Łukasik, P., Dawid, M., Ferrari, J., Godfray, H.C., The diversity and fitness effects of infection with facultative endosymbionts in the grain aphid, Sitobion avenae. Oecologia 173 (2013), 985–996.
Łukasik, P., Guo, H., van Asch, M., Ferrari, J., Godfray, H.C.J., Protection against a fungal pathogen conferred by the aphid facultative endosymbionts Rickettsia and Spiroplasma is expressed in multiple host genotypes and species and is not influenced by co-infection with another symbiont. J. Evol. Biol. 26 (2013), 2654–2661.
Łukasik, P., van Asch, M., Guo, H., Ferrari, J., Godfray, H.C.J., Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecol. Lett. 16 (2013), 214–218.
Łukasik, P., Guo, H., van Asch, M., Henry, L.M., Godfray, H.C.J., Ferrari, J., Horizontal transfer of facultative endosymbionts is limited by host relatedness. Evolution 69 (2015), 2757–2766.
Majerus, T., Der Schulenburg, V., Graf, J., Majerus, M., Hurst, G., Molecular identification of a male-killing agent in the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Insect Mol. Biol. 8 (1999), 551–555.
Manzano-Marín, A., Latorre, A., Settling down: the genome of Serratia symbiotica from the aphid Cinara tujafilina zooms in on the process of accommodation to a cooperative intracellular life. Genome Biol. Evol. 6 (2014), 1683–1698.
Martinez, A.J., Weldon, S.R., Oliver, K.M., Effects of parasitism on aphid nutritional and protective symbioses. Mol. Ecol. 23 (2014), 1594–1607.
McCutcheon, J.P., Moran, N.A., Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10 (2012), 13–26.
Mclean, A.H., Godfray, H.C., Evidence for specificity in symbiont-conferred protection against parasitoids. P. Roy. Soc. B-Biol. Sci., 282(1811), 2015.
Montllor, C.B., Maxmen, A., Purcell, A.H., Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol. Entomol. 27 (2002), 189–195.
Moran, N.A., Russell, J.A., Koga, R., Fukatsu, T., Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl. Environ. Microbiol. 71 (2005), 3302–3310.
Nováková, E., Hypša, V., Moran, N.A., Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol. 9 (2009), 1–14.
Nyabuga, F.N., Outreman, Y., Simon, J.C., Heckel, D.G., Weisser, W.W., Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study. Entomol. Exp. Appl. 136 (2010), 243–253.
Oliver, K.M., Russell, J.A., Moran, N.A., Hunter, M.S., Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl. Acad. Sci. 100 (2003), 1803–1807.
Oliver, K.M., Moran, N.A., Hunter, M.S., Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 12795–12800.
Oliver, K.M., Moran, N.A., Hunter, M.S., Costs and benefits of a superinfection of facultative symbionts in aphids. P. Roy. Soc. B-Biol. Sci. 273 (2006), 1273–1280.
Oliver, K.M., Campos, J., Moran, N.A., Hunter, M.S., Population dynamics of defensive symbionts in aphids. P. Roy. Soc. B-Biol. Sci. 275 (2008), 293–299.
Oliver, K.M., Degnan, P.H., Hunter, M.S., Moran, N.A., Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325 (2009), 992–994.
Oliver, K.M., Degnan, P.H., Burke, G.R., Moran, N.A., Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu. Rev. Entomol. 55 (2010), 247–266.
Oliver, K.M., Smith, A.H., Russell, J.A., Defensive symbiosis in the real world-advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct. Ecol. 28 (2014), 341–355.
Peccoud, J., Bonhomme, J., Mahéo, F., de la Huerta, M., Cosson, O., Simon, J.C., Inheritance patterns of secondary symbionts during sexual reproduction of pea aphid biotypes. Insect Sci. 21 (2014), 291–300.
Peccoud, J., Mahéo, F., de la Huerta, M., Laurence, C., Simon, J.C., Genetic characterisation of new host-specialised biotypes and novel associations with bacterial symbionts in the pea aphid complex. Insect Conserv. Diversity 8:5 (2015), 484–492.
Pérez-Brocal, V., Gil, R., Ramos, S., Lamelas, A., Postigo, M., Michelena, J.M., Silva, F.J., Moya, A., Latorre, A., A small microbial genome: the end of a long symbiotic relationship?. Science 314 (2006), 312–313.
Polin, S., Simon, J.C., Outreman, Y., An ecological cost associated with protective symbionts of aphids. Ecol. Evol. 4 (2014), 826–830.
Polin, S., Le Gallic, J.F., Simon, J.C., Tsuchida, T., Outreman, Y., Conditional reduction of predation risk associated with a facultative symbiont in an insect. PLoS One, 10, 2015, e0143728.
Rothacher, L., Ferrer-Suay, M., Vorburger, C., Bacterial endosymbionts protect aphids in the field and alter parasitoid community composition. Ecology 97:7 (2016), 1712–1723.
Rouchet, R., Vorburger, C., Experimental evolution of parasitoid infectivity on symbiont-protected hosts leads to the emergence of genotype specificity. Evolution 68 (2014), 1607–1616.
Roux, V., Bergoin, M., Lamaze, N., Raoult, D., Reassessment of the taxonomic position of Rickettsiella grylli. Int. J. Syst. Bacteriol. 47 (1997), 1255–1257.
Russell, J.A., Moran, N.A., Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host. Appl. Environ. Microbiol. 71 (2005), 7987–7994.
Russell, J.A., Moran, N.A., Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. P. Roy. Soc. B-Biol. Sci. 273 (2006), 603–610.
