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.

某些昆虫躯体部位的表皮可通过金属沉积实现硬化，而生态位分化往往需要伴随形态适应性演化，因此这类金属的富集现象或与物种生活史特征存在关联。本研究针对一类大型虫瘿诱导蜂类群（瘿蜂科Cynipidae，又称瘿蜂）及1种广肩小蜂总科Chalcidoidea虫瘿诱导物种，及其伴生类群（包括瘿寄生蜂与瘿寄居蜂，类群涵盖瘿蜂科、广肩小蜂总科以及姬蜂总科Ichneumonoidea）的上颚与产卵器内的金属分布与富集特征展开分析。虫瘿诱导所针对的植物类型/器官，以及虫瘿本身的硬度差异显著，因此该蜂类类群可作为理想实验模型，用以验证基质硬度能否有效预测金属富集程度。本研究选取攻击裸露寄主的非虫瘿诱导型寄生瘿蜂总科Cynipoidea物种作为生态外类群。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），三种金属的检出率与浓度均存在差异。锌多仅富集于器官的远端区域，而锰与铜则呈现从器官近端向远端线性递增的分布模式。总体而言，多数产卵器存在金属富集现象的物种（无论金属种类与浓度如何）均为虫瘿入侵类群。在虫瘿诱导蜂类中，产卵器携带金属富集特征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，本研究均发现基质硬度对金属浓度存在显著正向影响。根据最新研究估算得到的物种系统发育关系，其对金属含量变异的解释力相对较弱。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。我们推测，与产卵行为相关的生态压力足够强烈，足以驱动这类虫瘿关联膜翅目Hymenoptera昆虫的产卵器元素结构发生适应性演化。