Abstract
The conditions of entomopathogen persistence in a host-insect organism and the mechanisms of their conversion to the acute form of infection is one of the most important questions for an understanding of epizootics functioning. Here, we estimate the dynamics of the physiological parameters of the gypsy moth (Lymantria dispar L.) responsible for insect protection from antivirals under stress (starvation) and their correlation with the activation of the latent form of L. dispar, multiple nucleopolyhedrosis. We find that starvation leads to an increase in the dopamine concentration in the larval hemolymph and a decrease in the total number of hemocytes, which is associated with the high necrotic cell death. The number of viral carriers in the studied population and their activation level with starvation are estimated to be more than 70%. Polymerase chain reaction analysis showed an increase in the number of virus-positive individuals starting from the first day of starvation. At the same time, the nonspecific mortality of insects began only after 7 days of starvation, whereas the mortality from an activated virus began after 2–3 days of starvation. Thus, we show that at high insect-population density, a lack of food resources plays the leading role in the activation of the covert form of baculovirus infection. When analyzing the dynamics of physiological parameters, we assume that the conversion of a covert baculovirus form into an acute infection can be triggered by necrotic processes induced by starvation.
Similar content being viewed by others
REFERENCES
Bakhvalov, S.A., Insect viroses, in Patogeny nasekomykh: strukturnye i funktsional’nye aspekty (Pathogens of Insects: Structural and Functional Aspects), Glupov, V.V., Ed., Moscow: Kruglyi God, 2001, pp. 20–75.
Bakhvalov, S.A., Koltunov, E.V., and Martemyanov, V.V., Faktory i ekologicheskie mekhanizmy populyatsionnoi dinamiki lesnykh nasekomykh-fillofagov (Factors and Ecological Mechanisms of Population Dynamics of Forest Phyllophagous Insects), Novosibirsk: Sib. Otd., Ross. Akad. Nauk, 2010.
Blissard, G.W., Baculovirus-insect cell interactions, Cytotechnology, 1996, vol. 20, pp. 73–93.
Clem, R.J., The role of apoptosis in defense against baculovirus infection in insects, Curr. Topics Microbiol. Immunol., 2005, vol. 289, pp. 113–129.
Cory, J.S. and Myers, J.H., The ecology and evolution of insect baculoviruses, Annu. Rev. Ecol. Evol. Syst., 2003, vol. 34, pp. 239–272.
Cory, J.S. and Myers, J.H., Adaptation in an insect host-plant pathogen interaction, Ecol. Lett., 2004, vol. 7, pp. 632–639.
Fuxa, J.R., Sun, J.Z., Weidner, E.H., and LaMotte, L.R., Stressors and rearing diseases of Trichoplusia ni: evidence of vertical transmission of NPV and CPV, J. Invertebr. Pathol., 1999, vol. 74, pp. 149–155.
Gruntenko, N.E., Karpova, E.K., Alekseev, A.A., Chentsova, N.A., Saprykina, Z.V., et al., Effects of dopamine on juvenile hormone metabolism and fitness in Drosophila virilis, J. Insect Physiol., 2005, vol. 51, pp. 959–968.
Hillyer, J.F., Insect immunology and hematopoiesis, Dev. Comp. Immunol., 2016, vol. 58, pp. 102–118.
Ikeda, M., Yamada, H., Hamajima, R., and Kobayashi, M., Baculovirus genes modulating intracellular innate antiviral immunity of lepidopteran insect cells, Virology, 2013, vol. 435, pp. 1–13.
Ilyinykh, A.V., Vertical transmission of baculoviruses, Biol. Bull. (Moscow), 2019, vol. 46, no. 3, pp. 302–310.
Ilyinykh, A.V. and Polenogova, O.V., Demonstration of remote effect for vertical transmission of baculovirus based on example of gypsy moth, Lymantria dispar L. (Lepidoptera, Lymantriidae), Biol. Bull. Rev., 2013, vol. 3, no. 3, pp. 214–218.
International Committee Virus Taxonomy, 2013. https://talk.ictvonline.org/taxonomy/.
Kang, K.D., Kamita, S.G., Suzuki, K., and Seong, S.I., Effect of starvation upon baculovirus replication in larval Bombyx mori and Heliothis virescens, J. Invertebr. Pathol., 2011, vol. 106, pp. 205–210.
Kasianov, N.S., Belousova, I.A., Pavlushin, S.V., Dubovskiy, I.M., Podgwaite, J.D., et al., The activity of phenoloxidase in haemolymph plasma is not a predictor of Lymantria dispar resistance to its baculovirus, PLoS One., 2017, vol. 12, p. e0183940.
