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The parasitoid factor in the virulence and spread of lepidopteran baculoviruses

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Virologica Sinica

Abstract

Insect parasitoids and baculoviruses play important roles in the natural and strategic biological control of insects. The two parasites are frequent competitors within common hosts and much research has focused on the negative impact that baculoviral host infections have on parasitoids. This review summarizes the impacts that parasitoids may have on the virulence and spread of lepidopteran baculoviruses. By changing host behavior and development, parasitoids have been shown to decrease baculovirus virulence and productivity within parasitized baculovirus-susceptible hosts; however, studies of the tools used by hymenopteran parasitoids to overcome their hosts’immune systems, suggest that parasitoids may, in some cases, facilitate baculoviral infections in less susceptible hosts. Laboratory and field research have demonstrated that parasitoids can mechanically transmit baculoviruses between insects, and in this way, increase the efficacy of the viruses. Instances of new, more virulent isolates of baculoviruses have been recorded from specifically parasitoid-targeted hosts suggesting other possible benefits from the transmission or activation of baculoviruses by parasitoids.

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References

  1. Beckage N E. 1993. Games parasites play: the dynamic roles of proteases and peptides in the relationship between parasite and host. In: Parasites and pathogens of insects (Beckage N E, Thompson S N, Federici B A, ed.). San Diego CA: Academic Press, p25–57

    Google Scholar 

  2. Beegle C C, Oatman E R. 1974. Differential susceptibility of parasitized and nonparasitized larvae of Trichoplusia ni to a nuclear polyhedrosis virus. J Invertebr Pathol, 24: 188–195.

    Article  PubMed  CAS  Google Scholar 

  3. Beegle C C, Oatman E R. 1975. Effect of a nuclear polyhedrosis virus on the relationship between Trichoplusia ni (Lepidoptera: Noctuidae) and the parasite, Hyposoter exiguae (Hymenoptera: Ichneumonidae). J Invertebr Pathol, 25: 59–71.

    Article  PubMed  CAS  Google Scholar 

  4. Brown J R, Phillips J R, Yearian W C. 1989. Transmission of Heliothis NPV by Microplitis croceipes Cresson in Heliothis virescens. Southwest Entomol, 14: 139–146.

    Google Scholar 

  5. Brown J R, Phillips J R. 1991. Survival of Microplitis croceipes in Heliothis NPV-infected Heliothis virescens larvae. Southwest Entomol, 16: 25–30.

    Google Scholar 

  6. Brooks W M. 1993. Host-parasitoid-pathogen interactions. In: Parasites and Pathogens of Insects (Beckage N E, Thompson S N, Federici B A eds), Vol 2. San Diego: Academic Press, CA, p231–272.

    Google Scholar 

  7. Burden J P, Nixon C P, Hodgkinson A E,et al. 2003. Covert infections as a mechanism for long-term persistence of aculoviruses. Ecol Lett, 6: 524–531.

    Article  Google Scholar 

  8. Caballero P, Vargas-Osuna E, Santiago-Alvarez C. 1991. Parasitization of granulosis virus infected and noninfected Agrotis segetum larvae and the virus transmission by three hymenopteran parasitoids. Entomol Exper Appl, 58: 55–60.

    Article  Google Scholar 

  9. Cory J S. 2003. Ecological impacts of virus insecticides: host range and non-target organisms. In: Environmental Impacts of Microbial Insecticides (Hokkanen H M T, Hajek A E, ed.), Boston: Kluwer Academic. p73–92.

    Google Scholar 

  10. Cory J S, Myers J H. 2003. The ecology and evolution of insect baculoviruses. Ann Rev Ecol Evol Syst, 34: 239–272.

    Article  Google Scholar 

  11. Doucet D, Cusson M. 1996. Alteration of developmental rate and growth of Choristoneura fumiferana parasitized by Tranosema rostrale: role of the calyx fluid. Entomol Exp Appl, 81: 21B30.

    Article  Google Scholar 

  12. Dwyer G, Elkinton J S. 1995. Host dispersal and the spatial spread of insect pathogens. Ecology, 76:1262–1275.

    Article  Google Scholar 

  13. Edson K M, Vinson S B, Stoltz D B,et al. 1981. Virus in a parasitoid wasp: suppression of the cellular immune response in the parasitoid=s host. Science, 211: 582–583.

