Venom tradeoff shapes interspecific interactions, physiology and reproduction

An animal’s ability to effectively capture prey and defend against predators is pivotal to its survival1. A key innovation in many predator-prey interactions is venom, which consists of many toxin proteins that shape its phenotype2. Its unusually direct relationship of gene-toxin-phenotype make it an appealing system for studies at the organismal level 3,4. In this work we use the sea anemone Nematostella vectensis as a model organism as it provides us with the opportunity to test for the first time how toxin-genotypes impact predator-prey interactions. Specifically, we compare a native-population5 and a transgenic line which both have significantly reduced levels of Nv1, the major toxin in adult Nematostella6, to animals with wildtype levels of Nv1. We demonstrate that the transgenic strain phenocopies native anemones lacking Nv1 as they both have impaired ability to defend themselves against grass shrimp, a native predator. Mummichog killifish, unexpectedly are attracted to Nematostella with wildtype-levels of Nv1, highlighting that Nv1 plays a complex role in shaping interspecific-interactions. Finally, we demonstrate an evolutionary tradeoff as the reduction of Nv1 levels causes faster growth and increased reproductive rates compared to Nematostella control lines. Overall, our results experimentally link organism’s venom to its physiology, reproduction and interspecific interactions.

动物有效捕获猎物并抵御捕食者的能力，对其生存至关重要¹。在众多捕食者-猎物互作关系中，毒液是一项关键演化创新，其由多种塑造宿主表型（phenotype）的毒素蛋白构成²。该毒液系统所具备的基因-毒素-表型间异常直接的关联，使其成为个体水平研究的极具吸引力的模型系统³,⁴。
本研究以韦氏海葵（Nematostella vectensis）作为模式生物，因其为我们提供了首次验证毒素基因型如何影响捕食者-猎物互作的契机。具体而言，我们将两类个体——野生种群⁵以及Nv1（成年韦氏海葵的主要毒素⁶）表达量显著下调的转基因品系——与Nv1表达量处于野生型（wildtype）水平的个体进行对比。
本研究证实，该转基因品系可模拟缺失Nv1的野生海葵的表型：二者抵御草虾（一种本地捕食者）的能力均受到损伤。令人意外的是，底鳉（Mummichog killifish）会被Nv1表达量处于野生型水平的韦氏海葵所吸引，这表明Nv1在塑造种间互作中发挥着复杂的调控作用。最后，本研究证实存在一项演化权衡：与韦氏海葵的对照组品系相比，Nv1表达量下调的个体生长速度更快、繁殖率更高。
综上，本研究结果通过实验将生物体的毒液与其生理机能、繁殖能力以及种间互作建立了直接关联。