The evolutionary ecology of symbiont-conferred resistance to parasitoids in aphids

Insect Science

Volumn 21, Issue 3, 2014, Pages 251-264

  Vorburger, Christoph ^a,b  

^a ETH ZURICH   (Switzerland)

^b SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

Author keywords

Aphids; Biological control; Coevolution; Genotype genotype interaction; Hamiltonella defensa; Parasitoid; Resistance; Symbiosis

Indexed keywords

ANIMAL; APHID; ENVIRONMENTAL ASPECTS AND RELATED PHENOMENA; EVOLUTION; HOST PARASITE INTERACTION; INFECTION CONTROL; PARASITOLOGY; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; APHIDS; BIOLOGICAL EVOLUTION; COMMUNICABLE DISEASE CONTROL; ECOLOGICAL AND ENVIRONMENTAL PROCESSES; HOST-PARASITE INTERACTIONS; SYMBIOSIS;

EID: 84901195424     PISSN: 16729609     EISSN: 17447917     Source Type: Journal    
DOI: 10.1111/1744-7917.12067     Document Type: Article

References (101)

1. Agrawal, A. and Lively, C.M. (2002) Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evolutionary Ecology Research, 4, 79-90.
2. Baumann, P., Moran, N.A. and Baumann, L. (2000) Bacteriocyte-associated endosymbionts of insects. The Prokaryotes (ed. M. Dworkins ), pp. 1-55. Springer, New York.
3. Bensadia, F., Boudreault, S., Guay, J.F., Michaud, D. and Cloutier, C. (2006) Aphid clonal resistance to a parasitoid fails under heat stress. Journal of Insect Physiology, 52, 146-157.
4. Boivin, G., Hance, T. and Brodeur, J. (2012) Aphid parasitoids in biological control. Canadian Journal of Plant Science, 92, 1-12.
5. Brady, C.M. and White, J.A. (2013) Cowpea aphid (Aphis craccivora) associated with different host plants has different facultative endosymbionts. Ecological Entomology, 38, 433-437.
6. Buchner, P. (1965) Endosymbiosis of Animals with Plant Microorganisms. Interscience, New York. 909 pp.
7. Caspi-Fluger, A., Inbar, M., Mozes-Daube, N., Katzir, N., Portnoy, V., Belausov, E., Hunter, M.S. and Zchori-Fein, E. (2012) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proceedings of the Royal Society B-Biological Sciences, 279, 1791-1796.
8. Cayetano, L. and Vorburger, C. (2013) Genotype-by-genotype specificity remains robust to average temperature variation in an aphid/endosymbiont/parasitoid system. Journal of Evolutionary Biology, 26, 1603-1610.
9. Chen, D.Q. and Purcell, A.H. (1997) Occurrence and transmission of facultative endosymbionts in aphids. Current Microbiology, 34, 220-225.
10. Coeur d'acier, A., Jousselin, E., Martin, J.F. and Rasplus, J.Y. (2007) Phylogeny of the genus Aphis Linnaeus, 1758 (Homoptera: Aphididae) inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 42, 598-611.
11. Darby, A.C. and Douglas, A.E. (2003) Elucidation of the transmission patterns of an insect-borne bacterium. Applied and Environmental Microbiology, 69, 4403-4407.
12. Degnan, P.H. and Moran, N.A. (2008) Diverse phage-encoded toxins in a protective insect endosymbiont. Applied and Environmental Microbiology, 74, 6782-6791.
13. Dion, E., Polin, S.E., Simon, J.-C. and Outreman, Y. (2011a) Symbiont infection affects aphid defensive behaviours. Biology Letters, 7, 743-746.
14. Dion, E., Zele, F., Simon, J.-C. and Outreman, Y. (2011b) Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts. Journal of Evolutionary Biology, 24, 741-750.
15. Duron, O. and Hurst, G.D.D. (2013) Arthropods and inherited bacteria: from counting the symbionts to understanding how symbionts count. BMC Biology, 11, 45.
16. Erickson, D.M., Wood, E.A., Oliver, K.M., Billick, I. and Abbot, P. (2012) The effect of ants on the population dynamics of a protective symbiont of aphids, Hamiltonella defensa. Annals of the Entomological Society of America, 105, 447-453.
