Mackenzie Hoogshagen, Amy P Hastings, Joselyne Chavez, Marissa Duckett, Rayshaun Pettit, Andrew P Pahnke, Anurag A Agrawal, Jacobus C de Roode
{"title":"Mixtures of Milkweed Cardenolides Protect Monarch Butterflies against Parasites.","authors":"Mackenzie Hoogshagen, Amy P Hastings, Joselyne Chavez, Marissa Duckett, Rayshaun Pettit, Andrew P Pahnke, Anurag A Agrawal, Jacobus C de Roode","doi":"10.1007/s10886-023-01461-y","DOIUrl":null,"url":null,"abstract":"<p><p>Plants have evolved a diverse arsenal of defensive secondary metabolites in their evolutionary arms race with insect herbivores. In addition to the bottom-up forces created by plant chemicals, herbivores face top-down pressure from natural enemies, such as predators, parasitoids and parasites. This has led to the evolution of specialist herbivores that do not only tolerate plant secondary metabolites but even use them to fight natural enemies. Monarch butterflies (Danaus plexippus) are known for their use of milkweed chemicals (cardenolides) as protection against vertebrate predators. Recent studies have shown that milkweeds with high cardenolide concentrations can also provide protection against a virulent protozoan parasite. However, whether cardenolides are directly responsible for these effects, and whether individual cardenolides or mixtures of these chemicals are needed to reduce infection, remains unknown. We fed monarch larvae the four most abundant cardenolides found in the anti-parasitic-milkweed Asclepias curassavica at varying concentrations and compositions to determine which provided the highest resistance to parasite infection. Measuring infection rates and infection intensities, we found that resistance is dependent on both concentration and composition of cardenolides, with mixtures of cardenolides performing significantly better than individual compounds, even when mixtures included lower concentrations of individual compounds. These results suggest that cardenolides function synergistically to provide resistance against parasite infection and help explain why only milkweed species that produce diverse cardenolide compounds provide measurable parasite resistance. More broadly, our results suggest that herbivores can benefit from consuming plants with diverse defensive chemical compounds through release from parasitism.</p>","PeriodicalId":15346,"journal":{"name":"Journal of Chemical Ecology","volume":null,"pages":null},"PeriodicalIF":2.2000,"publicationDate":"2024-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Chemical Ecology","FirstCategoryId":"93","ListUrlMain":"https://doi.org/10.1007/s10886-023-01461-y","RegionNum":3,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2023/11/6 0:00:00","PubModel":"Epub","JCR":"Q4","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Plants have evolved a diverse arsenal of defensive secondary metabolites in their evolutionary arms race with insect herbivores. In addition to the bottom-up forces created by plant chemicals, herbivores face top-down pressure from natural enemies, such as predators, parasitoids and parasites. This has led to the evolution of specialist herbivores that do not only tolerate plant secondary metabolites but even use them to fight natural enemies. Monarch butterflies (Danaus plexippus) are known for their use of milkweed chemicals (cardenolides) as protection against vertebrate predators. Recent studies have shown that milkweeds with high cardenolide concentrations can also provide protection against a virulent protozoan parasite. However, whether cardenolides are directly responsible for these effects, and whether individual cardenolides or mixtures of these chemicals are needed to reduce infection, remains unknown. We fed monarch larvae the four most abundant cardenolides found in the anti-parasitic-milkweed Asclepias curassavica at varying concentrations and compositions to determine which provided the highest resistance to parasite infection. Measuring infection rates and infection intensities, we found that resistance is dependent on both concentration and composition of cardenolides, with mixtures of cardenolides performing significantly better than individual compounds, even when mixtures included lower concentrations of individual compounds. These results suggest that cardenolides function synergistically to provide resistance against parasite infection and help explain why only milkweed species that produce diverse cardenolide compounds provide measurable parasite resistance. More broadly, our results suggest that herbivores can benefit from consuming plants with diverse defensive chemical compounds through release from parasitism.
期刊介绍:
Journal of Chemical Ecology is devoted to promoting an ecological understanding of the origin, function, and significance of natural chemicals that mediate interactions within and between organisms. Such relationships, often adaptively important, comprise the oldest of communication systems in terrestrial and aquatic environments. With recent advances in methodology for elucidating structures of the chemical compounds involved, a strong interdisciplinary association has developed between chemists and biologists which should accelerate understanding of these interactions in nature.
Scientific contributions, including review articles, are welcome from either members or nonmembers of the International Society of Chemical Ecology. Manuscripts must be in English and may include original research in biological and/or chemical aspects of chemical ecology. They may include substantive observations of interactions in nature, the elucidation of the chemical compounds involved, the mechanisms of their production and reception, and the translation of such basic information into survey and control protocols. Sufficient biological and chemical detail should be given to substantiate conclusions and to permit results to be evaluated and reproduced.