1932

Abstract

Insect host–parasitoid interactions abound in nature and are characterized by a high degree of host specialization. In addition to their behavioral and immune defenses, many host species rely on heritable bacterial endosymbionts for defense against parasitoids. Studies on aphids and flies show that resistance conferred by symbionts can be very strong and highly specific, possibly as a result of variation in symbiont-produced toxins. I argue that defensive symbionts are therefore an important source of diversifying selection, promoting the evolution of host specialization by parasitoids. This is likely to affect the structure of host–parasitoid food webs. I consider potential changes in terms of food web complexity, although the nature of these effects will also be influenced by whether maternally transmitted symbionts have some capacity for lateral transfer. This is discussed in the light of available evidence for horizontal transmission routes. Finally, I propose that defensive mutualisms other than microbial endosymbionts may also exert diversifying selection on insect parasitoids.

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2022-01-07
2024-04-26
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Literature Cited

  1. 1. 
    Asplen MK, Bano N, Brady CM, Desneux N, Hopper KR et al. 2014. Specialisation of bacterial endosymbionts that protect aphids from parasitoids. Ecol. Entomol. 39:736–39
    [Google Scholar]
  2. 2. 
    Ballinger MJ, Gawryluk RMR, Perlman SJ. 2018. Toxin and genome evolution in a Drosophila defensive symbiosis. Genome Biol. Evol. 11:253–62
    [Google Scholar]
  3. 3. 
    Ballinger MJ, Perlman SJ. 2017. Generality of toxins in defensive symbiosis: ribosome-inactivating proteins and defense against parasitic wasps in Drosophila. PLOS Pathog 13:e1006431
    [Google Scholar]
  4. 4. 
    Barbour MA, Fortuna MA, Bascompte J, Nicholson JR, Julkunen-Tiitto R et al. 2016. Genetic specificity of a plant–insect food web: implications for linking genetic variation to network complexity. PNAS 113:2128–33
    [Google Scholar]
  5. 5. 
    Beckett SJ, Williams HTP. 2013. Coevolutionary diversification creates nested-modular structure in phage-bacteria interaction networks. Interface Focus 3:20130033
    [Google Scholar]
  6. 6. 
    Bersier LF, Banasek-Richter C, Cattin MF. 2002. Quantitative descriptors of food-web matrices. Ecology 83:2394–407
    [Google Scholar]
  7. 7. 
    Bolnick DI, Amarasekare P, Araujo MS, Burger R, Levine JM et al. 2011. Why intraspecific trait variation matters in community ecology. Trends Ecol. Evol. 26:183–92
    [Google Scholar]
  8. 8. 
    Bukovinszky T, van Veen FJF, Jongema Y, Dicke M 2008. Direct and indirect effects of resource quality on food web structure. Science 319:804–7
    [Google Scholar]
  9. 9. 
    Carton Y, Poirie M, Nappi AJ 2008. Insect immune resistance to parasitoids. Insect Sci 15:67–87
    [Google Scholar]
  10. 10. 
    Caspi-Fluger A, Inbar M, Mozes-Daube N, Katzir N, Portnoy V et al. 2012. Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc. R. Soc. B 279:1791–96
    [Google Scholar]
  11. 11. 
    Cayetano L, Rothacher L, Simon JC, Vorburger C. 2015. Cheaper is not always worse: Strongly protective isolates of a defensive symbiont are less costly to the aphid host. Proc. R. Soc. B 282:20142333
    [Google Scholar]
  12. 12. 
    Cayetano L, Vorburger C. 2013. Genotype-by-genotype specificity remains robust to average temperature variation in an aphid/endosymbiont/parasitoid system. J. Evol. Biol. 26:1603–10
    [Google Scholar]
  13. 13. 
    Cayetano L, Vorburger C. 2015. Symbiont-conferred protection against Hymenopteran parasitoids in aphids: How general is it?. Ecol. Entomol. 40:85–93
    [Google Scholar]
  14. 14. 
    Chen XA, Li S, Aksoy S 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
    [Google Scholar]
  15. 15. 