Russell, J.A., Latorre, A., Sabater-Muñoz, B., Moya, A., Moran, N.A., Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol. Ecol. 12 (2003), 1061–1075.
Russell, J.A., Weldon, S., Smith, A.H., Kim, K.L., Hu, Y., Łukasik, P., Doll, S., Anastopoulos, I., Novin, M., Oliver, K.M., Uncovering symbiont-driven genetic diversity across North American pea aphids. Mol. Ecol. 22 (2013), 2045–2059.
Sakurai, M., Koga, R., Tsuchida, T., Meng, X.Y., Fukatsu, T., 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 (2005), 4069–4075.
Sandström, J.P., Russell, J.A., White, J.P., Moran, N.A., Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol. Ecol. 10 (2001), 217–228.
Scarborough, C.L., Ferrari, J., Godfray, H.C.J., Aphid protected from pathogen by endosymbiont. Science, 310, 2005, 1781.
Schmid, M., Sieber, R., Zimmermann, Y.S., Vorburger, C., Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Funct. Ecol. 26 (2012), 207–215.
Shigenobu, S., Hattori, H.W.M., Sakaki, Y., Ishikawa, H., Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407 (2000), 81–86.
Simon, J.C., Sakurai, M., Bonhomme, J., Tsuchida, T., Koga, R., Fukatsu, T., Elimination of a specialised facultative symbiont does not affect the reproductive mode of its aphid host. Ecol. Entomol. 32 (2007), 296–301.
Simon, J.C., Boutin, S., Tsuchida, T., Koga, R., Le Gallic, J.-F., Frantz, A., Outreman, Y., Fukatsu, T., Facultative symbiont infections affect aphid reproduction. PLoS One, 6, 2011, e21831.
Smith, A.H., Łukasik, P., O'Connor, M.P., Lee, A., Mayo, G., Drott, M.T., Doll, S., Tuttle, R., Disciullo, R.A., Messina, A., Patterns, causes and consequences of defensive microbiome dynamics across multiple scales. Mol. Ecol. 24:5 (2015), 1135–1149.
Tsuchida, T., Koga, R., Shibao, H., Matsumoto, T., Fukatsu, T., Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol. Ecol. 11 (2002), 2123–2135.
Tsuchida, T., Koga, R., Fukatsu, T., Host plant specialization governed by facultative symbiont. Science, 303, 2004, 1989.
Tsuchida, T., Koga, R., Horikawa, M., Tsunoda, T., Maoka, T., Matsumoto, S., Simon, J.C., Fukatsu, T., Symbiotic bacterium modifies aphid body color. Science (New York, N.Y.) 330:6007 (2010), 1102–1104.
Tsuchida, T., Koga, R., Matsumoto, S., Fukatsu, T., Interspecific symbiont transfection confers a novel ecological trait to the recipient insect. Biol. Lett. 7 (2011), 245–248.
Vorburger, C., The evolutionary ecology of symbiont-conferred resistance to parasitoids in aphids. Insect Sci. 21 (2014), 251–264.
Vorburger, C., Gouskov, A., Only helpful when required: a longevity cost of harbouring defensive symbionts. J. Evol. Biol. 24 (2011), 1611–1617.
Vorburger, C., Gehrer, L., Rodriguez, P., A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol. Lett. 6 (2009), 109–111.
Vorburger, C., Sandrock, C., Gouskov, A., Castañeda, L.E., Ferrari, J., Genotypic variation and the role of defensive endosymbionts in an all-parthenogenetic host-parasitoid interaction. Evolution 63 (2009), 1439–1450.
Vorburger, C., Ganesanandamoorthy, P., Kwiatkowski, M., Comparing constitutive and induced costs of symbiont-conferred resistance to parasitoids in aphids. Ecol. Evol. 3 (2013), 706–713.
Wagner, S.M., Martinez, A.J., Ruan, Y.m., Kim, K.L., Lenhart, P.A., Dehnel, A.C., Oliver, K.M., White, J.A., Facultative endosymbionts mediate dietary breadth in a polyphagous herbivore. Funct. Ecol. 29 (2015), 1402–1410.
Wang, Z., Su, X.M., Wen, J., Jiang, L.Y., Qiao, G.X., Widespread infection and diverse infection patterns of Wolbachia in Chinese aphids. Insect Sci. 21 (2014), 313–325.
Werren, J.H., Zhang, W., Guo, L.R., Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. P. Roy. Soc. B-Biol. Sci. 261 (1995), 55–63.
van der Wilk, F., Dullemans, A.M., Verbeek, M., van den Heuvel, J.F.J.M., Isolation and characterization of APSE-1, a bacteriophage infecting the secondary endosymbiont of Acyrthosiphon pisum. Virology 262 (1999), 104–113.
Wulff, J.A., White, J.A., The endosymbiont Arsenophonus provides a general benefit to soybean aphid (Hemiptera: Aphididae) regardless of host plant resistance (Rag). Environ. Entomol. 44 (2015), 574–581.
Wulff, J.A., Buckman, K.A., Wu, K., Heimpel, G.E., White, J.A., The endosymbiont Arsenophonus is widespread in soybean aphid, Aphis glycines, but does not provide protection from parasitoids or a fungal pathogen. PLoS One, 8, 2013, e62145.
Xie, J., Vilchez, I., Mateos, M., Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS One, 5(8), 2010, e12149.
Zytynska, S.E., Meyer, S.T., Sturm, S., Ullmann, W., Mehrparvar, M., Weisser, W.W., Secondary bacterial symbiont community in aphids responds to plant diversity. Oecologia 180:3 (2016), 735–747.