Host permissiveness to baculovirus influences time‐dependent immune responses and fitness costs

Insects possess specific immune responses to protect themselves from different types of pathogens. Activation of immune cascades can inflict significant developmental costs on the surviving host. To characterize infection kinetics in a surviving host that experiences baculovirus inoculation, it is crucial to determine the timing of immune responses. Here, we investigated time‐dependent immune responses and developmental costs elicited by inoculations from each of two wild‐type baculoviruses, Autographa californica multiple nucleopolyhedrovirus (AcMNPV) and Helicoverpa zea single nucleopolyhedrovirus (HzSNPV), in their common host H. zea. As H. zea is a semi‐permissive host of AcMNPV and fully permissive to HzSNPV, we hypothesized there are differential immune responses and fitness costs associated with resisting infection by each virus species. Newly molted 4th‐instar larvae that were inoculated with a low dose (LD15) of either virus showed significantly higher hemolymph FAD‐glucose dehydrogenase (GLD) activities compared to the corresponding control larvae. Hemolymph phenoloxidase (PO) activity, protein concentration and total hemocyte numbers were not increased, but instead were lower than in control larvae at some time points post‐inoculation. Larvae that survived either virus inoculation exhibited reduced pupal weight; survivors inoculated with AcMNPV grew slower than the control larvae, while survivors of HzSNPV pupated earlier than control larvae. Our results highlight the complexity of immune responses and fitness costs associated with combating different baculoviruses.

[1]  J. Cory,et al.  The impact of baculovirus challenge on immunity: the effect of dose and time after infection. , 2019, Journal of invertebrate pathology.

[2]  T. Williams,et al.  Covert Infection of Insects by Baculoviruses , 2017, Front. Microbiol..

[3]  J. Cory,et al.  Baculovirus-challenge and poor nutrition inflict within-generation fitness costs without triggering transgenerational immune priming. , 2016, Journal of invertebrate pathology.

[4]  R. Frutos,et al.  Insect pathogens as biological control agents: Back to the future. , 2015, Journal of invertebrate pathology.

[5]  J. Cory,et al.  Impact Of Environmental Variation On Host Performance Differs With Pathogen Identity: Implications For Host-Pathogen Interactions In A Changing Climate , 2015, Scientific Reports.

[6]  J. Cory,et al.  Impact of non‐pathogenic bacteria on insect disease resistance: importance of ecological context , 2015 .

[7]  J. Cory,et al.  Trade-offs between transgenerational transfer of nutritional stress tolerance and immune priming , 2015 .

[8]  J. Scholefield.  Baculovirus infection, host immunity and pathogen competition in the cabbage looper, Trichoplusia ni , 2015 .

[9]  J. Cory.  Insect virus transmission: different routes to persistence. , 2015, Current opinion in insect science.

[10]  S. Altizer,et al.  Dynamics of macronutrient self-medication and illness-induced anorexia in virally infected insects , 2013, The Journal of animal ecology.

[11]  J. Cory,et al.  Population Cycles in Forest Lepidoptera Revisited , 2013 .

[12]  J. Moreau,et al.  Immunocompetence increases with larval body size in a phytophagous moth , 2013 .

[13]  E. Hafen,et al.  The Hemolymph Proteome of Fed and Starved Drosophila Larvae , 2013, PloS one.

[14]  Hayato Yamada,et al.  Baculovirus genes modulating intracellular innate antiviral immunity of lepidopteran insect cells. , 2013, Virology.

[15]  T. Shimada,et al.  Silkworm plasmatocytes are more resistant than other hemocyte morphotypes to Bombyx mori nucleopolyhedrovirus infection. , 2013, Journal of invertebrate pathology.

[16]  J. Cory,et al.  The effect of food limitation on immunity factors and disease resistance in the western tent caterpillar , 2011, Oecologia.

[17]  K. Hoover,et al.  Contributions of immune responses to developmental resistance in Lymantria dispar challenged with baculovirus. , 2010, Journal of insect physiology.

[18]  M. Boots,et al.  Examining the relationship between hemolymph phenoloxidase and resistance to a DNA virus, Plodia interpunctella granulosis virus (PiGV). , 2010, Journal of insect physiology.

[19]  S. Thiem,et al.  Pathogenesis of Lymantria dispar multiple nucleopolyhedrovirus in L. dispar and mechanisms of developmental resistance. , 2010, The Journal of general virology.

[20]  J. Cory,et al.  Indirect plant-mediated effects on insect immunity and disease resistance in a tritrophic system , 2010 .

[21]  U. Shankar,et al.  Sub-lethal effects of SpltMNPV infection on developmental stages of Spodoptera litura (Lepidoptera: Noctuidae) , 2008 .

[22]  B. Sadd,et al.  Self-harm caused by an insect's innate immunity , 2006, Proceedings of the Royal Society B: Biological Sciences.