17. Ferrari, J., Darby, A.C., Daniell, T.J., Godfray, H.C.J. and Douglas, A.E. (2004) Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecological Entomology, 29, 60-65.
18. Ferrari, J., Müller, C.B., Kraaijeveld, A.R. and Godfray, H.C.J. (2001) Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution, 55, 1805-1814.
19. Ferrari, J., Scarborough, C.L. and 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.
20. Ferrari, J. and Vavre, F. (2011) Bacterial symbionts in insects or the story of communities affecting communities. Philosophical Transactions of the Royal Society B-Biological Sciences, 366, 1389-1400.
21. Ferrari, J., West, J.A., Via, S. and Godfray, H.C.J. (2012) Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution, 66, 375-390.
22. Flor, H.H. (1971) Current status of the gene-for-gene concept. Annual Review of Phytopathology, 9, 275-296.
23. Foster, S.P., Denholm, I. and Devonshire, A.L. (2000) The ups and downs of insecticide resistance in peach-potato aphids (Myzus persicae) in the UK. Crop Protection, 19, 873-879.
24. Foster, S.P., Denholm, I., Harling, Z.K., Moores, G.D. and Devonshire, A.L. (1998) Intensification of insecticide resistance in UK field populations of the peach-potato aphid, Myzus persicae (Hemiptera: Aphididae) in 1996. Bulletin of Entomological Research, 88, 127-130.
25. Foster, S.P., Devine, G. and Devonshire, A.L. (2007) Insecticide resistance. Aphids as Crop Pests (eds. H. Van Emden & R. Harringtons ), pp. 261-285. CAB International, Wallingford, UK.
26. Frank, S.A. (1993) Specificity versus detectable polymorphism in host-parasite genetics. Proceedings of the Royal Society B-Biological Sciences, 254, 191-197.
27. Frantz, A., Calcagno, V., Mieuzet, L., Plantegenest, M. and Simon, J.-C. (2009) Complex trait differentiation between host-populations of the pea aphid Acyrthosiphon pisum (Harris): implications for the evolution of ecological specialisation. Biological Journal of the Linnean Society, 97, 718-727.
28. Gehrer, L. and Vorburger, C. (2012) Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biology Letters, 8, 613-615.
29. Griffiths, D.C. (1960) Immunity of aphids to insect parasites. Nature, 187, 346.
30. Gross, P. (1993) Insect behavioral and morphological defenses against parasitoids. Annual Review of Entomology, 38, 251-273.
31. Guay, J.F., Boudreault, S., Michaud, D. and 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. Journal of Insect Physiology, 55, 919-926.
32. Hansen, A.K., Vorburger, C. and Moran, N.A. (2012) Genomic basis of endosymbiont-conferred protection against an insect parasitoid. Genome Research, 22, 106-114.
33. Henter, H.J. (1995) The potential for coevolution in a host-parasitoid system. II. Genetic variation within a population of wasps in the ability to parasitize an aphid host. Evolution, 49, 439-445.
34. Henter, H.J. and Via, S. (1995) The potential for coevolution in a host-parasitoid system. I. Genetic variation within an aphid population in susceptibility to a parasitic wasp. Evolution, 49, 427-438.
35. Herzog, J., Müller, C.B. and Vorburger, C. (2007) Strong parasitoid-mediated selection in experimental populations of aphids. Biology Letters, 3, 667-669.
36. Howard, R.S. and Lively, C.M. (2002) The Ratchet and the Red Queen: the maintenance of sex in parasites. Journal of Evolutionary Biology, 15, 648-656.
37. Jaenike, J., Polak, M., Fiskin, A., Helou, M. and Minhas, M. (2007) Interspecific transmission of endosymbiotic Spiroplasma by mites. Biology Letters, 3, 23-25.
38. Jones, E.O., White, A. and Boots, M. (2007) Interference and the persistence of vertically transmitted parasites. Journal of Theoretical Biology, 246, 10-17.
39. Jones, E.O., White, A. and Boots, M. (2011) The evolution of host protection by vertically transmitted parasites. Proceedings of the Royal Society B-Biological Sciences, 278, 863-870.
