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The ovipositor actuation mechanism of a parasitic wasp and its functional implications.

ABSTRACT: Parasitic wasps use specialized needle-like structures, ovipositors, to drill into substrates to reach hidden hosts. The external ovipositor (terebra) consists of three interconnected, sliding elements (valvulae), which are moved reciprocally during insertion. This presumably reduces the required pushing force on the terebra and limits the risk of damage whilst probing. Although this is an important mechanism, it is still not completely understood how the actuation of the valvulae is achieved, and it has only been studied with the ovipositor in rest position. Additionally, very little is known about the magnitude of the forces generated during probing. We used synchrotron X-ray microtomography to reconstruct the actuation mechanism of the parasitic wasp Diachasmimorpha longicaudata (Braconidae) in four distinct phases of the probing cycle. We show that only the paired first valvulae of the terebra move independently, while the second valvula moves with the metasoma ('abdomen'). The first valvula movements are initiated by rotation of one chitin plate (first valvifer) with respect to another such plate (second valvifer). This is achieved indirectly by muscles connecting the non-rotating second valvifer and the abdominal ninth tergite. Contrary to previous reports, we found muscle fibres running inside the terebra, although their function remains unclear. The estimated maximal forces that can be exerted by the first valvulae are small (protraction 1.19 mN and retraction 0.874 mN), which reduces the risk of buckling, but are sufficient for successful probing. The small net forces of the valvulae on the substrate may still lead to buckling of the terebra; we show that the sheaths surrounding the valvulae prevent this by effectively increasing the diameter and second moment of area of the terebra. Our findings improve the comprehension of hymenopteran probing mechanisms, the function of the associated muscles, and the forces and damage-limiting mechanism that are involved in drilling a slender terebra into a substrate.

SUBMITTER: van Meer NMME

PROVIDER: S-EPMC7495304 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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The ovipositor actuation mechanism of a parasitic wasp and its functional implications.

van Meer Noraly M M E NMME Cerkvenik Uroš U Schlepütz Christian M CM van Leeuwen Johan L JL Gussekloo Sander W S SWS

Journal of anatomy 20200613 4

Parasitic wasps use specialized needle-like structures, ovipositors, to drill into substrates to reach hidden hosts. The external ovipositor (terebra) consists of three interconnected, sliding elements (valvulae), which are moved reciprocally during insertion. This presumably reduces the required pushing force on the terebra and limits the risk of damage whilst probing. Although this is an important mechanism, it is still not completely understood how the actuation of the valvulae is achieved, a ...[more]

PMID: 32533567

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Project description:BackgroundResource partitioning is facilitated by adaptations along niche dimensions that range from morphology to behaviour. The exploitation of hidden resources may require specially adapted morphological or sensory tools for resource location and utilisation. Differences in tool diversity and complexity can determine not only how many species can utilize these hidden resources but also how they do so.Methodology and principal findingsThe sclerotisation, gross morphology and ultrastructure of the ovipositors of a seven-member community of parasitic wasps comprising of gallers and parasitoids developing within the globular syconia (closed inflorescences) of Ficus racemosa (Moraceae) was investigated. These wasps also differ in their parasitism mode (external versus internal oviposition) and their timing of oviposition into the expanding syconium during its development. The number and diversity of sensilla, as well as ovipositor teeth, increased from internally ovipositing to externally ovipositing species and from gallers to parasitoids. The extent of sclerotisation of the ovipositor tip matched the force required to penetrate the syconium at the time of oviposition of each species. The internally ovipositing pollinator had only one type of sensillum and a single notch on the ovipositor tip. Externally ovipositing species had multiple sensilla types and teeth on their ovipositors. Chemosensilla were most concentrated at ovipositor tips while mechanoreceptors were more widely distributed, facilitating the precise location of hidden hosts in these wasps which lack larval host-seeking behaviour. Ovipositor traits of one parasitoid differed from those of its syntopic galler congeners and clustered with those of parasitoids within a different wasp subfamily. Thus ovipositor tools can show lability based on adaptive necessity, and are not constrained by phylogeny.Conclusions/significanceOvipositor structure mirrored the increasingly complex trophic ecology and requirements for host accessibility in this parasite community. Ovipositor structure could be a useful surrogate for predicting the biology of parasites in other communities.

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The ovipositor actuation mechanism of a parasitic wasp and its functional implications.

Publications

The ovipositor actuation mechanism of a parasitic wasp and its functional implications.

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