[23]  H. J. Popham,et al.  Journal of Insect Science: Vol. 2006 | Article 13 , 2008 .

[24]  N. Chejanovsky,et al.  Response of immunocompetent and immunosuppressed Spodoptera littoralis larvae to baculovirus infection. , 2006, The Journal of general virology.

[25]  N. Narang,et al.  Fluorescent brightener inhibits apoptosis in baculovirus-infected gypsy moth larval midgut cells in vitro , 2006 .

[26]  J. Cory,et al.  Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar , 2006, Proceedings of the Royal Society B: Biological Sciences.

[27]  J. Cho,et al.  Cellular immune responses and FAD‐glucose dehydrogenase activity of Mamestra brassicae (Lepidoptera: Noctuidae) challenged with three species of entomopathogenic fungi , 2005 .

[28]  A. Mcintosh,et al.  AcMNPV in permissive, semipermissive, and nonpermissive cell lines from arthropoda , 2005, In Vitro Cellular & Developmental Biology - Animal.

[29]  E. Deglow.  THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF PEST MANAGEMENT , 2004 .

[30]  J. Cory,et al.  The Ecology and Evolution of Insect Baculoviruses , 2003 .

[31]  S. Armitage,et al.  Examining costs of induced and constitutive immune investment in Tenebrio molitor , 2003, Journal of evolutionary biology.

[32]  L. Volkman,et al.  Pathogenesis of Autographa californica M nucleopolyhedrovirus in fifth instar Spodoptera frugiperda. , 2003, The Journal of general virology.

[33]  M. Strand,et al.  Insect hemocytes and their role in immunity. , 2002, Insect biochemistry and molecular biology.

[34]  M. Zuk,et al.  Immune Defense and Host Life History , 2002, The American Naturalist.

[35]  L. Volkman,et al.  Comparative pathogenesis of Helicoverpa zea S nucleopolyhedrovirus in noctuid larvae. , 2001, The Journal of general virology.

[36]  L. Volkman,et al.  Central Role of Hemocytes in Autographa californica M Nucleopolyhedrovirus Pathogenesis in Heliothis virescens and Helicoverpa zea , 2001, Journal of Virology.

[37]  J. Cory,et al.  Sublethal Nucleopolyhedrovirus Infection Effects on Female Pupal Weight, Egg Mass Size, and Vertical Transmission in Gypsy Moth (Lepidoptera: Lymantriidae) , 2000 .

[38]  Hoover,et al.  Midgut-based resistance of Heliothis virescens to baculovirus infection mediated by phytochemicals in cotton. , 2000, Journal of insect physiology.

[39]  L. Volkman,et al.  Co-infection of Manduca sexta larvae with polydnavirus from Cotesia congregata increases susceptibility to fatal infection by Autographa californica M Nucleopolyhedrovirus. , 2000, Journal of insect physiology.

[40]  R. Granados,et al.  Calcofluor disrupts the midgut defense system in insects. , 2000, Insect biochemistry and molecular biology.

[41]  R. Lochmiller,et al.  Trade‐offs in evolutionary immunology: just what is the cost of immunity? , 2000 .

[42]  D. Cox-Foster,et al.  Alteration in FAD-glucose dehydrogenase activity and hemocyte behavior contribute to initial disruption of Manduca sexta immune response to Cotesia congregata parasitoids. , 1999, Journal of insect physiology.

[43]  F. Moscardi,et al.  Assessment of the application of baculoviruses for control of Lepidoptera. , 1999, Annual review of entomology.

[44]  R. Granados,et al.  Observations on the presence of the peritrophic membrane in larval Trichoplusia ni and its role in limiting baculovirus infection. , 1998, Journal of invertebrate pathology.

[45]  J. Myers,et al.  Influence of Larval Age on the Lethal and Sublethal Effects of the Nucleopolyhedrovirus ofTrichoplusia niin the Cabbage Looper , 1998 .

[46]  L. Volkman,et al.  Evidence That the Stilbene-Derived Optical Brightener M2R EnhancesAutographa californicaM Nucleopolyhedrovirus Infection ofTrichoplusia niandHeliothis virescensby Preventing Sloughing of Infected Midgut Epithelial Cells , 1998 .

[47]  P. Wang,et al.  An intestinal mucin is the target substrate for a baculovirus enhancin. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[48]  L. Volkman,et al.  Developmental resistance in fourth instar Trichoplusia ni orally inoculated with Autographa californica M nuclear polyhedrosis virus. , 1995, Virology.

[49]  L. Kam-Morgan,et al.  The insect tracheal system: a conduit for the systemic spread of Autographa californica M nuclear polyhedrosis virus. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[50]  D. Cox-Foster,et al.  Induction and localization of FAD-glucose dehydrogenase (GLD) during encapsulation of abiotic implants in Manduca sexta larvae , 1994 .

[51]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.