    Article  PubMed  CAS  Google Scholar 

  14. Eller F J, Boucias D G, Tumlinson J H. 1988. Interactions between Microplitis croceipes (Hymenoptera: Braconidae) and a nuclear polyhedrosis virus of Heliothis zea (Lepidoptera: Noctuidae). Environ Entomol, 17: 977–982.

    Google Scholar 

  15. Engelhard E K, Volkman L E. 1995. Developmental resistance in fourth instar Trichoplusia ni orally inoculated with Autographa californica M nuclear polyhedrosis virus. Virology, 209: 384–389.

    Article  PubMed  CAS  Google Scholar 

  16. Escribano A, Williams T, Goulson D,et al. 2000a. Parasitoid-pathogen-pest interactions of Chelonus insularis, Campoletis sonorensis, and a nucleopolyhedrovirus in Spodoptera frugiperda larvae. Biol Cont, 19: 265–273.

    Article  Google Scholar 

  17. Escribano A, Williams T, Goulson D,et al. 2000b. Effect of parasitism on a nucleopolyhedrovirus amplified in Spodoptera frugiperda larvae parasitized by Campoletis sonorensis. Entomol Exper Appl, 97(3): 257–264.

    Article  Google Scholar 

  18. Escribano A, Williams T, Goulson D,et al. 2001. Consequences of interspecific competition on the virulence and genetic composition of a nucleopolyhedrovirus in Spodoptera frugiperda larvae parasitized by Chelonus insularis. Biocontrol, 11: 649–662.

    Article  Google Scholar 

  19. Evans H F, Shapiro M. 1997. Viruses. In: Manual of Techniques in Insect Pathology-Biological Techniques (Lacey L A. ed.). San Diego: Academic Press, CA, p17–53.

    Chapter  Google Scholar 

  20. Feng G, Yu Q, Hu C,et al. 2007. Apoptosis is induced in the haemolymph and fat body of Spodoptera exigua larvae upon oral inoculation with Spodoptera litura nucleopolyhedrovirus. J Gen Virol, 88: 2185–2193.

    Article  PubMed  CAS  Google Scholar 

  21. Flexner J L, Lighthart B, Croft B A. 1986. The effects of microbial pesticides on non-target, beneficial arthropods. Agric Ecosystems Environ, 16: 203–254.

    Article  Google Scholar 

  22. Grasela J J, McIntosh A H, Shelby K S,et al. 2008. Isolation and characterization of a baculovirus associated with the insect parasitoid wasp, Cotesia marginiventris, or its host, Trichoplusia ni. J Insect Sci, 8: 42.

    Article  Google Scholar 

  23. Guzo D, Stoltz D B. 1987. Observations on cellular immunity and parasitism in the tussock moth. J Insect Physiol, 33: 19–31.

    Article  Google Scholar 

  24. Haas-Stapleton E J, Wahshurn J O, Volkman L E. 2005. Spodoptera frugiperda resistance to oral infection by Autographa californica multiple nucleopolyhedrovirus linked to aberrant occlusion-derived virus binding in the midgut. J Gen Virol, 86: 1349–1355.

    Article  PubMed  CAS  Google Scholar 

  25. Herniou E A., Olezewski J A, O=Reilly D R,et al. 2004. Ancient coevolution of baculoviruses and their insect hosts. J Virol, 78: 3244–3251.

    Article  PubMed  CAS  Google Scholar 

  26. Hochberg M E. 1991a. Intra-host interactions between Braconid endoparasitoid Apanteles glomeratus and a baculovirus for larvae of Pieris brassicae. J Anim Ecol, 60: 51–63.

    Article  Google Scholar 

  27. Hochberg M E. 1991b. Extra-host interactions between Braconid endoparasitoid Apanteles glomeratus and a baculovirus for larvae of Pieris brassicae. J Anim Ecol, 60: 65–77.

    Article  Google Scholar 

  28. Hodgson D J, Hitchman R B, Vanbergen A J,et al. 2004. Host ecology determines the relative fitness of virus genotypes in mixed-genotype neucleopolyhedrovirus infections. J Evol Biol, 17: 1018–1025.

