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Sensory arsenal on the stinger of the parasitoid jewel wasp and its possible role in identifying cockroach brains.

Gal R, Kaiser M, Haspel G, Libersat F - PLoS ONE (2014)

Bottom Line: Extracellular electrophysiological recordings from stinger afferents show increased firing rate in response to mechanical stimulation with agarose.This response is direction-selective and depends upon the concentration (density) of the agarose, such that the most robust response is evoked when the stinger is stimulated in the distal-to-proximal direction (concomitant with the penetration during the natural stinging behavior) and penetrating into relatively hard (0.75%-2.5%) agarose pellets.We conclude that the parasitoid jewel wasp uses at least mechanosensory inputs from its stinger to identify the brain within the head capsule of the cockroach prey.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Sciences and the Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva, Israel.

ABSTRACT
The parasitoid jewel wasp uses cockroaches as live food supply for its developing larva. To this end, the adult wasp stings a cockroach and injects venom directly inside its brain, turning the prey into a submissive 'zombie'. Here, we characterize the sensory arsenal on the wasp's stinger that enables the wasp to identify the brain target inside the cockroach's head. An electron microscopy study of the stinger reveals (a) cuticular depressions innervated by a single mechanosensory neuron, which are presumably campaniform sensilla; and (b) dome-shaped structures innervated by a single mechanosensory neuron and 4-5 chemosensory neurons, which are presumably contact-chemoreceptive sensilla. Extracellular electrophysiological recordings from stinger afferents show increased firing rate in response to mechanical stimulation with agarose. This response is direction-selective and depends upon the concentration (density) of the agarose, such that the most robust response is evoked when the stinger is stimulated in the distal-to-proximal direction (concomitant with the penetration during the natural stinging behavior) and penetrating into relatively hard (0.75%-2.5%) agarose pellets. Accordingly, wasps demonstrate a normal stinging behavior when presented with cockroaches in which the brain was replaced with a hard (2.5%) agarose pellet. Conversely, wasps demonstrate a prolonged stinging behavior when the cockroach brain was either removed or replaced by a soft (0.5%) agarose pellet, or when stinger sensory organs were ablated prior to stinging. We conclude that the parasitoid jewel wasp uses at least mechanosensory inputs from its stinger to identify the brain within the head capsule of the cockroach prey.

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The wasp uses mechanosensory inputs to identify the cockroach’s brain.(A) Mean (±SD) stinging duration after different surgical manipulations on the cockroach’s brain prior to a wasp’s sting (see text for details). Control (n = 30); ‘Brainless’ (n = 19); Brain replaced with agarose pellets: 0.25% (n = 12), 0.5% (n = 9), 0.75% (n = 8), 1% (n = 6), 2.5% (n = 12); brain injected with TTX (n = 6); Brain homogenized (n = 5). **p<0.01, ***p<0.001 (Kruskal-Wallis One-Way ANOVA on Ranks versus the control group). (B) Number of red pixels, indicative of amount of injected venom in hard (2.5%, n = 10) and soft (0.5%, n = 9) agarose pellets following a wasp’s sting. Inserts are representative photomicrographs of one hard (left) and one soft (right) agarose pellet extracted from cockroach heads immediately after the sting (Scale bars = 0.1 mm). ***p<0.001 (t-test).
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pone-0089683-g004: The wasp uses mechanosensory inputs to identify the cockroach’s brain.(A) Mean (±SD) stinging duration after different surgical manipulations on the cockroach’s brain prior to a wasp’s sting (see text for details). Control (n = 30); ‘Brainless’ (n = 19); Brain replaced with agarose pellets: 0.25% (n = 12), 0.5% (n = 9), 0.75% (n = 8), 1% (n = 6), 2.5% (n = 12); brain injected with TTX (n = 6); Brain homogenized (n = 5). **p<0.01, ***p<0.001 (Kruskal-Wallis One-Way ANOVA on Ranks versus the control group). (B) Number of red pixels, indicative of amount of injected venom in hard (2.5%, n = 10) and soft (0.5%, n = 9) agarose pellets following a wasp’s sting. Inserts are representative photomicrographs of one hard (left) and one soft (right) agarose pellet extracted from cockroach heads immediately after the sting (Scale bars = 0.1 mm). ***p<0.001 (t-test).

