Department of Biology, Loyola University Chicago, Chicago, IL, 60660, USA.
Poisonous Plant Research Laboratory, USDA-ARS, Logan, UT, 84341, USA.
J Chem Ecol. 2024 Oct;50(9-10):465-477. doi: 10.1007/s10886-024-01529-3. Epub 2024 Sep 5.
Legumes are notorious for coevolutionary arms races where chemical defenses are employed to ward off herbivores-particularly insect seed predators. Locoweeds are legumes containing the toxic alkaloid swainsonine which can poison livestock, but its role as a deterrent for insects is unknown. Swainsonine is 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 quantify 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 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.
豆科植物以协同进化军备竞赛而闻名，在这种竞赛中，化学防御被用来抵御草食动物——特别是昆虫种子捕食者。疯草是豆科植物，含有有毒生物碱苦马豆素，会毒害牲畜，但它作为昆虫驱避剂的作用尚不清楚。苦马豆素是由真菌内生菌Alternaria 节Undifilum 产生的，毒素的化学组成已经得到很好的描述。尽管有这些知识，但疯草中苦马豆素毒素的生态作用和进化驱动因素仍不确定。在这里，我们量化了超多样的疯草 Astragalus lentiginosus 中的苦马豆素浓度和草食性水平，以评估其作为一种进化化学防御的作用。我们发现，A. lentiginosus 显示出苦马豆素浓度的相当大的变异，根据品种的不同，特别是在种群和局部地理尺度上都存在存在/缺失的变异。令人惊讶的是，来自果实中出现的假定普通昆虫的草食性水平与苦马豆素浓度没有相关性。相反，与专门的 Acanthoscelides 种子甲虫相关的种子和果实草食性水平随着苦马豆素浓度的增加而增加——这表明可能存在协同进化军备竞赛。我们的结果表明，内生菌产生的毒素系统的变异可能不符合植物化学物质地理变异和生态作用的经典预期。我们更广泛地讨论了这些结果对植物-内生毒素系统和协同进化动态的影响，强调了这些系统需要更多研究。
