Water-repellent plant surface structure induced by gall-forming insects for waste management

Many animals and plants have evolved elaborate water-repellent microstructures on their surface, which often play important roles in their ecological adaptation. Here we report a unique type of water-repellent structure on plant surface, which develops as an insect-induced plant morphology in a social context. Some social aphids form galls on their host plant, in which they produce large amount of hydrophobic wax. Excreted honeydew is coated by the powdery wax to form “honeydew balls”, which are actively disposed by soldier nymphs through an opening on their gall. These activities are enabled by a highly water-repellent inner gall surface, and we discovered that this surface is covered with dense trichomes that are not found on normal plant surface. The trichomes are coated by fine particles of the insect-produced wax, thereby realizing a high water repellency with a cooperative interaction between aphids and plants. The plant leaves on which the gall is formed often exhibit patchy areas with dense trichomes, representing an ectopic expression of the insect-induced plant morphology. In the pouch-shaped closed galls of a related social aphid species, by contrast, the inner surface was not covered with trichomes. Our findings provide a convincing example of how the extended phenotype of an animal, expressed in a plant, plays a pivotal role in maintaining sociality.

诸多动植物已在其体表演化出精巧的疏水微结构，此类结构通常在其生态适应过程中发挥关键作用。本研究报道了一类独特的植物体表疏水结构，该结构以昆虫诱导的植物形态形式在社会背景下形成。部分社会蚜虫会在宿主植物上形成虫瘿，并在虫瘿内分泌大量疏水蜡质。蚜虫排泄的蜜露会被粉状蜡质包裹形成"蜜露球"，兵若虫会通过虫瘿上的开口主动移除这些蜜露球。这类移除活动依赖于虫瘿内壁极高的疏水性能，我们发现该内壁覆盖有致密的毛状体（trichomes），此类结构在正常植物体表并不存在。这些毛状体表面覆有蚜虫分泌的蜡质微细颗粒，从而通过蚜虫与植物的协同互作实现了高疏水性能。形成虫瘿的植物叶片常出现分布不均的致密毛状体区域，这代表了昆虫诱导的植物形态的异位表达。与之相对，近缘社会蚜虫物种的囊状封闭虫瘿，其内壁并未覆盖毛状体。本研究结果为"动物的延伸表型在植物体内表达，并在维持社会性中发挥关键作用"提供了极具说服力的例证。