Breaking up the Wall: Metal-Enrichment in Ovipositors, but Not in Mandibles, Co-Varies with Substrate Hardness in Gall-Wasps and Their Associates

The cuticle of certain insect body parts can be hardened by the addition of metals, and because niche separation may require morphological adaptations, inclusion of such metals may be linked to life history traits. Here, we analysed the distribution and enrichment of metals in the mandibles and ovipositors of a large family of gall-inducing wasps (Cynipidae, or Gall-Wasps) (plus one gall-inducing Chalcidoidea), and their associated wasps (gall-parasitoids and gall-inquilines) (Cynipidae, Chalcidoidea and Ichneumonoidea). Both plant types/organs where galls are induced, as well as galls themselves, vary considerably in hardness, thus making this group of wasps an ideal model to test if substrate hardness can predict metal enrichment. Non-galler, parasitic Cynipoidea attacking unconcealed hosts were used as ecological “outgroup”. With varying occurrence and concentration, Zn, Mn and Cu were detected in mandibles and ovipositors of the studied species. Zn tends be exclusively concentrated at the distal parts of the organs, while Mn and Cu showed a linear increase from the proximal to the distal parts of the organs. In general, we found that most of species having metal-enriched ovipositors (independently of metal type and concentration) were gall-invaders. Among gall-inducers, metals in the ovipositors were more likely to be found in species inducing galls in woody plants. Overall, a clear positive effect of substrate hardness on metal concentration was detected for all the three metals. Phylogenetic relationships among species, as suggested by the most recent estimates, seemed to have a weak role in explaining metal variation. On the other hand, no relationships were found between substrate hardness or gall-association type and concentration of metals in mandibles. We suggest that ecological pressures related to oviposition were sufficiently strong to drive changes in ovipositor elemental structure in these gall-associated Hymenoptera.部分昆虫躯体部位的表皮可通过金属富集实现硬化，而生态位分化往往需要对应的形态适应性演化，因此此类金属的富集可能与昆虫的生活史特征存在关联。本研究针对大型造瘿蜂类群（瘿蜂科Cynipidae，Gall-Wasps）及其伴生类群（含1种隶属于小蜂总科Chalcidoidea的造瘿蜂类群）、瘿寄生蜂与瘿寄居蜂（类群覆盖瘿蜂科、小蜂总科与姬蜂总科Ichneumonoidea）的上颚（mandibles）与产卵器（ovipositors）中金属的分布与富集特征展开分析。造瘿蜂所诱导虫瘿的寄主植物类型/器官，以及虫瘿本身的硬度均存在显著差异，因此该蜂类类群可作为理想模型，用于验证基质硬度是否能够预测金属富集程度。本研究以攻击裸露寄主的非造瘿寄生性瘿蜂总科Cynipoidea类群作为生态外群（outgroup）。在所研究物种的上颚与产卵器中，均检测到锌（Zn）、锰（Mn）与铜（Cu），且其检出频率与浓度存在差异。其中锌多仅富集于器官的远心端区域，而锰与铜则呈现从近心端向远心端线性递增的分布模式。总体而言，多数产卵器富含金属的物种（无论金属种类与浓度如何）均为虫瘿入侵类群。在造瘿蜂类群中，产卵器携带金属的物种更倾向于在木本植物上诱导形成虫瘿。针对三种金属的分析均显示，基质硬度对金属浓度存在显著的正向影响。根据最新的系统发育估算结果，物种间的系统发育关系对金属富集变异的解释力较弱。另一方面，基质硬度或虫瘿关联类型与上颚中的金属浓度均未发现显著关联。本研究认为，与产卵行为相关的生态压力足够强大，足以驱动这类虫瘿关联膜翅目（Hymenoptera）昆虫产卵器的元素结构演化。