Abstract
Host plant consumption and pathogen infection commonly influence insect traits related to development and immunity, which are ultimately reflected in the behavior and physiology of the insect. Herein, we explored changes in the metabolome of a generalist insect herbivore, Vanessa cardui (Lepidoptera: Nymphalidae), in response to both dietary variation and pathogen infection in order to gain insight into tritrophic interactions for insect metabolism and immunity. Caterpillars were reared on two different host plants, Plantago lanceolata (Plantaginaceae) and Taraxacum officinale (Asteraceae) and subjected to a viral infection by Junonia coenia densovirus (JcDV), along with assays to determine the insect immune response and development. Richness and diversity of plant and caterpillar metabolites were evaluated using a liquid chromatography-mass spectrometry approach and showed that viral infection induced changes to the chemical content of V. cardui hemolymph and frass dependent upon host plant consumption. Overall, the immune response as measured by phenoloxidase (PO) enzymatic activity was higher in individuals feeding on P. lanceolata compared with those feeding on T. officinale. Additionally, infection with JcDV caused suppression of PO activity, which was not host plant dependent. We conclude that viral infection combined with host plant consumption creates a unique chemical environment, particularly within the insect hemolymph. Whether and how these metabolites contribute to defense against viral infection is an open question in chemical ecology.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The data sets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Beckage NE (2008) Insect Immunology. Academic Press, San Diego
Bruemmer A, Scholari F, Lopez-Ferber M et al (2005) Structure of an insect parvovirus (Junonia coenia densovirus) determined by cryo-electron microscopy. J Mol Biol 347:791–801. https://doi.org/10.1016/j.jmb.2005.02.009
Cory JS, Hoover K (2006) Plant-mediated effects in insect-pathogen interactions. Trends Ecol Evol 21:278–286
Defossez E, Pitteloud C, Descombes P et al (2021) Spatial and evolutionary predictability of phytochemical diversity. Proc Natl Acad Sci 118:1–7. https://doi.org/10.1073/pnas.2013344118
Dyer LA, Philbin CS, Ochsenrider KM et al (2018) Modern approaches to study plant–insect interactions in chemical ecology. Nat Rev Chem 2:50–64. https://doi.org/10.1038/s41570-018-0009-7
Eleftherianos I, Revenis C (2011) Role and importance of phenoloxidase in insect hemostasis. J Innate Immun 3:28–33. https://doi.org/10.1159/000321931
Gallon ME, Smilanich AM (2023) Effects of host plants on development and immunity of a generalist insect herbivore. J Chem Ecol 9:142–154. https://doi.org/10.1007/s10886-023-01410-9
Ghosh E, Paul RL, Ode PJ (2023) Plant species with higher chemical defences enhance herbivore cellular immunity with differential effectiveness against two parasitoid species. Funct Ecol 37:1492–1503. https://doi.org/10.1111/1365-2435.14292
Glassmire AE, Zehr LN, Wetzel WC (2020) Disentangling dimensions of phytochemical diversity: alpha and beta have contrasting effects on an insect herbivore. Ecology 101:1–12. https://doi.org/10.1002/ecy.3158
González-Santoyo I, Córdoba-Aguilar A (2012) Phenoloxidase: a key component of the insect immune system. Entomol Exp Appl 142:1–16. https://doi.org/10.1111/j.1570-7458.2011.01187.x
Jousse C, Dalle C, Abila A et al (2020) A combined LC-MS and NMR approach to reveal metabolic changes in the hemolymph of honeybees infected by the gut parasite Nosema ceranae. J Invertebr Pathol 176:1–8. https://doi.org/10.1016/j.jip.2020.107478
Kaplan I, Carrillo J, Garvey M, Ode PJ (2016) Indirect plant-parasitoid interactions mediated by changes in herbivore physiology. Curr Opin Insect Sci 14:112–119. https://doi.org/10.1016/j.cois.2016.03.004
Knolhoff LM, Heckel DG (2014) Behavioral assays for studies of host plant choice and adaptation in herbivorous insects. Annu Rev Entomol 59:263–278. https://doi.org/10.1146/annurev-ento-011613-161945
Lampert EC, Dyer LA, Bowers MD (2014) Dietary specialization and the effects of plant species on potential multitrophic interactions of three species of nymphaline caterpillars. Entomol Exp Appl 153:207–216. https://doi.org/10.1111/eea.12242
Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295–1309
Li T, Wang X, Qin S et al (2021) The hemolymph melanization response is related to defence against the AcMNPV infection in Bombyx mori. Arch Insect Biochem Physiol 108:e21764. https://doi.org/10.1002/arch.21764