    Chrostek E, Pelz-Stelinski K, Hurst GDD, Hughes GL. 2017. Horizontal transmission of intracellular insect symbionts via plants. Front. Microbiol. 8:2237
    [Google Scholar]
  16. 16. 
    Combes C. 2005. The Art of Being a Parasite Chicago: Univ. Chicago Press
  17. 17. 
    Degnan PH, Moran NA. 2008. Diverse phage-encoded toxins in a protective insect endosymbiont. Appl. Environ. Microbiol. 74:6782–91
    [Google Scholar]
  18. 18. 
    Dennis AB, Patel V, Oliver KM, Vorburger C 2017. Parasitoid gene expression changes after adaptation to symbiont-protected hosts. Evolution 71:2599–617
    [Google Scholar]
  19. 19. 
    Dion E, Zélé F, Simon JC, Outreman Y. 2011. Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts. J. Evol. Biol. 24:741–50
    [Google Scholar]
  20. 20. 
    Duron O, Hurst GDD. 2013. Arthropods and inherited bacteria: from counting the symbionts to understanding how symbionts count. BMC Biol 11:45
    [Google Scholar]
  21. 21. 
    Dykstra HR, Weldon SR, Martinez AJ, White JA, Hopper KR et al. 2014. Factors limiting the spread of the protective symbiont Hamiltonella defensa in Aphis craccivora aphids. Appl. Environ. Microbiol. 80:5818–27
    [Google Scholar]
  22. 22. 
    Eubanks MD, Styrsky JD 2006. Ant-hemipteran mutualisms: keystone interactions that alter food web dynamics and influence plant fitness. Trophic and Guild in Biological Interactions Control J Brodeur, G Boivin 171–89 Berlin: Springer
    [Google Scholar]
  23. 23. 
    Fazalova V, Nevado B. 2020. Low spontaneous mutation rate and Pleistocene radiation of pea aphids. Mol. Biol. Evol. 37:2045–51
    [Google Scholar]
  24. 24. 
    Feng D-D, Michaud JP, Li P, Zhou Z-S, Xu Z-F. 2015. The native ant, Tapinoma melanocephalum, improves the survival of an invasive mealybug, Phenacoccus solenopsis, by defending it from parasitoids. Sci. Rep. 5:15691
    [Google Scholar]
  25. 25. 
    Ferrari J, Vavre F. 2011. Bacterial symbionts in insects or the story of communities affecting communities. Philos. Trans. R. Soc. B 366:1389–400
    [Google Scholar]
  26. 26. 
    Ferrari J, West JA, Via S, Godfray HCJ. 2012. Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution 66:375–90
    [Google Scholar]
  27. 27. 
    Florez LV, Scherlach K, Miller IJ, Rodrigues A, Kwan JC et al. 2018. An antifungal polyketide associated with horizontally acquired genes supports symbiont-mediated defense in Lagria villosa beetles. Nat. Commun. 9:10
    [Google Scholar]
  28. 28. 
    Forbes AA, Bagley RK, Beer MA, Hippee AC, Widmayer HA. 2018. Quantifying the unquantifiable: why Hymenoptera, not Coleoptera, is the most speciose animal order. BMC Ecol 18:11
    [Google Scholar]
  29. 29. 
    Futuyma DJ, Moreno G. 1988. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19:207–33
    [Google Scholar]
  30. 30. 
    Gehrer L, Vorburger C. 2012. Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol. Lett. 8:613–15
    [Google Scholar]
  31. 31. 
    Gerardo NM, Parker BJ 2014. Mechanisms of symbiont-conferred protection against natural enemies: an ecological and evolutionary framework. Curr. Opin. Insect Sci. 4:8–14
    [Google Scholar]
  32. 32. 
    Godfray HCJ. 1994. Parasitoids: Behavioral and Evolutionary Ecology Princeton, NJ: Princeton Univ. Press
  33. 33. 
    Gonella E, Pajoro M, Marzorati M, Crotti E, Mandrioli M et al. 2015. Plant-mediated interspecific horizontal transmission of an intracellular symbiont in insects. Sci. Rep. 5:15811
    [Google Scholar]
  34. 34. 