40. Judson, O.P. (1995) Preserving genes-a model of the maintenance of genetic variation in a metapopulation under frequency-dependent selection. Genetical Research, 65, 175-191.
41. Kraaijeveld, A.R., Ferrari, J. and Godfray, H.C.J. (2002) Costs of resistance in insect-parasite and insect-parasitoid interactions. Parasitology, 125, S71-S82.
42. Kwiatkowski, M., Engelstadter, J. and Vorburger, C. (2012) On genetic specificity in symbiont-mediated host-parasite coevolution. PLoS Computational Biology, 8, e1002633.
43. Kwiatkowski, M. and Vorburger, C. (2012) Modeling the ecology of symbiont-mediated protection against parasites. The American Naturalist, 179, 595-605.
44. Kyei-Poku, G.K., Floate, K.D., Benkel, B. and Goettel, M.S. (2003) Elimination of Wolbachia from Urolepis rufipes (Hymenoptera: Pteromalidae) with heat and antibiotic treatments: implications for host reproduction. Biocontrol Science and Technology, 13, 341-354.
45. Leonardo, T.E. (2004) Removal of a specialization-associated symbiont does not affect aphid fitness. Ecology Letters, 7, 461-468.
46. Le Ralec, A., Anselme, C., Outreman, Y., Poirié, M., van Baaren, J., Le Lann, C. and van Alphen, J.J.M. (2010) Evolutionary ecology of the interactions between aphids and their parasitoids. Comptes Rendus Biologies, 333, 554-565.
47. Li, S., Falabella, P., Giannantonio, S., Fanti, P., Battaglia, D., Digilio, M.C., Volkl, W., Sloggett, J.J., Weisser, W. and Pennacchio, F. (2002) Pea aphid clonal resistance to the endophagous parasitoid Aphidius ervi. Journal of Insect Physiology, 48, 971-980.
48. Lively, C.M., Clay, K., Wade, M.J. and Fuqua, C. (2005) Competitive co-existence of vertically and horizontally transmitted parasites. Evolutionary Ecology Research, 7, 1183-1190.
49. Lukasik, P., Dawid, M.A., Ferrari, J. and Godfray, H.C.J. (2013a) The diversity and fitness effects of infection with facultative endosymbionts in the grain aphid, Sitobion avenae. Oecologia, 173, 985-906.
50. Lukasik, P., van Asch, M., Guo, H.F., Ferrari, J. and Godfray, H.C.J. (2013b) Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecology Letters, 16, 214-218.
51. McLean, A.H.C., van Asch, M., Ferrari, J. and Godfray, H.C.J. (2011) Effects of bacterial secondary symbionts on host plant use in pea aphids. Proceedings of the Royal Society B-Biological Sciences, 278, 760-766.
52. Montllor, C.B., Maxmen, A. and Purcell, A.H. (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecological Entomology, 27, 189-195.
53. Moran, N.A. and Dunbar, H.E. (2006) Sexual acquisition of beneficial symbionts in aphids. Proceedings of the National Academy of Sciences of the United States of America, 103, 12803-12806.
54. Moran, N.A., Degnan, P.H., Santos, S.R., Dunbar, H.E. and Ochman, H. (2005a) The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proceedings of the National Academy of Sciences of the United States of America, 102, 16919-16926.
55. Moran, N.A., Russell, J.A., Koga, R. and Fukatsu, T. (2005b) Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Applied and Environmental Microbiology, 71, 3302-3310.
56. Müller, F.P. (1982) Das problem Aphis fabae. Zeitschrift für angewandte Entomologie, 94, 432-446.
57. Noyes, J.S. (2012) Universal Chalcidoidea Database. World Wide Web Electronic Publication. Accessed on 13 August 2013. http://www.nhm.ac.uk/chalcidoids.
58. Nyabuga, F.N., Outreman, Y., Simon, J.C., Heckel, D.G. and Weisser, W.W. (2010) Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study. Entomologia Experimentalis et Applicata, 136, 243-253.
59. Oliver, K.M., Campos, J., Moran, N.A. and Hunter, M.S. (2008) Population dynamics of defensive symbionts in aphids. Proceedings of the Royal Society B-Biological Sciences, 275, 293-299.