Lü D, Xu P, Hou C et al (2019) Label-free LC-MS/MS proteomic analysis of the hemolymph of silkworm larvae infected with Beauveria bassiana. J Invertebr Pathol 166:1–8. https://doi.org/10.1016/j.jip.2019.107227
Marion ZH, Fordyce JA, Fitzpatrick BM (2015) Extending the concept of diversity partitioning to characterize phenotypic complexity. Am Nat 186:348–361. https://doi.org/10.1086/682369
Marmaras VJ, Charalambidis ND, Zervas CG (1996) Immune response in insects: the role of phenoloxidase in defense reactions in relation to melanization and sclerotization. Arch Insect Biochem Physiol 31:119–133. https://doi.org/10.1002/(SICI)1520-6327(1996)31:2%3c119::AID-ARCH1%3e3.0.CO;2-V
Mauck KE, Smyers E, De Moraes CM, Mescher MC (2015) Virus infection influences host plant interactions with non-vector herbivores and predators. Funct Ecol 29:662–673. https://doi.org/10.1111/1365-2435.12371
McKeegan KJ, Muchoney ND, Teglas MB et al (2024) Exploring spatial and temporal patterns of viral infection across populations of the Melissa blue butterfly. Ecol Entomol 49:54–66. https://doi.org/10.1111/een.13280
Mooney KA, Pratt RT, Singer MS (2012) The tri-trophic interactions hypothesis: interactive effects of host plant quality, diet breadth and natural enemies on herbivores. PLoS ONE 7:1–11. https://doi.org/10.1371/journal.pone.0034403
Morris EK, Caruso T, Buscot F et al (2014) Choosing and using diversity indices: insights for ecological applications from the German Biodiversity exploratories. Ecol Evol 4:3514–3524. https://doi.org/10.1002/ece3.1155
Muchoney ND, Bowers MD, Carper AL et al (2022) Use of an exotic host plant shifts immunity, chemical defense, and viral burden in wild populations of a specialist insect herbivore. Ecol Evol 12:1–15. https://doi.org/10.1002/ece3.8723
Muchoney ND, Bowers MD, Carper AL et al (2023) Use of an exotic host plant reduces viral burden in a native insect herbivore. Ecol Lett 26:425–436
Mutuel D, Ravallec M, Chabi B et al (2010) Pathogenesis of Junonia coenia densovirus in Spodoptera frugiperda: a route of infection that leads to hypoxia. Virology 403:137–144. https://doi.org/10.1016/j.virol.2010.04.003
Nakai M, Goto C, Shiotsuki T, Kunimi Y (2002) Granulovirus prevents pupation and retards development of Adoxophyes honmai larvae. Physiol Entomol 27:157–164. https://doi.org/10.1046/j.1365-3032.2002.00282.x
Nakai M, Kinjo H, Takatsuka J et al (2016) Entomopoxvirus infection induces changes in both juvenile hormone and ecdysteroid levels in larval Mythimna Separata. J Gen Virol 97:225–232. https://doi.org/10.1099/jgv.0.000325
O’Neill BF, Zangerl AR, Casteel CL et al (2008) Larval development and mortality of the painted lady butterfly, Vanessa cardui (Lepidoptera: Nymphalidae), on foliage grown under elevated carbon dioxide. Great Lakes Entomol 41:103–110
Ode PJ (2006) Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu Rev Entomol 51:163–185. https://doi.org/10.1146/annurev.ento.51.110104.151110
Ode PJ (2019) Plant toxins and parasitoid trophic ecology. Curr Opin Insect Sci 32:118–123
Ode PJ, Berenbaum MR, Zangerl AR et al (2004) Host plant, host plant chemistry and the polyembryonic parasitoid Copidosoma sosares: indirect effects in a tritrophic interaction. Oikos 104:388–400
Pan LL, Miao H, Wang Q et al (2021) Virus-induced phytohormone dynamics and their effects on plant–insect interactions. New Phytol 230:1305–1320. https://doi.org/10.1111/nph.17261
Peñaflor MFGV, Mauck KE, Alves KJ et al (2016) Effects of single and mixed infections of Bean pod mottle virus and Soybean mosaic virus on host-plant chemistry and host–vector interactions. Funct Ecol 30:1648–1659. https://doi.org/10.1111/1365-2435.12649
Philbin CS, Dyer LA, Jeffrey CS et al (2021) Structural and compositional dimensions of phytochemical diversity in the genus Piper reflect distinct ecological modes of action. J Ecol 1–11. https://doi.org/10.1111/1365-2745.13691
Poston FL, Hammond RB, Pedigo LP (1977) Growth and development of the painted lady on soybeans (Lepidoptera: Nymphalidae). J Kans Entomol Soc 50:31–36
Povey S, Cotter SC, Simpson SJ et al (2009) Can the protein costs of bacterial resistance be offset by altered feeding behaviour? J Anim Ecol 78:437–446. https://doi.org/10.1111/j.1365-2656.2008.01499.x
Putman RJ, Wratten SD (1984) Species diversity. Principles of Ecology. Springer Netherlands, Dordrecht, pp 320–337
Resnik JL, Smilanich AM (2020) The effect of phenoloxidase activity on survival is host plant dependent in virus-infected caterpillars. J Insect Sci 20:1–4. https://doi.org/10.1093/jisesa/ieaa116