    Article  PubMed  CAS  Google Scholar 

  29. Hotckin P G, Kaya H K. 1983. Pathological response of the parasitoid, Glyptapanteles militaris, to nuclear polyhedrosis virus-infected armyworm host. J Invertebr Pathol, 42: 51–61.

    Article  Google Scholar 

  30. Irabagon T A, Brooks W M. 1974. Interaction of Campoletis sonorensis and a nuclear polyhedrosis virus in larvae of Heliothis virescens. J Econ Entomol, 67: 229–331.

    PubMed  CAS  Google Scholar 

  31. Jehle J A, Blissard G W, Bonning B C,et al. 2006. On the classification and nomenclature of baculoviruses: A proposal for revision. Archives of Virol, 151: 1257–1266.

    Article  CAS  Google Scholar 

  32. Kukan B. 1999. Vertical transmission of nucleopolyhedrovirus in insects. J Invertebr Pathol, 74: 103–111.

    Article  PubMed  CAS  Google Scholar 

  33. Levin D B, Laing J E, Jacques R P. 1979. Transmission of granulosis virus by Apanteles glomeratus to its host Pieris rapae. J Invertebr Pathol, 34: 317–318.

    Article  Google Scholar 

  34. Levin D B, Laing J E, Jacques R P. 1981. Interactions between Apanteles glomeratus (Hymenoptera: Braconidae) and granulosis virus in Pieris rapae (Lepidoptera:Pieridae). Environ Entomol, 10: 65–68.

    Google Scholar 

  35. Levin D B, Laing J E, Jacques R P. 1983. Transmission of the granulosis virus of Pieris rapae (Lepidoptera: Pieridae) by the parasitoid Apanteles glomeratus (Hymenoptera: Braconidae). Environ Entomol, 12: 166–170.

    Google Scholar 

  36. López M, Rojas R C, Vandame Ret al. 2002. Parasitoid-mediated transmission of an iridescent virus. J Invertebr Pathol, 80: 160–170.

    Article  PubMed  Google Scholar 

  37. Lou K, Pang Y. 2006. Spodoptera litura multicapsid nucleopolyhedrovirus inhibits Microplitis bicoloratus polydnavirus-induced host granulocytes apoptosis. J Insect Physiol, 52: 795–806.

    Article  CAS  Google Scholar 

  38. Matthews H J, Smith I, Bell H A,et al. 2004. Interactions between the parasitoid Meteorus gyrator (Hymenoptera: Braconidae) and a granulovirus in Lacanobia oleracea (Lepidoptera: Noctuidae). Environ Entomol, 33: 949–957.

    Google Scholar 

  39. McCutchen B F, Herrmann R, Heinz K M,et al. 1996. Effects of recombinant baculoviruses on a nontarget endoparasitoid of Heliothis virescens. Biol Con, 6: 45–50.

    Article  Google Scholar 

  40. Murray D A, Monsour C J, Teakle R E,et al. 1995. Interactions between nuclear polyhedrosis virus and three larval parasitoids of Helioverpa armigera (Hübner) (Lepidoptera: Noctuidae). J Aust Ent Soc, 34: 319–322.

    Article  Google Scholar 

  41. Nusawardani T, Ruberson J, Obrycki J J,et al. 2005. Effects of a protease-expressing recombinant baculovirus insecticide on the parasitoid Cotesia marginiventris (Cresson). Biol Con, 35: 46B54.

    Google Scholar 

  42. Raimo B, Reardon R C, Podgwaite J D. 1977. Vectoring gypsy moth nuclear polyhedrosis virus by Apanteles elanoscelus (Hymenoptera:Braconidae). Entomophaga, 22: 207–216.

    Article  Google Scholar 

  43. Reardon R C, Podgwaite J D. 1976. Disease-parasitoid relationships in natural populations of Lymantria dispar (Lep.:Lymantridae) in the northeastern United States. Entomophaga, 21: 333–341.

    Article  Google Scholar 

  44. Rivkin H, Kroemer J A, Bronshtein A,et al. 2006. Response of immunocompetent and immunosuppressed Spodoptera ittoralis larvae to baculovirus infection. J Gen Virol, 87: 2217–2225.