    Goto S, Anbutsu H, Fukatsu T. 2006. Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Appl. Environ. Microbiol. 72:4805–10
    [Google Scholar]
  35. 35. 
    Gross P. 1993. Insect behavioral and morphological defenses against parasitoids. Annu. Rev. Entomol. 38:251–73
    [Google Scholar]
  36. 36. 
    Guyomar C, Legeai F, Jousselin E, Mougel C, Lemaitre C, Simon J-C. 2018. Multi-scale characterization of symbiont diversity in the pea aphid complex through metagenomic approaches. Microbiome 6:181
    [Google Scholar]
  37. 37. 
    Hafer-Hahmann N, Vorburger C. 2020. Parasitoids as drivers of symbiont diversity in an insect host. Ecol. Lett. 23:1232–41
    [Google Scholar]
  38. 38. 
    Hamilton PT, Peng FN, Boulanger MJ, Perlman SJ. 2016. A ribosome-inactivating protein in a Drosophila defensive symbiont. PNAS 113:350–55
    [Google Scholar]
  39. 39. 
    Hansen AK, Vorburger C, Moran NA. 2012. Genomic basis of endosymbiont-conferred protection against an insect parasitoid. Genome Res 22:106–14
    [Google Scholar]
  40. 40. 
    Haselkorn TS, Cockburn SN, Hamilton PT, Perlman SJ, Jaenike J. 2013. Infectious adaptation: potential host range of a defensive endosymbiont in Drosophila. Evolution 67:934–45
    [Google Scholar]
  41. 41. 
    Hayashi M, Nakamuta K, Nomura M. 2015. Ants learn aphid species as mutualistic partners: Is the learning behavior species-specific?. J. Chem. Ecol. 41:1148–54
    [Google Scholar]
  42. 42. 
    Henry LM, Peccoud J, Simon J-C, Hadfield JD, Maiden JCM et al. 2013. Horizontally transmitted symbionts and host colonization of ecological niches. Curr. Biol. 23:1713–17
    [Google Scholar]
  43. 43. 
    Herren JK, Paredes JC, Schüpfer F, Arafah K, Bulet P, Lemaitre B. 2014. Insect endosymbiont proliferation is limited by lipid availability. eLife 3:e02964
    [Google Scholar]
  44. 44. 
    Hertäg C, Vorburger C. 2018. Defensive symbionts mediate species coexistence in phytophagous insects. Funct. Ecol. 32:1057–64
    [Google Scholar]
  45. 45. 
    Higashi CHV, Barton BT, Oliver KM 2020. Warmer nights offer no respite for a defensive mutualism. J. Anim. Ecol. 89:1895–905
    [Google Scholar]
  46. 46. 
    Hughes GL, Rasgon JL. 2014. Transinfection: a method to investigate Wolbachia-host interactions and control arthropod-borne disease. Insect Mol. Biol. 23:141–51
    [Google Scholar]
  47. 47. 
    Jaenike J. 1990. Host specialization in phytophagous insects. Annu. Rev. Ecol. Syst. 21:243–73
    [Google Scholar]
  48. 48. 
    Jaenike J, Polak M, Fiskin A, Helou M, Minhas M. 2007. Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol. Lett. 3:23–25
    [Google Scholar]
  49. 49. 
    Jones JE, Hurst GDD. 2020. Symbiont-mediated fly survival is independent of defensive symbiont genotype in the Drosophila melanogasterSpiroplasma–wasp interaction. J. Evol. Biol. 33:1625–33
    [Google Scholar]
  50. 50. 
    Jones JE, Hurst GDD. 2020. Symbiont-mediated protection varies with wasp genotype in the Drosophila melanogasterSpiroplasma interaction. Heredity 124:592–602
    [Google Scholar]
  51. 51. 
    Käch H, Mathé-Hubert H, Dennis AB, Vorburger C 2018. Rapid evolution of symbiont-mediated resistance compromises biological control of aphids by parasitoids. Evol. Appl. 11:220–30
    [Google Scholar]
  52. 52. 