Richards LA, Dyer LA, Forister ML et al (2015) Phytochemical diversity drives plant-insect community diversity. Proc Natl Acad Sci U S A 112:10973–10978. https://doi.org/10.1073/pnas.1504977112
Richards LA, Glassmire AE, Ochsenrider KM et al (2016) Phytochemical diversity and synergistic effects on herbivores. Phytochem Rev 15:1153–1166. https://doi.org/10.1007/s11101-016-9479-8
Rivers CF, Longworth JF (1972) A nonoccluded virus of Junonia coenia (Nymphalidae: Lepidoptera). J Invertebr Pathol 20:369–370
Rolff J, Reynolds SE (2009) Insect Infection and Immunity: evolution, ecology and mechanisms. Oxford University Press Inc., New York
Simpson SJ, Clissold FJ, Lihoreau M et al (2015) Recent advances in the integrative nutrition of arthropods. Annu Rev Entomol 60:16.1-16.19. https://doi.org/10.1146/annurev-ento-010814-020917
Slinn HL, Richards LA, Dyer LA et al (2018) Across multiple species, phytochemical diversity and herbivore diet breadth have cascading effects on herbivore immunity and parasitism in a tropical model system. Front Plant Sci 9:1–12. https://doi.org/10.3389/fpls.2018.00656
Smilanich AM, Dyer LA, Gentry GL (2009) The insect immune response and other putative defenses as effective predictors of parasitism. Ecology 90:1434–1440. https://doi.org/10.1890/08-1906.1
Smilanich AM, Langus TC, Doan L et al (2018) Host plant associated enhancement of immunity and survival in virus infected caterpillars. J Invertebr Pathol 151:102–112. https://doi.org/10.1016/j.jip.2017.11.006
Smilanich AM, Muchoney ND (2022) Host Plant effects on the Caterpillar Immune Response. In: Marquis RJ, Koptur S (eds) Caterpillars in the Middle. Springer, Cham, pp 449–484
Stefanescu C, Askew RR, Corbera J, Shaw MR (2012) Parasitism and migration in southern Palaearctic populations of the painted lady buttefly, Vanessa cardui (Lepidoptera: Nymphalidae). Eur J Entomol 109:85–94
Tian Z, Zhu L, Michaud JP et al (2023) Metabolic reprogramming of Helicoverpa armigera larvae by HearNPV facilitates viral replication and host immune suppression. Mol Ecol 32:1169–1182. https://doi.org/10.1111/mec.16817
Wang L-L, Swevers L, Rambouts C et al (2019a) A metabolomics approach to unravel cricket paralysis virus infection in silkworm BM5 cells. Viruses 11:1–18. https://doi.org/10.3390/v11090861
Wang X, Shao Z, Zhang Y et al (2019b) A 1H NMR based study of hemolymph metabonomics in different resistant silkworms, Bombyx mori (lepidotera), after BmNPV inoculation. J Insect Physiol 117:1–10. https://doi.org/10.1016/j.jinsphys.2019.103911
Wetzel WC, Whitehead SR (2020) The many dimensions of phytochemical diversity: linking theory to practice. Ecol Lett 23:16–32. https://doi.org/10.1111/ele.13422
Whittaker RH (1972) Evolution and measurement of species diversity. Taxon 21:213–251
Williams CB (1970) The migrations of the painted lady butterfly, Vanessa cardui (Nymphalidae), with special reference to North America. J Lepid Soc 24:157–175
Yoon S (2021) Novel immunological interactions as an overlooked aspect of global change- insights from the host range expansion of Lycaeides melissa. University of Nevada, Reno. PhD dissertation
Zhang Z, He H, Yan M et al (2022) Widely targeted analysis of metabolomic changes of Cucumis sativus induced by cucurbit chlorotic yellows virus. BMC Plant Biol 22:1–12. https://doi.org/10.1186/s12870-022-03555-3
Acknowledgements
The authors thank the Shared Instruments Laboratory (SIL) of the University of Nevada, Reno, and Dr. Stephen M. Spain and Janina Ruprecht for technical support.
Funding
This work was supported by the São Paulo Research Foundation - FAPESP (grant #2021/07911-5) and a grant from the National Science Foundation DEB 1929522.
Author information
Authors and Affiliations
Contributions
MEG and AMS contributed to the study conception and design. Data collection and analyses were performed by MEG. NDM contributed to the statistical analyses.The first draft of the manuscript was written by MEG. All authors commented on previous versions of the manuscript, as well as read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing Interests
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gallon, M.E., Muchoney, N.D. & Smilanich, A.M. Viral Infection Induces Changes to the Metabolome, Immune Response and Development of a Generalist Insect Herbivore. J Chem Ecol 50, 152–167 (2024). https://doi.org/10.1007/s10886-024-01472-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-024-01472-3