    Article  PubMed  CAS  Google Scholar 

  45. Sait S M, Begon M, Thompson D J,et al. 1996. Parasitism of baculovirus-infected Plodia interpunctella by Venturia canescens and subsequent virus transmission. Funct Ecol, 10: 586–591.

    Article  Google Scholar 

  46. Santiago-Alvarez C, Caballero P. 1990. Susceptibility of parasitized Agrotis segetum larvae to a granulosis virus. J Invertebr Pathol, 56: 128–131.

    Article  Google Scholar 

  47. Smith O J, Hughes K M, Dunn P H,et al. 1956. A granulosis virus disease of the western grape leaf skeletonizer and its transmission. Can Entomol, 88: 507–515.

    Article  Google Scholar 

  48. Strand M R, Pech L L. 1995. Immunological basis for compatibility in parasitoid-host relationships. Ann Rev Entomol 40: 31–56.

    Article  CAS  Google Scholar 

  49. Stolz D B. 1993. The polydnavirus cycle. In: Parasites and pathogens of insects (Beckage N E, Thompson S N, Federici B A, ed.), CA,San Diego: Academic Press, p167–187.

    Google Scholar 

  50. Stoltz D B, Guzo D, Cook D. 1986. Studies on polydnavirus transmission. Virology, 155: 120–131.

    Article  PubMed  CAS  Google Scholar 

  51. Stoltz D, Makkay A. 2003. Overt viral disease induced from apparent latency following parasitization by the ichneumonid wasp, Hyposoter exiguae. J Insect Physiol, 49: 483–489.

    Article  PubMed  CAS  Google Scholar 

  52. Van Driesche R G, Bellows T S. 1996. Biology of arthropod parasitoids and predators. In: Biological control (Van Driesche R G, Bellows T S. ed.) New York: Chapman & Hall, p309–336.

    Google Scholar 

  53. Washburn J O, Kirkpatrick B A, Volkman L E. 1996. Insect protection against viruses. Nature, 383: 767.

    Article  CAS  Google Scholar 

  54. Washburn J O, Haas-Stapleton E J, Tan F F,et al. 2000. Co-infection of Manduca sexta larvae with polydnavirus from Cotesia congregata increases susceptibility to fatal infection by Autographa californica M Nucleopolyhedrovirus. J Insect Physiol, 46: 179–190.

    Article  PubMed  CAS  Google Scholar 

  55. Washburn J O, Trudeau D, Wong J F,et al. 2003. Early pathogenesis of Autographa californica multiple nucleopolyhedrovirus and Helicoverpa zea single nucleopolyhedrovirus in Heliothis virescens: a comparison of the >M=and >S= strategies for establishing fatal infection. J Gen Virol. 84: 343–351.

    Article  PubMed  CAS  Google Scholar 

  56. Webb R E, Strand M R. 2005. The biology and genomics of polydnaviruses. Compre Molecul Insect Sci, 6: 323–360.

    Article  CAS  Google Scholar 

  57. Wu M, Ye G, Zhu J,et al. 2008. Isolation and characterization of an immunosuppressive protein from venom of the pupa-specific endoparasitoid Pteromalus puparum. J Invertebr Pathol, 99: 186–191.

    Article  PubMed  CAS  Google Scholar 

  58. Young S Y, Yearian W C. 1989. Nuclear polyhedrosis virus transmission by Microplitis croceipes (Hymenoptera: Braconidae) adult females reared in infected Heliothis virescens (Lepidoptera: Noctuidae) larvae. J Entomol Sci, 24: 500–506.

    Google Scholar 

  59. Young S Y, Yearian W C. 1990. Transmission of nuclear polyhedrosis virus by theparasitoid Microplitis croceipes (Hymenoptera: Braconidae) to Heliothis virescens (Lepidoptera: Noctuidae) on soybean. Environ Entomol, 19: 251–256.

    Google Scholar 

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  1. Pacific Agri-Food Research Centre, 4200 Highway 97, Box 5000, Summerland, BC, V0H 1Z0, Canada

    J. E. Cossentine

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Cossentine, J.E. The parasitoid factor in the virulence and spread of lepidopteran baculoviruses. Virol. Sin. 24, 305–314 (2009). https://doi.org/10.1007/s12250-009-3049-9

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  • DOI: https://doi.org/10.1007/s12250-009-3049-9

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