Extensive local geographic variation in locoweed toxin produced by a fungal endophyte

Authors: DAVIS, JEREMY - Loyola University; SCOTT, MATTHEW - Loyola University; Cook, Daniel; GARDNER, DALE - Retired ARS Employee; MORSE, GEOFFERY - University Of San Diego; GRILLO, MICHAEL - Loyola University

Submitted to: Journal of Chemical Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/13/2024
Publication Date: 9/5/2024
Citation: Davis, J.S., Scott, M., Cook, D., Gardner, D., Morse, G., Grillo, M. 2024. Extensive local geographic variation in locoweed toxin produced by a fungal endophyte. Journal of Chemical Ecology. 50:465-477. https://doi.org/10.1007/s10886-024-01529-3.
DOI: https://doi.org/10.1007/s10886-024-01529-3

Interpretive Summary: Legumes are notorious for coevolutionary arms races where chemical defenses are employed to ward off herbivores—particularly insect seed predators. Locoweeds are a group of plants containing the toxic alkaloid swainsonine which can poison livestock and causes millions in economic damage every year. Swainsonine is known to be produced by the fungal endophyte Alternaria section Undifilum, and the chemical composition of the toxin has been well characterized. Despite this knowledge, the ecological roles and evolutionary drivers of swainsonine toxins in locoweeds remain uncertain. Here, we quantitate swainsonine concentrations and herbivory levels in the hyper-diverse locoweed Astragalus lentiginosus to evaluate its role as an evolved chemical defense. We found that A. lentiginosus shows considerable variation in swainsonine concentrations according to variety, in particular showing presence/absence variation at both population and local geographic scales. Surprisingly, herbivory levels from presumed generalist insects emerging from fruits showed no correlation with swainsonine concentrations. Conversely, seed and fruit herbivory levels linked to specialist Acanthoscelides seed beetles actually increased with concentrations of swainsonine—suggesting a possible coevolutionary arms race. Our results highlight that variation in endophyte-produced toxin systems may not follow classical expectations for geographic variation and ecological roles of plant chemicals. We discuss the implications of these results on plant-endophytic toxin systems and coevolutionary dynamics more broadly, highlighting a considerable need for more research in these systems.

Technical Abstract: Legumes are notorious for coevolutionary arms races where chemical defenses are employed to ward off herbivores—particularly insect seed predators. Locoweeds are a group of plants containing the toxic alkaloid swainsonine which can poison livestock and causes millions in economic damage every year. Swainsonine is known to be produced by the fungal endophyte Alternaria section Undifilum, and the chemical composition of the toxin has been well characterized. Despite this knowledge, the ecological roles and evolutionary drivers of swainsonine toxins in locoweeds remain uncertain. Here, we quantitate swainsonine concentrations and herbivory levels in the hyper-diverse locoweed Astragalus lentiginosus to evaluate its role as an evolved chemical defense. We found that A. lentiginosus shows considerable variation in swainsonine concentrations according to variety, in particular showing presence/absence variation at both population and local geographic scales. Surprisingly, herbivory levels from presumed generalist insects emerging from fruits showed no correlation with swainsonine concentrations. Conversely, seed and fruit herbivory levels linked to specialist Acanthoscelides seed beetles actually increased with concentrations of swainsonine—suggesting a possible coevolutionary arms race. Our results highlight that variation in endophyte-produced toxin systems may not follow classical expectations for geographic variation and ecological roles of plant chemicals. We discuss the implications of these results on plant-endophytic toxin systems and coevolutionary dynamics more broadly, highlighting a considerable need for more research in these systems.