    Kawecki TJ. 1998. Red Queen meets Santa Rosalia: arms races and the evolution of host specialization in organisms with parasitic lifestyles. Am. Nat. 152:635–51
    [Google Scholar]
  53. 53. 
    Kraaijeveld AR, Ferrari J, Godfray HCJ. 2002. Costs of resistance in insect-parasite and insect-parasitoid interactions. Parasitology 125:S71–82
    [Google Scholar]
  54. 54. 
    Kraft LJ, Kopco J, Harmon JP, Oliver KM. 2017. Aphid symbionts and endogenous resistance traits mediate competition between rival parasitoids. PLOS ONE 12:e0180729
    [Google Scholar]
  55. 55. 
    Kroiss J, Kaltenpoth M, Schneider B, Schwinger M-G, Hertweck C et al. 2010. Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat. Chem. Biol. 6:261–63
    [Google Scholar]
  56. 56. 
    Kwiatkowski M, Engelstädter J, Vorburger C. 2012. On genetic specificity in symbiont-mediated host-parasite coevolution. PLOS Comput. Biol. 8:e1002633
    [Google Scholar]
  57. 57. 
    Lang C, Menzel F 2011. Lasius niger ants discriminate aphids based on their cuticular hydrocarbons. Anim. Behav. 82:1245–54
    [Google Scholar]
  58. 58. 
    Li S-J, Ahmed MZ, Lv N, Shi P-Q, Wang X-M et al. 2017. Plant-mediated horizontal transmission of Wolbachia between whiteflies. ISME J 11:1019–28
    [Google Scholar]
  59. 59. 
    Liepert C, Dettner K. 1993. Recognition of aphid parasitoids by honeydew-collecting ants: the role of cuticular lipids in a chemical mimicry system. J. Chem. Ecol. 19:2143–53
    [Google Scholar]
  60. 60. 
    Liepert C, Dettner K. 1996. Role of cuticular hydrocarbons of aphid parasitoids in their relationship to aphid-attending ants. J. Chem. Ecol. 22:695–707
    [Google Scholar]
  61. 61. 
    Łukasik P, Guo H, van Asch M, Ferrari J, Godfray HCJ. 2013. 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. 26:2654–61
    [Google Scholar]
  62. 62. 
    Łukasik P, Guo HF, van Asch M, Henry LM, Godfray HCJ, Ferrari J. 2015. Horizontal transfer of facultative endosymbionts is limited by host relatedness. Evolution 69:2757–66
    [Google Scholar]
  63. 63. 
    Łukasik P, van Asch M, Guo HF, Ferrari J, Godfray HCJ. 2013. Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecol. Lett. 16:214–18
    [Google Scholar]
  64. 64. 
    Martinez AJ, Kim KL, Harmon JP, Oliver KM 2016. Specificity of multi-modal aphid defenses against two rival parasitoids. PLOS ONE 11:e0154670
    [Google Scholar]
  65. 65. 
    Mateos M, Winter L, Winter C, Higareda-Alvear VM, Martinez-Romero E, Xie J. 2016. Independent origins of resistance or susceptibility of parasitic wasps to a defensive symbiont. Ecol. Evol. 6:2679–87
    [Google Scholar]
  66. 66. 
    Mathé-Hubert H, Kaech H, Ganesanandamoorthy P, Vorburger C. 2019. Evolutionary costs and benefits of infection with diverse strains of Spiroplasma in pea aphids. Evolution 73:1466–81
    [Google Scholar]
  67. 67. 
    May RM. 1988. How many species are there on Earth?. Science 241:1441–49
    [Google Scholar]
  68. 68. 
    McLean AHC, Godfray HCJ. 2015. Evidence for specificity in symbiont-conferred protection against parasitoids. Proc. R. Soc. B 282:20150977
    [Google Scholar]
  69. 69. 
    McLean AHC, Godfray HCJ. 2017. The outcome of competition between two parasitoid species is influenced by a facultative symbiont of their aphid host. Funct. Ecol. 31:927–33
    [Google Scholar]
  70. 70. 
