Pharmacophagy in Insects: Ecological and Evolutionary Perspectives on the Non-Nutritional Use of Plant Specialized Metabolites

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Abstract

Herbivorous insects can interact with plants in ways that go beyond nutrition, with plant specialized (secondary) metabolites (PSMs) mediating complex non-nutritional relationships. While PSMs often function as anti-herbivore defenses, many insects have evolved strategies to counteract and even exploit these compounds, using them for purposes such as their own defense against antagonists, enhanced mating success, or self-medication. This review explores pharmacophagy, where insects actively seek and acquire specific PSMs from both food and non-food plants for benefits unrelated to nutrition, across different insect orders such as Coleoptera, Orthoptera, Hymenoptera, Lepidoptera, Diptera and Neuroptera. Key examples include the acquisition of cucurbitacins by Diabrotica spp., neo-clerodane diterpenoids by Athalia rosae, and pyrrolizidine alkaloids by butterflies of the Danaini tribe, each demonstrating unique adaptive uses of non-nutritional plant chemicals. We discuss the intra- and transgenerational transfer of pharmacophagously acquired PSMs among conspecifics and the methods for identifying and testing pharmacophagy, emphasizing the importance of interdisciplinary approaches that combine field observations, behavioral studies, and chemical analyses. The evolutionary pathways leading to pharmacophagy are considered, highlighting selective pressures such as predation, parasitism, and sexual selection. We also address the costs associated with pharmacophagy, including energetic demands and potential toxicity. Extending the discussion to non-insect taxa suggests that pharmacophagy may be a broader ecological phenomenon. By establishing a comprehensive framework for understanding pharmacophagy, we aim to stimulate further research into this intriguing aspect of plant-insect interactions and highlight its potential applications in pest management, conservation, and human health.
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Abstract

Herbivorous insects can interact with plants in ways that go beyond nutrition, with plant specialized (secondary) metabolites (PSMs) mediating complex non-nutritional relationships. While PSMs often function as anti-herbivore defenses, many insects have evolved strategies to counteract and even exploit these compounds, using them for purposes such as their own defense against antagonists, enhanced mating success, or self-medication. This review explores pharmacophagy, where insects actively seek and acquire specific PSMs from both food and non-food plants for benefits unrelated to nutrition, across different insect orders such as Coleoptera, Orthoptera, Hymenoptera, Lepidoptera, Diptera and Neuroptera. Key examples include the acquisition of cucurbitacins by Diabrotica spp., neo-clerodane diterpenoids by Athalia rosae, and pyrrolizidine alkaloids by butterflies of the Danaini tribe, each demonstrating unique adaptive uses of non-nutritional plant chemicals. We discuss the intra- and transgenerational transfer of pharmacophagously acquired PSMs among conspecifics and the methods for identifying and testing pharmacophagy, emphasizing the importance of interdisciplinary approaches that combine field observations, behavioral studies, and chemical analyses. The evolutionary pathways leading to pharmacophagy are considered, highlighting selective pressures such as predation, parasitism, and sexual selection. We also address the costs associated with pharmacophagy, including energetic demands and potential toxicity. Extending the discussion to non-insect taxa suggests that pharmacophagy may be a broader ecological phenomenon. By establishing a comprehensive framework for understanding pharmacophagy, we aim to stimulate further research into this intriguing aspect of plant-insect interactions and highlight its potential applications in pest management, conservation, and human health. DOI https://doi.org/10.32942/X23D12 Subjects Ecology and Evolutionary Biology, Entomology, Life Sciences

Keywords

Pharmacophagy, plant secondary metabolites, chemical defense, non-nutritional exploitation, insect-plant interactions, Sequestration, chemical ecology Dates Published: 2025-04-03 04:02 Last Updated: 2025-04-03 04:02 License CC-By Attribution-NonCommercial-NoDerivatives 4.0 International Additional Metadata Conflict of interest statement: None Data and Code Availability Statement: Not applicable Language: English

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