Abstract

BackgroundModifications of the ovipositor appear to have played a prominent role in defining the host range of parasitoid hymenopterans, highlighting an important contributing factor in shaping their oviposition strategies, life histories and diversification. Despite many comparative studies on the structure of the hymenopteran terebra, little is known about functional aspects of the musculoskeletal ovipositor system. Therefore, we examined all inherent cuticular elements and muscles of the ovipositor of the ichneumonid wasp Venturia canescens (Gravenhorst, 1829), investigated the mechanics of the ovipositor system and determined its mode of function.ResultsWe found that the movements of the ichneumonid ovipositor, which consists of the female T9 (9th abdominal tergum), two pairs of valvifers and three pairs of valvulae, are actuated by a set of six paired muscles. The posterior and the anterior 2nd valvifer-2nd valvula muscles flex and extend the terebra from its resting towards an active probing position and back. The dorsal T9-2nd valvifer muscle is modified in V. canescens and forms distinct bundles that, together with the antagonistically acting ventral T9-2nd valvifer muscle, change the relative position of the 2nd valvifer to the female T9. Thereby, they indirectly tilt the 1st valvifer because it is linked with both of them via intervalvifer and tergo-valvifer articulation, respectively. The 1st valvifer acts as a lever arm that transfers movements to the 1st valvula. The posterior T9-2nd valvifer muscle and the small 1st-valvifer-genital membrane muscle stabilize the system during oviposition.ConclusionsFrom our examination of the elements of the musculoskeletal ovipositor system of ichneumonids, we discussed leverages and muscle forces and developed a functional model of the underlying working mechanisms adding to our understanding of a key feature that has largely determined the evolutionary success of the megadiverse Ichneumonidae with more than 24,000 hitherto described species.

Highlights

  • Modifications of the ovipositor appear to have played a prominent role in defining the host range of parasitoid hymenopterans, highlighting an important contributing factor in shaping their oviposition strategies, life histories and diversification

  • The hymenopteran ovipositor consists of the female Female T9 (T9) (9th abdominal tergum), two pairs of valvifers and three pairs of valvulae

  • We combined light microscopy (LM), scanning electron microscopy (SEM), synchrotron X-ray phase-contrast microtomography (SR-μCT) and subsequent 3D image processing with muscle and leverage analyses. Based on these microscopical and microtomographical studies, we present a thorough morphological, mechanical and functional analysis of the musculoskeletal ovipositor system (Additional file 2) that steers the various movements executed by the female ichneumonid wasp during oviposition

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Summary

Introduction

Modifications of the ovipositor appear to have played a prominent role in defining the host range of parasitoid hymenopterans, highlighting an important contributing factor in shaping their oviposition strategies, life histories and diversification. The 1st valvifers (fusion of the 8th gonocoxites with the gonangula [10]; = gonangulum, gonangula sensu [1]) anterordorsally are continuous with the rami of the 1st valvulae (8th gonapophyses; = lower valves sensu [1]). Their posterior angles articulate dorsally with the female T9 via the tergo-valvifer articulation and ventrally with the 2nd valvifers via the intervalvifer articulation. The sensillar equipment of the 1st and 2nd valvulae is highly variable among parasitoid hymenopterans [2]

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