    McLean AHC, Hrček J, Parker BJ, Godfray HCJ. 2017. Cascading effects of herbivore protective symbionts on hyperparasitoids. Ecol. Entomol. 42:601–9
    [Google Scholar]
  71. 71. 
    McLean AHC, Hrček J, Parker BJ, Mathé-Hubert H, Kaech H et al. 2020. Multiple phenotypes conferred by a single insect symbiont are independent. Proc. R. Soc. B 287:20200562
    [Google Scholar]
  72. 72. 
    Monticelli LS, Nguyen LTH, Amiens-Desneux E, Luo C, Lavoir A-v et al. 2019. The preference–performance relationship as a means of classifying parasitoids according to their specialization degree. Evol. Appl. 12:1626–40
    [Google Scholar]
  73. 73. 
    Moran NA, Degnan PH, Santos SR, Dunbar HE, Ochman H. 2005. The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. PNAS 102:16919–26
    [Google Scholar]
  74. 74. 
    Moran NA, Dunbar HE. 2006. Sexual acquisition of beneficial symbionts in aphids. PNAS 103:12803–6
    [Google Scholar]
  75. 75. 
    Moran NA, Munson MA, Baumann P, Ishikawa H. 1993. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc. R. Soc. Lond. B 253:167–71
    [Google Scholar]
  76. 76. 
    Moran NA, Russell JA, Koga R, Fukatsu T 2005. Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl. Environ. Microbiol. 71:3302–10
    [Google Scholar]
  77. 77. 
    Morris RJ, Lewis OT, Godfray HCJ 2004. Experimental evidence for apparent competition in a tropical forest food web. Nature 428:310–13
    [Google Scholar]
  78. 78. 
    Moya-Laraño J. 2011. Genetic variation, predator-prey interactions and food web structure. Philos. Trans. R. Soc. B 366:1425–37
    [Google Scholar]
  79. 79. 
    Müller CB, Adriaanse ICT, Belshaw R, Godfray HCJ. 1999. The structure of an aphid-parasitoid community. J. Anim. Ecol. 68:346–70
    [Google Scholar]
  80. 80. 
    Nakabachi A, Ueoka R, Oshima K, Teta R, Mangoni A et al. 2013. Defensive bacteriome symbiont with a drastically reduced genome. Curr. Biol. 23:1478–84
    [Google Scholar]
  81. 81. 
    Niepoth N, Ellers J, Henry LM 2018. Symbiont interactions with non-native hosts limit the formation of new symbioses. BMC Evol. Biol. 18:27
    [Google Scholar]
  82. 82. 
    Oliver KM, Campos J, Moran NA, Hunter MS. 2008. Population dynamics of defensive symbionts in aphids. Proc. R. Soc. B 275:293–99
    [Google Scholar]
  83. 83. 
    Oliver KM, Degnan PH, Hunter MS, Moran NA. 2009. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325:992–94
    [Google Scholar]
  84. 84. 
    Oliver KM, Higashi CHV. 2019. Variations on a protective theme: Hamiltonella defensa infections in aphids variably impact parasitoid success. Curr. Opin. Insect Sci. 32:1–7
    [Google Scholar]
  85. 85. 
    Oliver KM, Moran NA, Hunter MS. 2005. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. PNAS 102:12795–800
    [Google Scholar]
  86. 86. 
    Oliver KM, Perlman SJ 2020. Toxin-mediated protection against natural enemies by insect defensive symbionts. Advances in Insect Physiology KM Oliver, JA Russell 277–316 Cambridge, MA: Academic
    [Google Scholar]
  87. 87. 
    Oliver KM, Russell JA, Moran NA, Hunter MS. 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. PNAS 100:1803–7
    [Google Scholar]
  88. 88. 
    Oliver KM, Smith AH, Russell JA. 2014. Defensive symbiosis in the real world: advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct. Ecol. 28:341–55
    [Google Scholar]
  89. 89. 
    Osaka R, Ichizono T, Kageyama D, Nomura M, Watada M. 2013. Natural variation in population densities and vertical transmission rates of a Spiroplasma endosymbiont in Drosophila hydei. Symbiosis 60:73–78
    [Google Scholar]
  90. 90. 
