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

Abstract

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.

Mechanisms of ovipositor insertion and steering of a parasitic wasp

“…Therefore, they need to pierce and explore the substrate (3,6), locate the host, and sometimes also pierce through the host's integument (44)(45)(46)(47), which is all done with the ovipositor apparatus only. Although the probing behavior of parasitic wasps has been repeatedly mentioned in the literature (3,6,17,18,(48)(49)(50)(51), no quantitative studies have been performed until now. Here, we show evidence that wasps are able to explore a large space from a single puncture point and that they use relative valve motions to insert and steer the ovipositor.…”

“…Despite the proposed importance of ovipositors for the evolutionary success of hymenopterans, there is only a small number of empirical studies quantifying mechanical properties of the ovipositors (6,(16)(17)(18). The proposed theories of probing are based on morphological data, with only a few studies focusing on the ovipositor inside the substrate (25,37), but no one has ever analyzed the dynamics of probing inside the substrate.…”

“…The ovipositor and the "wasp waist," a constriction of the body between the first and second abdominal segment (11), are essential in probing behavior and are therefore considered to be instrumental in the evolution of the order (11)(12)(13)(14)(15). The shape, structure, and mechanical properties of the ovipositors are putatively adapted to the substrates into which the animals need to probe (6,(16)(17)(18), and because both substrates and hosts are so diverse, this might have resulted in high species diversification of the hymenopterans (13,14). However, to understand the observed diversity in the ovipositor shapes, understanding of the probing mechanics is essential.…”

Biomechanics of substrate boring by fig wasps

“…and Heterospilus prosopidi, the presence of calcium in the ovipositor tips enables high wear resistance through biomineralization (Quicke et al, 2004). Most other reported wasp species have higher amounts of zinc and/or manganese in their ovipositors Vincent and King, 1995;Polidori et al, 2013;Quicke et al, 2004). Similarly, the presence of transition metals in larvae mandibles of Stegobium paniceum and Gibbium aequinoctiale species of beetles aids in boring into hard seeds as oppposed to others without metals, which are incapable of seed boring (Morgan et al, 2003).…”

How to be a fig wasp parasite on the fig–fig wasp mutualism

“…Pollinators and early gallers had smooth ovipositors, whereas all late-arriving gallers and parasitoids had well developed serrations on their ovipositors for syconium penetration [18 ]. Penetration of harder figs was facilitated by the presence of metals, such as zinc, in the ovipositors [43,44] as was also found for cynipid gall wasps [45]. Some parasites use oviposition channels drilled by other NPFWs [37]; these may be hyperparasites ovipositing in locations where other eggs were laid or with ovipositors that are unable to independently penetrate the syconium.…”