Abstract
Plants and herbivores have co-existed for millions of years, leading to complex relationships. Recent studies of plant–insect interactions have focused on important implications of plant defenses on insect immunity. Plants express defenses against herbivores through the production of toxic secondary chemicals, which may alter immune responses. The monarch butterfly, Danaus plexippus, has been shown to use toxic secondary chemicals (cardenolides) of milkweed plants (Asclepias spp.) to help reduce parasitism. However, little is known about the interaction of these secondary chemicals on the insect immune response. Therefore, we reared monarch caterpillars on five different milkweed species with varying cardenolide levels and measured their immune response to an immune stimulus. In particular, we measured a humoral immune response, in the form of anti-microbial growth, following exposure to lipopolysaccharide (LPS), a bacterial cell wall component. We show that the immune challenge caused a strong humoral immune response in monarch caterpillars. However, the response did not vary with milkweed species and cardenolide concentrations. Our results suggest that the toxins of milkweeds do not directly impact the humoral immune response.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article.
References
Agrawal AA, Petschenka G, Bingham RA, Weber MG, Rasmann S (2012) Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol 194(1):28–45
Altizer SM, Oberhauser KS, Geurts KA (2004) Transmission of the protozoan parasite Ophyocystis elektroscirrha in monarch butterfly populations: implications for prevalence and population-level impacts: biology and conservation. The monarch butterfly biology and conservation. Cornell Univeristy Press, New York, pp 203–218
Cory JS, Hoover K (2006) Plant-mediated effects in insect-pathogen interactions. Trends Ecol Evol 21(5):278–286
Gowler CD, Leon KE, Hunter MD, de Roode JC (2015) Secondary defense chemicals in milkweed reduce parasite infection in monarch butterflies Danaus plexippus. J Chem Ecol 41(6):520–523
Harris EV, de Roode JC, Gerardo NM (2019) Diet-microbiome-disease: investigating diet’s influence on infectious disease resistance through alteration of the gut microbiome. PLoS Pathog 15(10):e1007891
Laurentz M, Reudler JH, Mappes J, Friman V, Ikonen S, Lindstedt C (2012) Diet quality can play a critical role in defense efficacy against parasitoids and pathogens in the Glanville fritillary (Melitaea cinxia). J Chem Ecol 38(1):116–125
Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290(5494):1166–1168
Petschenka G, Agrawal AA (2016) How herbivores coopt plant defenses: natural selection, specialization, and sequestration. Curr Opin Insect Sci 14:17–24
Smilanich AM, Dyer LA, Chambers JQ, Bowers MD (2009) Immunological cost of chemical defence and the evolution of herbivore diet breadth. Ecol Lett 12(7):612–621
Sternberg ED, Lefevre T, Li J, de Castillejo CL, Li H, Hunter MD, de Roode JC (2012) Food plant derived disease tolerance and resistance in a natural butterfly-plant-parasite interactions. Evolution 66(11):3367–3376
Sugio A, Dubreuil G, Giron D, Simon JC (2015) Plant-insect interactions under bacterial influence: ecological implications and underlying mechanisms. J Exp Bot 66(2):467–478
Tan WH, Tao L, Hoang KM, Hunter MD, de Roode JC (2018) The effects of milkweed induced defense on parasite resistance in monarch butterflies Danaus plexippus. J Chem Ecol 44(11):1040–1044
Tan WH, Acevedo T, Harris EV, Alcaide TY, Walters JR, Hunter MD, Gerardo NM, de Roode JC (2019) Transcriptomics of monarch butterflies (Danaus plexippus) reveals that toxic host plants alter expression of detoxification genes and down-regulate a small number of immune genes. Mol Ecol 28(22):4845–4863
Tao L, Hoang KM, Hunter MD, de Roode JC (2016) Fitness costs of animal medication: antiparasitic plant chemicals reduce fitness of monarch butterfly hosts. J Anim Ecol 85(5):1246–1254
Acknowledgements
We thank Erik Edwards for maintaining plants, Miles Holliman and Krish Khurana for assisting with monarch maintenance and injections, and Benjamin Wertz and Huw Davies for providing UPLC technology and training.
Funding
This research was funded by the National Science Foundation grant IOS-1557724 to JCDR and IRACDA Fellowships in Research and Science Teaching (NIH K12 GM 000680).
Author information
Authors and Affiliations
Contributions
KLA and JCDR contributed to the study conception and design. Material preparation, data collection and analysis were performed by KLA, AA, and JC. Original draft preparation was written by KLA. Review and editing was performed by KLA and JCDR. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare there is no conflict of interest.
Additional information
Handling Editor: Chen-Zhu Wang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Adams, K.L., Aljohani, A., Chavez, J. et al. Effects of cardenolides of milkweed plants on immunity of the monarch butterfly. Arthropod-Plant Interactions 15, 249–252 (2021). https://doi.org/10.1007/s11829-021-09812-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-021-09812-w