    Osaka R, Watada M, Kageyama D, Nomura M 2010. Population dynamics of a maternally-transmitted Spiroplasma infection in Drosophila hydei. Symbiosis 52:41–45
    [Google Scholar]
  91. 91. 
    Paredes JC, Herren JK, Schüpfer F, Lemaitre B. 2016. The role of lipid competition for endosymbiont-mediated protection against parasitoid wasps in Drosophila. mBio 7:e01006-16
    [Google Scholar]
  92. 92. 
    Parker BJ, Hrček J, McLean AHC, Godfray HCJ. 2017. Genotype specificity among hosts, pathogens, and beneficial microbes influences the strength of symbiont-mediated protection. Evolution 71:1222–31
    [Google Scholar]
  93. 93. 
    Peccoud J, Bonhomme J, Maheo F, de la Huerta M, Cosson O, Simon JC 2014. Inheritance patterns of secondary symbionts during sexual reproduction of pea aphid biotypes. Insect Sci 21:291–300
    [Google Scholar]
  94. 94. 
    Peccoud J, Ollivier A, Plantegenest M, Simon JC 2009. A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. PNAS 106:7495–500
    [Google Scholar]
  95. 95. 
    Peccoud J, Simon JC, McLaughlin HJ, Moran NA. 2009. Post-Pleistocene radiation of the pea aphid complex revealed by rapidly evolving endosymbionts. PNAS 106:16315–20
    [Google Scholar]
  96. 96. 
    Piel J. 2002. A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of Paederus beetles. PNAS 99:14002–7
    [Google Scholar]
  97. 97. 
    Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J et al. 2002. The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annu. Rev. Entomol. 47:733–71
    [Google Scholar]
  98. 98. 
    Pierce NE, Easteal S. 1986. The selective advantage of attendant ants for the larvae of a Lycaenid butterfly, Glaucopsyche lygdamus. J. Anim. Ecol. 55:451–62
    [Google Scholar]
  99. 99. 
    Poisot T, Stouffer DB, Gravel D. 2015. Beyond species: why ecological interaction networks vary through space and time. Oikos 124:243–51
    [Google Scholar]
  100. 100. 
    Pons I, Renoz F, Noel C, Hance T 2019. Circulation of the cultivable symbiont Serratia symbiotica in aphids is mediated by plants. Front. Microbiol. 10:13
    [Google Scholar]
  101. 101. 
    Raboudi F, Mezghani M, Makni H, Marrakchi M, Rouault JD, Makni M. 2005. Aphid species identification using cuticular hydrocarbons and cytochrome b gene sequences. J. Appl. Entomol. 129:75–80
    [Google Scholar]
  102. 102. 
    Raffard A, Santoul F, Cucherousset J, Blanchet S 2019. The community and ecosystem consequences of intraspecific diversity: a meta-analysis. Biol. Rev. 94:648–61
    [Google Scholar]
  103. 103. 
    Rock DI, Smith AH, Joffe J, Albertus A, Wong N et al. 2018. Context-dependent vertical transmission shapes strong endosymbiont community structure in the pea aphid, Acyrthosiphon pisum. Mol. Ecol. 27:2039–56
    [Google Scholar]
  104. 104. 
    Rolff J, Siva-Jothy M. 2003. Invertebrate ecological immunology. Science 301:472–75
    [Google Scholar]
  105. 105. 
    Rothacher L, Ferrer-Suay M, Vorburger C. 2016. Bacterial endosymbionts protect aphids in the field and alter parasitoid community composition. Ecology 97:1712–23
    [Google Scholar]
  106. 106. 
    Rouchet R, Vorburger C. 2012. Strong specificity in the interaction between parasitoids and symbiont-protected hosts. J. Evol. Biol. 25:2369–75
    [Google Scholar]
  107. 107. 
    Rouchet R, Vorburger C. 2014. Experimental evolution of parasitoid infectivity on symbiont-protected hosts leads to the emergence of genotype-specificity. Evolution 68:1607–16
    [Google Scholar]
  108. 108. 