60. Oliver, K.M., Degnan, P.H., Burke, G.R. and Moran, N.A. (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annual Review of Entomology, 55, 247-266.
61. Oliver, K.M., Degnan, P.H., Hunter, M.S. and Moran, N.A. (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science, 325, 992-994.
62. Oliver, K.M., Moran, N.A. and Hunter, M.S. (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proceedings of the National Academy of Sciences of the United States of America, 102, 12795-12800.
63. Oliver, K.M., Moran, N.A. and Hunter, M.S. (2006) Costs and benefits of a superinfection of facultative symbionts in aphids. Proceedings of the Royal Society B-Biological Sciences, 273, 1273-1280.
64. Oliver, K.M., Noge, K., Huang, E.M., Campos, J.M., Becerra, J.X. and Hunter, M.S. (2012) Parasitic wasp responses to symbiont-based defense in aphids. BMC Biology, 10: 11.
65. Oliver, K.M., Russell, J.A., Moran, N.A. and Hunter, M.S. (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences of the United States of America, 100, 1803-1807.
66. Oliver, K.M., Smith, A.H. and Russell, J.A. (2013) Defensive symbiosis in the real world-advancing ecological studies of heritable, protective bacteria in aphids and beyond. Functional Ecology, DOI: 10.1111/1365-2435.12133.
67. Peccoud, J., Ollivier, A., Plantegenest, M. and Simon, J.-C. (2009) A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proceedings of the National Academy of Sciences of the United States of America, 106, 7495-7500.
68. Poirié, M. and Coustau, C. (2011) The evolutionary ecology of aphids' immunity. ISJ-Invertebrate Survival Journal, 8, 247-255.
69. Rouchet, R. (2012) Host-Parasitoid Coevolution: The Role of Parasitoid Adaptation to Endosymbiont-Mediated Defence in Aphids. Ph.D. Thesis. p. 102. ETH Zürich, Zürich, Switzerland.
70. Rouchet, R. and Vorburger, C. (2012) Strong specificity in the interaction between parasitoids and symbiont-protected hosts. Journal of Evolutionary Biology, 25, 2369-2375.
71. Russell, J.A., Latorre, A., Sabater-Muñoz, B., Moya, A. and Moran, N.A. (2003) Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Molecular Ecology, 12, 1061-1075.
72. Russell, J.A. and Moran, N.A. (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proceedings of the Royal Society B-Biological Sciences, 273, 603-610.
73. Russell, J.A., Weldon, S., Smith, A.H., Kim, K.L., Hu, Y., Lukasik, P., Doll, S., Anastopoulos, I., Novin, M. and Oliver, K.M. (2013) Uncovering symbiont-driven genetic diversity across North American pea aphids. Molecular Ecology, 22, 2045-2059.
74. Salathé, M., Kouyos, R.D. and Bonhoeffer, S. (2008) The state of affairs in the kingdom of the Red Queen. Trends in Ecology and Evolution, 23, 439-445.
75. Sandrock, C., Gouskov, A. and Vorburger, C. (2010) Ample genetic variation but no evidence for genotype specificity in an all-parthenogenetic host-parasitoid interaction. Journal of Evolutionary Biology, 23, 578-585.
76. Sandström, J.P., Russell, J.A., White, J.P. and Moran, N.A. (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Molecular Ecology, 10, 217-228.
77. Scarborough, C.L., Ferrari, J. and Godfray, H.C.J. (2005) Aphid protected from pathogen by endosymbiont. Science, 310, 1781-1781.
78. Schmid, M., Sieber, R., Zimmermann, Y.S. and Vorburger, C. (2012) Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Functional Ecology, 26, 207-215.
79. Schmid-Hempel, P. (2003) Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London Series B-Biological Sciences, 270, 357-366.
80. Schmidt, M.H., Lauer, A., Purtauf, T., Thies, C., Schaefer, M. and Tscharntke, T. (2003) Relative importance of predators and parasitoids for cereal aphid control. Proceedings of the Royal Society of London Series B-Biological Sciences, 270, 1905-1909.