Kukan, B., Vertical transmission of nucleopolyhedrovirus in insects, J. Invertebr. Pathol., 1999, vol. 74, pp. 103–111.
Martemyanov, V.V., Dubovskiy, I.M., Belousova, I.A., Pavlushin, S.V., Domrachev, D.V., et al., Rapid induced resistance of silver birch affects both innate immunity and performance of gypsy moths: the role of plant chemical defenses, Arthropod-Plant Interact., 2012a, vol. 6, pp. 507–518.
Martemyanov, V.V., Dubovskiy, I.M., Rantala, M.J., Salminen, J.P., Belousova, I.A., et al., The effects of defoliation-induced delayed changes in silver birch foliar chemistry on gypsy moth fitness, immune response, and resistance to baculovirus infection, J. Chem. Ecol., 2012b, vol. 38, pp. 295–305.
Martemyanov, V.V., Pavlushin, S.V., Dubovskiy, I.M., Yushkova, Y.V., Morosov, S.V., et al., Asynchrony between host plant and insects-defoliator within a tritrophic system: the role of herbivore innate immunity, PLoS One., 2015, vol. 10, p. e0130988.
McNeil, J., Cox-Foster, D., Slavicek, J., and Hoover, K., Contributions of immune responses to developmental resistance in Lymantria dispar challenged with baculovirus, J. Insect Physiol., 2010a, vol. 56, pp. 1167–1177.
McNeil, J., Cox-Foster, D., Gardner, M., Slavicek, J., Thiem, S., and Hoover, K., Pathogenesis of Lymantria dispar multiple nucleopolyhedrovirus in L. dispar and mechanisms of developmental resistance, J. Gen. Virol., 2010b, vol. 91, pp. 1590–1600.
Myers, J.H., Cory, J.S., Ericsson, J.D., and Tseng, M.L., The effect of food limitation on immunity factors and disease resistance in the western tent caterpillar, Oecologia, 2011, vol. 167, pp. 647–655.
Pavlushin, S.V., Belousova, I.A., Chertkova, E.A., Kryukova, N.A., Glupov, V.V., and Martemyanov, V.V., The effect of population density of Lymantria dispar (Lepidoptera: Erebidae) on its fitness, physiology and activation of the covert nucleopolyhedrovirus, Eur. J. Entomol., 2019, vol. 116, pp. 85–91.
Reilly, J.R. and Hajek, A.E., Density-dependent resistance of the gypsy moth Lymantria dispar to its nucleopolyhedrovirus, and the consequences for population dynamics, Oecologia, 2008, vol. 154, pp. 691–701.
Trudeau, D., Washburn, J.O., and Volkman, L.E., Central role of hemocytes in Autographa californica M nucleopolyhedrovirus pathogenesis in Heliothis virescens and Helicoverpa zea, J. Virol., 2001, vol. 75, pp. 996–1003.
Washburn, J.O., Kirkpatrick, B.A., and Volkman, L.E., Insect protection against viruses, Nature, 1996, vol. 383, pp. 767–767.
Williams, T., Virto, C., Murillo, R., and Caballero, P., Covert infection of insects by baculoviruses, Front. Microbiol., 2017, vol. 8, p. 1337.
Yamada, H., Shibuya, M., Kobayashi, M., and Ikeda, M., Baculovirus Lymantria dispar multiple nucleopolyhedrovirus IAP2 and IAP3 do not suppress apoptosis, but trigger apoptosis of insect cells in a transient expression assay, Virus Genes, 2012, vol. 45, pp. 370–379.
Zhao, P.C., Lu, Z.Q., Strand, M.R., and Jiang, H.B., Antiviral, anti-parasitic, and cytotoxic effects of 5,6-dihydroxyindole (DHI), a reactive compound generated by phenoloxidase during insect immune response, Insect Biochem. Mol. Biol., 2011, vol. 41, pp. 645–652.
Funding
This work was supported by the Russian Foundation for Basic Research (project no. 15-04-08197a) and the Russian Science Foundation (project no. 17-46-07002, funding for PCR diagnostics of the gypsy-moth nuclear polyhedrosis virus).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests. The authors declare that they have no conflicts of interest.
Statement on the welfare of humans or animals. This article does not contain any studies involving animals performed by any of the authors.
Rights and permissions
About this article
Cite this article
Pavlushin, S.V., Belousova, I.A., Chertkova, E.A. et al. Effect of Starvation as a Population Stress-Factor on the Activation of Covert Baculovirus Infection in the Gypsy Moth. Biol Bull Rev 11, 86–91 (2021). https://doi.org/10.1134/S2079086421010047
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S2079086421010047