    Rouïl J, Jousselin E, Coeur d'acier A, Cruaud C, Manzano-Marín A 2020. The protector within: Comparative genomics of APSE phages across aphids reveals rampant recombination and diverse toxin arsenals. Genome Biol. Evol. 12:878–89
    [Google Scholar]
  109. 109. 
    Russell JA, Latorre A, Sabater-Muñoz B, Moya A, Moran NA 2003. Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol. Ecol. 12:1061–75
    [Google Scholar]
  110. 110. 
    Russell JA, Weldon S, Smith AH, Kim KL, Hu Y et al. 2013. Uncovering symbiont-driven genetic diversity across North American pea aphids. Mol. Ecol. 22:2045–59
    [Google Scholar]
  111. 111. 
    Sadd BM, Schmid-Hempel P. 2009. Principles of ecological immunology. Evol. Appl. 2:113–21
    [Google Scholar]
  112. 112. 
    Sakata I, Hayashi M, Nakamuta K. 2017. Tetramorium tsushimae ants use methyl branched hydrocarbons of aphids for partner recognition. J. Chem. Ecol. 43:966–70
    [Google Scholar]
  113. 113. 
    Sanders D, Kehoe R, van Veen FJF, McLean A, Godfray HCJ et al. 2016. Defensive insect symbiont leads to cascading extinctions and community collapse. Ecol. Lett. 19:789–99
    [Google Scholar]
  114. 114. 
    Sandrock C, Gouskov A, Vorburger C 2010. Ample genetic variation but no evidence for genotype specificity in an all-parthenogenetic host-parasitoid interaction. J. Evol. Biol. 23:578–85
    [Google Scholar]
  115. 115. 
    Sandrock C, Schirrmeister BE, Vorburger C. 2011. Evolution of reproductive mode variation and host associations in a sexual-asexual complex of aphid parasitoids. BMC Evol. Biol. 11:20
    [Google Scholar]
  116. 116. 
    Sandrock C, Vorburger C. 2011. Single-locus recessive inheritance of asexual reproduction in a parasitoid wasp. Curr. Biol. 21:433–37
    [Google Scholar]
  117. 117. 
    Schmid M, Sieber R, Zimmermann YS, Vorburger C. 2012. Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Funct. Ecol. 26:207–15
    [Google Scholar]
  118. 118. 
    Simon JC, Rispe C, Sunnucks P. 2002. Ecology and evolution of sex in aphids. Trends Ecol. Evol. 17:34–39
    [Google Scholar]
  119. 119. 
    Sint D, Traugott M. 2016. Food Web Designer: a flexible tool to visualize interaction networks. J. Pest Sci. 89:1–5
    [Google Scholar]
  120. 120. 
    Smith AH, Lukasik P, O'Connor MP, Lee A, Mayo G et al. 2015. Patterns, causes and consequences of defensive microbiome dynamics across multiple scales. Mol. Ecol. 24:1135–49
    [Google Scholar]
  121. 121. 
    Smith MA, Rodriguez JJ, Whitfield JB, Deans AR, Janzen DH et al. 2008. Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. PNAS 105:12359–64
    [Google Scholar]
  122. 122. 
    Smith MA, Wood DM, Janzen DH, Hallwachs W, Hebert PDN 2007. DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists. PNAS 104:4967–72
    [Google Scholar]
  123. 123. 
    Stadler B, Dixon AFG. 2005. Ecology and evolution of aphid-ant interactions. Annu. Rev. Ecol. Evol. Syst. 36:345–72
    [Google Scholar]
  124. 124. 
    Tomanović Ž, Mitrović M, Petrović A, Kavallieratos NG, Žikić V et al. 2018. Revision of the European Lysiphlebus species (Hymenoptera: Braconidae: Aphidiinae) on the basis of COI and 28SD2 molecular markers and morphology. Arthropod Syst. Phylogeny 76:179–213
    [Google Scholar]
  125. 125. 
    van der Wilk F, Dullemans AM, Verbeek M, van den Heuvel JFJM. 1999. Isolation and characterization of APSE-1, a bacteriophage infecting the secondary endosymbiont of Acyrthosiphon pisum. Virology 262:104–13
    [Google Scholar]
  126. 126. 
    van Veen FJF, Morris RJ, Godfray HCJ 2006. Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annu. Rev. Entomol. 51:187–208
    [Google Scholar]
  127. 127. 
