Escalation in coevolution: Characterization of novel plant toxins, how specialist herbivores cope, and tests of phylogenetic intensification in plant defense potency

共同进化的升级：新型植物毒素的表征、专业食草动物如何应对以及植物防御效力的系统发育强化测试

• 批准号: 2209762
• 负责人: Anurag Agrawal
• 金额: $ 65.77万
• 依托单位: Cornell University
• 依托单位国家: 美国
• 项目类别: Standard Grant
• 财政年份: 2022
• 资助国家: 美国
• 起止时间: 2022-06-01 至 2025-05-31
• 项目状态: 未结题
• 来源: https://www.nsf.gov/awardsearch/showAward?AWD_ID=2209762&HistoricalAwards=false
• 关键词: Escalation; coevolution; Characterization; novel; plant

Insects that feed on plants are thought to impose natural selection for chemical defenses in the plant tissues they eat. The research being conducted here is on milkweed plants, which contains a highly potent toxin, labriformin, which has evolved to high concentrations in in several species. When highly expressed, labriformin inhibits an essential transport enzyme (the sodium-potassium pump) of the monarch butterfly and the large milkweed bug. These specialized insect pests biochemically modify labriformin to less toxic compounds and sequester these-products for their own defense. The monarch and seed bug’s highly tolerant sodium pump and biochemical modifications point to labriformin being at the center of reciprocal evolution between milkweed and its herbivores. This work serves to unravel the mechanisms of the interaction through physiological and evolutionary analyses. The research also serves as a model for understanding both natural and agricultural interactions between plants and pests. Finally, the milkweed - monarch system lends itself well to public engagement because of its iconic stature, declining populations of conservation concern, and use in school curricula. As part of this project, the researchers are developing modules for K-12 schools and engaging in public outreach through presentations and blogs. Among milkweed plants which are fed upon by several specialized lineages of insect herbivores, coevolutionary interactions have been well-studied and novel mechanisms have been elucidated. Researchers recently discovered a milkweed that contains high levels of labriformin, a highly toxic cardenolide which is unusual in form (containing a ring with nitrogen (N) and sulfur (S)), which could well be an escalated form of costly defense. The current work seeks to investigate additional N-containing cardenolides across the milkweed phylogeny and seek to decipher their physiological impacts and detoxification in independent herbivores lineages. Repeatedly evolving offense-defense mechanisms in plant-herbivore lineages will likely reveal generalities of coevolution. Three objectives will address both sides of coevolution: 1) Determine the mechanisms by which N-containing cardenolide defenses are processed, detoxified, and stored by two specialist milkweed insects, monarch caterpillars and seed bugs. This will employ feeding trials with isolated compounds, physiological assays, and studies of behavior, using both specialists as well as CRISPR-edited Drosophila that have genetic substitutions for tolerating cardenolides. 2) Assess the costs and benefits of detoxification and sequestration using quantitative genetics coupled with feeding and chemical assays of monarchs and seed bugs on milkweed plants with and without N-containing cardenolides. Genetic correlations will reveal life-history costs and traits associated with differential sequestration. 3) Examine the pattern of N-containing defense evolution among milkweeds across the phylogeny, testing hypotheses about N-limitation, defense allocation, and trade-offs between cardenolide concentration and potency. One hypothesis, that later diverging milkweeds have evolved more potent but less concentrated cardenolides, was predicted by theory and suggested by a phylogenetic pattern, but never rigorously tested. Overall these objectives will advance understanding of coevolutionary mechanisms by characterizing novel plant defenses and the physiological ecology of counter-adaptation in specialist herbivores, genetic variation in detoxification and sequestration of toxins, and plant defense evolution at the macroevolutionary scale.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

