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.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
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
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.
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.
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.
Brown J R, Phillips J R. 1991. Survival of Microplitis croceipes in Heliothis NPV-infected Heliothis virescens larvae. Southwest Entomol, 16: 25–30.
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.
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.
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.
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.
Cory J S, Myers J H. 2003. The ecology and evolution of insect baculoviruses. Ann Rev Ecol Evol Syst, 34: 239–272.
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.
Dwyer G, Elkinton J S. 1995. Host dispersal and the spatial spread of insect pathogens. Ecology, 76:1262–1275.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Guzo D, Stoltz D B. 1987. Observations on cellular immunity and parasitism in the tussock moth. J Insect Physiol, 33: 19–31.
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.
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.
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.
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.
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.
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.
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.
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.
Kukan B. 1999. Vertical transmission of nucleopolyhedrovirus in insects. J Invertebr Pathol, 74: 103–111.
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.
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.
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.
López M, Rojas R C, Vandame Ret al. 2002. Parasitoid-mediated transmission of an iridescent virus. J Invertebr Pathol, 80: 160–170.
Lou K, Pang Y. 2006. Spodoptera litura multicapsid nucleopolyhedrovirus inhibits Microplitis bicoloratus polydnavirus-induced host granulocytes apoptosis. J Insect Physiol, 52: 795–806.
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.
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.
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.
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.
Raimo B, Reardon R C, Podgwaite J D. 1977. Vectoring gypsy moth nuclear polyhedrosis virus by Apanteles elanoscelus (Hymenoptera:Braconidae). Entomophaga, 22: 207–216.
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.
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.
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.
Santiago-Alvarez C, Caballero P. 1990. Susceptibility of parasitized Agrotis segetum larvae to a granulosis virus. J Invertebr Pathol, 56: 128–131.
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.
Strand M R, Pech L L. 1995. Immunological basis for compatibility in parasitoid-host relationships. Ann Rev Entomol 40: 31–56.
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.
Stoltz D B, Guzo D, Cook D. 1986. Studies on polydnavirus transmission. Virology, 155: 120–131.
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.
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.
Washburn J O, Kirkpatrick B A, Volkman L E. 1996. Insect protection against viruses. Nature, 383: 767.
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.
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.
Webb R E, Strand M R. 2005. The biology and genomics of polydnaviruses. Compre Molecul Insect Sci, 6: 323–360.
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.
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.
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.
Rights and permissions
About this article
Cite this article
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
- Insect parasitoid