    Vavre F, Fleury F, Lepetit D, Fouillet P, Boulétreau M 1999. Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol. Biol. Evol. 16:1711–23
    [Google Scholar]
  128. 128. 
    Vorburger C. 2014. The evolutionary ecology of symbiont-conferred resistance to parasitoids in aphids. Insect Sci 21:251–64
    [Google Scholar]
  129. 129. 
    Vorburger C, Gehrer L, Rodriguez P. 2010. A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol. Lett. 6:109–11
    [Google Scholar]
  130. 130. 
    Vorburger C, Gouskov A. 2011. Only helpful when required: a longevity cost of harbouring defensive symbionts. J. Evol. Biol. 24:1611–17
    [Google Scholar]
  131. 131. 
    Vorburger C, Perlman SJ. 2018. The role of defensive symbionts in host–parasite coevolution. Biol. Rev. 93:1747–64
    [Google Scholar]
  132. 132. 
    Vorburger C, Rouchet R. 2016. Are aphid parasitoids locally adapted to the prevalence of defensive symbionts in their hosts?. BMC Evol. Biol. 16:271
    [Google Scholar]
  133. 133. 
    Vorburger C, Sandrock C, Gouskov A, Castañeda LE, Ferrari J. 2009. Genotypic variation and the role of defensive endosymbionts in an all-parthenogenetic host-parasitoid interaction. Evolution 63:1439–50
    [Google Scholar]
  134. 134. 
    Vorburger C, Siegrist G, Rhyner N. 2017. Faithful vertical transmission but ineffective horizontal transmission of bacterial endosymbionts during sexual reproduction of the black bean aphid, Aphis fabae. Ecol. Entomol. 42:202–9
    [Google Scholar]
  135. 135. 
    Werren JH, Zhang W, Guo LR. 1995. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc. R. Soc. Lond. B 261:55–63
    [Google Scholar]
  136. 136. 
    Windsor DA. 1998. Most of the species on Earth are parasites. Int. J. Parasitol. 28:1939–41
    [Google Scholar]
  137. 137. 
    Xie J, Butler S, Sanchez G, Mateos M. 2014. Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps. Heredity 112:399–408
    [Google Scholar]
  138. 138. 
    Xie JL, Vilchez I, Mateos M. 2010. Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLOS ONE 5:e12149
    [Google Scholar]
  139. 139. 
    Xie JL, Winter C, Winter L, Mateos M 2015. Rapid spread of the defensive endosymbiont Spiroplasma in Drosophila hydei under high parasitoid wasp pressure. FEMS Microbiol. Ecol. 91:1–11
    [Google Scholar]
  140. 140. 
    Xue X, Li S-J, Ahmed MZ, De Barro PJ, Ren S-X, Qiu B-L. 2012. Inactivation of Wolbachia reveals its biological roles in whitefly host. PLOS ONE 7:e48148
    [Google Scholar]
  141. 141. 
    Ye Z, Vollhardt IMG, Girtler S, Wallinger C, Tomanovic Z, Traugott M 2017. An effective molecular approach for assessing cereal aphid-parasitoid-endosymbiont networks. Sci. Rep. 7:3138
    [Google Scholar]
  142. 142. 
    Ye ZP, Vollhardt IMG, Parth N, Rubbmark O, Traugott M 2018. Facultative bacterial endosymbionts shape parasitoid food webs in natural host populations: a correlative analysis. J. Anim. Ecol. 87:1440–51
    [Google Scholar]
  143. 143. 
    Zytynska SE, Weisser WW. 2016. The natural occurrence of secondary bacterial symbionts in aphids. Ecol. Entomol. 41:13–26
    [Google Scholar]
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