以植物为食的昆虫被认为对所食用的植物组织中的化学防御措施施加自然选择。此处进行的研究是在乳草植物上进行的，该植物中含有高潜在的毒素Labriformin，该植物已在几种物种的高浓度中发展为高浓度。当高度表达时，拉布格林会抑制君主蝴蝶和大乳草虫的基本运输酶（钠钾泵）。这些专门的绝缘害虫生物化学将labriformin修改为毒性较小的化合物，并隔离了这些产品以防御自己的防御。君主和种子虫的高度耐受钠泵和生化修饰表明，拉布拉菌素是米尔克草及其食草动物之间相互演变的中心。这项工作通过物理和进化分析来揭示相互作用的机制。该研究还可以作为理解植物与害虫之间自然和农业相互作用的模型。最后，Milkweed -Monarch系统由于其标志性的身材，保护关注的人口减少并在学校课程中使用，因此非常适合公众参与。作为该项目的一部分，研究人员正在为K-12学校开发模块，并通过演讲和博客从事公共宣传。在昆虫食草动物的几个专业谱系供养的乳草植物中，我们进行了深入研究，并阐明了新型机制。研究人员最近发现了一种含有高水平的labriformin的乳草，这是一种高度毒性的心甲醇，形式不寻常（含有氮（N）和硫（S）的环，很可能是昂贵的防御的形式。当前的工作旨在调查整个乳草系统发育中的其他含有N的Cardenolides，并试图破译其在独立的草食动物谱系中的身体影响和排毒。反复发展的植物饲养谱系中的犯罪机制可能会揭示共同进化的概括。三个目标将解决协同进化的两面：1）确定由两种专业的Milkweed绝缘材料，君主卡特彼勒和种子虫处理，排毒和存储的含有N含有N的机制。这将使用孤立的化合物，生理测定和行为研究的员工喂养试验，并使用专家以及CRISPR编辑的果蝇，这些果蝇具有遗传替代的遗传替代。 2）使用定量遗传学评估排毒和隔离的成本和收益，并对具有和不含N含N含有N的Milkweed植物的君主和种子虫的饲料和化学评估。遗传相关性将揭示生活成本和与差分差异相关的特征。 3）检查系统发育中的乳草之间含N的防御性进化模式，测试了关于N限制，防御分配以及Cardenolide浓度和效力之间的权衡的假设。一种假设，后来发散的乳草的潜力越来越大，但浓缩的心脏不足，是通过理论预测的，并通过系统发育模式提出了建议，但从未经过严格测试。总的来说，这些目标将通过表征新颖的植物防御能力以及专业草食动物的反适应的物理生态学来提高对协同进化机制的理解，在宏观进化范围内，在宏观进化范围内，在NSF的法定任务中，通过评估范围的范围，这一范围的范围是众多的构成者。

项目成果

Plant defense synergies and antagonisms affect performance of specialist herbivores of common milkweed

• DOI: 10.1002/ecy.3915
• 发表时间: 2022-12-26
• 期刊: ECOLOGY
• 影响因子: 4.8
• 作者: Edwards, Collin B.;Ellner, Stephen P.;Agrawal, Anurag A.
• 通讯作者: Agrawal, Anurag A.

A nutrition–defence trade-off drives diet choice in a toxic plant generalist

营养与防御的权衡推动了有毒植物多面手的饮食选择

• DOI: 10.1098/rspb.2023.0987
• 发表时间: 2023
• 期刊: Proceedings of the Royal Society B: Biological Sciences
• 作者: Carlson, Nathaniel J.;Agrawal, Anurag A.
• 通讯作者: Agrawal, Anurag A.

The Distribution of Species Interactions

• DOI: 10.1086/727939
• 发表时间: 2023-12
• 期刊: The Quarterly Review of Biology
• 作者: R. Karban;Anurag A. Agrawal

A direct comparison of ecological theories for predicting the relationship between plant traits and growth

• DOI: 10.1002/ecy.3986
• 发表时间: 2023-03-06
• 期刊: ECOLOGY
• 影响因子: 4.8
• 作者: Goud, Ellie M.;Agrawal, Anurag A.;Sparks, Jed P.
• 通讯作者: Sparks, Jed P.

Testing the selective sequestration hypothesis: Monarch butterflies preferentially sequester plant defences that are less toxic to themselves while maintaining potency to others

测试选择性隔离假说：帝王蝶优先隔离对自身毒性较小的植物防御，同时保持对他人的效力

• DOI: 10.1111/ele.14340
• 发表时间: 2023
• 期刊: Ecology Letters
• 影响因子: 8.8
• 作者: Agrawal, Anurag A.;Hastings, Amy P.;Duplais, Christophe
• 通讯作者: Duplais, Christophe