81. Schmitz, A., Anselme, C., Ravallec, M., Rebuf, C., Simon, J.C., Gatti, J.L. and Poirié, M. (2012) The cellular immune response of the pea aphid to foreign intrusion and symbiotic challenge. PLoS ONE, 7, e42114.
82. Sigsgaard, L. (2002) A survey of aphids and aphid parasitoids in cereal fields in Denmark, and the parasitoids' role in biological control. Journal of Applied Entomology, 126, 101-107.
83. Simon, J.-C., Boutin, S., Tsuchida, T., Koga, R., Le Gallic, J.F., Frantz, A., Outreman, Y. and Fukatsu, T. (2011) Facultative symbiont infections affect aphid reproduction. PLoS ONE, 6, e21831.
84. Starý, P. (1988) Aphidiidae. Aphids: Their Biology, Natural Enemies, and Control. Vol. 2B (eds. A.K. Minks & P. Harrewijns ), pp. 171-184. Elsevier, Amsterdam.
85. Starý, P. (2006) Aphid Parasitoids of the Czech Republic (Hymenoptera: Braconidae, Aphidiinae). Academia, Praha.
86. Stouthamer, R., Breeuwer, J.A.J. and Hurst, G.D.D. (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annual Review of Microbiology, 53, 71-102.
87. Tsuchida, T., Koga, R. and Fukatsu, T. (2004) Host plant specialization governed by facultative symbiont. Science, 303, 1989-1989.
88. Tsuchida, T., Koga, R., Shibao, H., Matsumoto, T. and Fukatsu, T. (2002) Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Molecular Ecology, 11, 2123-2135.
89. van Der Wilk, F., Dullemans, A.M., Verbeek, M. and van Den Heuvel, J.F.J.M. (1999) Isolation and characterization of APSE-1, a bacteriophage infecting the secondary endosymbiont of Acyrthosiphon pisum. Virology, 262, 104-113.
90. van Lenteren, J.C., Drost, Y.C., van Roermund, H.J.W. and Posthuma-Doodeman, C.J.A.M. (1997) Aphelinid parasitoids as sustainable biological control agents in greenhouses. Journal of Applied Entomology, 121, 473-485.
91. van Opijnen, T. and Breeuwer, J.A.J. (1999) High temperatures eliminate Wolbachia, a cytoplasmic incompatibility inducing endosymbiont, from the two-spotted spider mite. Experimental and Applied Acarology, 23, 871-881.
92. Via, S. (1991) Specialized host plant performance of pea aphid clones is not altered by experience. Ecology, 72, 1420-1427.
93. von Burg, S., Ferrari, J., Müller, C.B. and Vorburger, C. (2008) Genetic variation and covariation of susceptibility to parasitoids in the aphid Myzus persicae-no evidence for trade-offs. Proceedings of the Royal Society B-Biological Sciences, 275, 1089-1094.
94. Vorburger, C., Ganesanandamoorthy, P. and Kwiatkowski, M. (2013) Comparing constitutive and induced costs of symbiont-conferred resistance to parasitoids in aphids. Ecology and Evolution, 3, 706-713.
95. Vorburger, C., Gehrer, L. and Rodriguez, P. (2010) A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biology Letters, 6, 109-111.
96. Vorburger, C. and Gouskov, A. (2011) Only helpful when required: a longevity cost of harbouring defensive symbionts. Journal of Evolutionary Biology, 24, 1611-1617.
97. Vorburger, C., Gouskov, A. and von Burg, S. (2008) Genetic covariation between effectiveness and cost of defence in aphids. Biology Letters, 4, 674-676.
98. Vorburger, C., Sandrock, C., Gouskov, A., Castañeda, L.E. and Ferrari, J. (2009) Genotypic variation and the role of defensive endosymbionts in an all-parthenogenetic host-parasitoid interaction. Evolution, 63, 1439-1450.
99. Weldon, S.R., Strand, M.R. and Oliver, K.M. (2013) Phage loss and the breakdown of a defensive symbiosis in aphids. Proceedings of the Royal Society B-Biological Sciences, 280, 20122103.
100. Werren, J.H., Baldo, L. and Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology, 6, 741-751.
101. Woolhouse, M.E.J., Webster, J.P., Domingo, E., Charlesworth, B. and Levin, B.R. (2002) Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nature Genetics, 32, 569-577.