Mechanisms of ovipositor insertion and steering of a parasitic wasp

Abstract

Drilling into solid substrates with slender beam-like structures is a mechanical challenge, but is regularly done by female parasitic wasps. The wasp inserts her ovipositor into solid substrates to deposit eggs in hosts, and even seems capable of steering the ovipositor while drilling. The ovipositor generally consists of three longitudinally connected valves that can slide along each other. Alternative valve movements have been hypothesized to be involved in ovipositor damage avoidance and steering during drilling. However, none of the hypotheses have been tested in vivo. We used 3D and 2D motion analysis to quantify the probing behavior of the fruit-fly parasitoid Diachasmimorpha longicaudata (Braconidae) at the levels of the ovipositor and its individual valves. We show that the wasps can steer and curve their ovipositors in any direction relative to their body axis. In a soft substrate, the ovipositors can be inserted without reciprocal motion of the valves. In a stiff substrate, such motions were always observed. This is in agreement with the damage avoidance hypothesis of insertion, as they presumably limit the overall net pushing force. Steering can be achieved by varying the asymmetry of the distal part of the ovipositor by protracting one valve set with respect to the other. Tip asymmetry is enhanced by curving of ventral elements in the absence of an opposing force, possibly due to pretension. Our findings deepen the knowledge of the functioning and evolution of the ovipositor in hymenopterans and may help to improve man-made steerable probes.Diachasmimorpha longicaudata | ovipositor kinematics | buckling avoidance | spatial probing | minimally invasive probe F rom a mechanical perspective, it is very difficult to drill into a solid substrate with a very thin probe, because it can easily bend and break. Parasitic wasps, however, do this regularly when they use their slender ovipositors to search for hosts in solid substrates, such as fruits or even wood (1-3).The general morphology of the ovipositor is similar across all wasp species (4, 5); it consists of four elements, called valves, of which two are often merged such that three functional valves remain (Fig. 1). In most species, the distal part of the ovipositor is morphologically distinct (3, 6), which we will refer to as the tip. The valves can slide along each other (5, 7) and do not get dislocated under natural conditions, because they are longitudinally connected via a tongue-and-groove mechanism (5, 8-10). 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 (11-15). 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). Howeve...

Functional principles of steerable multi‐element probes in insects

“…This requires stiff needles which hinders the minimisation of their diameters. Furthermore, the reported relative curvatures of needle insertions (Caborni et al ., ; Moreira et al ., ) are generally much lower than found in wasps (Cerkvenik et al ., ), although some prototypes perform better when bending in one plane (Ko et al ., ). The restrictions in curving probably affect the accuracy and limit the versatility of these novel surgical tools.…”

“…Advancing a single valve only a short distance beyond the tip of the stationary ones assures that the slenderness ratio of the protracted part is low, thereby preventing buckling. The maximal recorded amplitude of valve protraction in D. longicaudata is approximately 200 µm (Cerkvenik et al ., ), which is roughly 3.5% of the total ovipositor length (Leyva, Browning & Gilstrap, ).…”

“…Inserting a single-element probe into a solid substrate requires a pushing force that is large enough to overcome these forces and a sufficiently stiff probe to avoid buckling (Okamura et al, 2004;Casanova, Carney & Sarntinoranont, 2014). A probe consisting of multiple reciprocally moving elements may be inserted more easily into a substrate than a single-element probe, because the former can reduce the net friction and pushing forces on the entire probe, as explained in Section II.2b (Vincent & King, 1995;Cerkvenik et al, 2017).…”

“…The ovipositors are often enveloped and protected by a pair of flexible sheaths, appendages that also originate at the ventral side of the animal's abdomen (Smith, 1969;Vilhelmsen, 2003). These sheaths are not inserted into the substrate (Ahmed et al, 2013;Kundanati & Gundiah, 2014;Cerkvenik et al, 2017).…”

“…In most cases, sheaths support the ovipositor during puncturing and at the beginning of its insertion into the substrate. The sheaths are not inserted into the substrate, but gradually fold over their full length in an arc-like shape away from the ovipositor base with increased insertion (Compton et al, 2009;Cerkvenik et al, 2017). Other buckling-prevention mechanisms include hardening the ovipositor tip (increasing E in Equation 2) with metal atoms, such as manganese and zinc , and shortening the probe's free length (L in Equation 2) by locking the ovipositor at the base (coxa) (Turrisi & Vilhelmsen, 2010), midway between their legs (Zhen et al, 2005;Kundanati & Gundiah, 2014), or in specialised grooves on their abdomen (Heatwole et al, 1962).…”