Mentions: Wasps introduced with surgically pre-treated cockroaches usually inflicted the two consecutive stings, first paralyzing the legs with a thoracic sting and then stinging into the head (Fig. 4). However, a Kruskal-Wallis one way ANOVA reveals that whereas the type of pre-treatment does not affect the duration of the thoracic-sting (H = 7.414, p = 0.493), it significantly affects the duration of the head-sting (H = 75.140, p<0.001). Concomitant with the electrophysiological data, the behavioral change depends on the mechanical cues that the stinger encounters inside the cockroach’s head capsule. More specifically, when wasps are introduced with ‘brainless’ cockroaches, from which the brain was completely removed prior to the sting, the head sting is dramatically prolonged often 10-fold and more (Fig. 4A). A similar prolongation of the head-sting occurs when wasps sting cockroaches in which the brain was surgically replaced with a low-density (0.25%–0.75%) agarose pellet. In contrast, the head-sting duration is normal if the cockroach’s brain is replaced with a high-density (0.75%–2.5%) agarose pellet (Fig. 4). The stinging duration appears to reflect events associated with the injection of venom inside the head of the cockroach, as pellets prepared with high-density but not with low-density agarose show traces of venom that can be detected after the sting (Fig. 4B). These results indicate that mechanosensory cues inside the head of the cockroach are sufficient to induce a normal stinging process, and that this sensory input is probably mediated by, at least, mechanosensitive sensilla distributed along the stinger. Furthermore, the head-sting duration is normal for TTX-injected cockroaches but is significantly increased for brain-homogenized cockroaches (Fig. 4A), suggesting that (a) electrical activity in the cockroach’s brain is not necessary for the head-stinging behavior; and (b) mechanical (but probably not chemical) cues are necessary for brain recognition and venom injection. The fact that TTX-injected and brain-homogenized cockroaches were behaviorally indistinguishable and showed the same behavior as “brainless” cockroaches (see [28]) indicates that behavioral cues also do not mediate the brain-recognition process. The specific chemosensory role of DS sensilla is therefore a subject for future study and may include, for example, monitoring venom concentrations proximal to the tip of the stinger during venom injection; determining host health-related factors or hyperparasitism, and more.


Sensory arsenal on the stinger of the parasitoid jewel wasp and its possible role in identifying cockroach brains.

Gal R, Kaiser M, Haspel G, Libersat F - PLoS ONE (2014)

The wasp uses mechanosensory inputs to identify the cockroach’s brain.(A) Mean (±SD) stinging duration after different surgical manipulations on the cockroach’s brain prior to a wasp’s sting (see text for details). Control (n = 30); ‘Brainless’ (n = 19); Brain replaced with agarose pellets: 0.25% (n = 12), 0.5% (n = 9), 0.75% (n = 8), 1% (n = 6), 2.5% (n = 12); brain injected with TTX (n = 6); Brain homogenized (n = 5). **p<0.01, ***p<0.001 (Kruskal-Wallis One-Way ANOVA on Ranks versus the control group). (B) Number of red pixels, indicative of amount of injected venom in hard (2.5%, n = 10) and soft (0.5%, n = 9) agarose pellets following a wasp’s sting. Inserts are representative photomicrographs of one hard (left) and one soft (right) agarose pellet extracted from cockroach heads immediately after the sting (Scale bars = 0.1 mm). ***p<0.001 (t-test).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC3935893&req=5

pone-0089683-g004: The wasp uses mechanosensory inputs to identify the cockroach’s brain.(A) Mean (±SD) stinging duration after different surgical manipulations on the cockroach’s brain prior to a wasp’s sting (see text for details). Control (n = 30); ‘Brainless’ (n = 19); Brain replaced with agarose pellets: 0.25% (n = 12), 0.5% (n = 9), 0.75% (n = 8), 1% (n = 6), 2.5% (n = 12); brain injected with TTX (n = 6); Brain homogenized (n = 5). **p<0.01, ***p<0.001 (Kruskal-Wallis One-Way ANOVA on Ranks versus the control group). (B) Number of red pixels, indicative of amount of injected venom in hard (2.5%, n = 10) and soft (0.5%, n = 9) agarose pellets following a wasp’s sting. Inserts are representative photomicrographs of one hard (left) and one soft (right) agarose pellet extracted from cockroach heads immediately after the sting (Scale bars = 0.1 mm). ***p<0.001 (t-test).
Mentions: Wasps introduced with surgically pre-treated cockroaches usually inflicted the two consecutive stings, first paralyzing the legs with a thoracic sting and then stinging into the head (Fig. 4). However, a Kruskal-Wallis one way ANOVA reveals that whereas the type of pre-treatment does not affect the duration of the thoracic-sting (H = 7.414, p = 0.493), it significantly affects the duration of the head-sting (H = 75.140, p<0.001). Concomitant with the electrophysiological data, the behavioral change depends on the mechanical cues that the stinger encounters inside the cockroach’s head capsule. More specifically, when wasps are introduced with ‘brainless’ cockroaches, from which the brain was completely removed prior to the sting, the head sting is dramatically prolonged often 10-fold and more (Fig. 4A). A similar prolongation of the head-sting occurs when wasps sting cockroaches in which the brain was surgically replaced with a low-density (0.25%–0.75%) agarose pellet. In contrast, the head-sting duration is normal if the cockroach’s brain is replaced with a high-density (0.75%–2.5%) agarose pellet (Fig. 4). The stinging duration appears to reflect events associated with the injection of venom inside the head of the cockroach, as pellets prepared with high-density but not with low-density agarose show traces of venom that can be detected after the sting (Fig. 4B). These results indicate that mechanosensory cues inside the head of the cockroach are sufficient to induce a normal stinging process, and that this sensory input is probably mediated by, at least, mechanosensitive sensilla distributed along the stinger. Furthermore, the head-sting duration is normal for TTX-injected cockroaches but is significantly increased for brain-homogenized cockroaches (Fig. 4A), suggesting that (a) electrical activity in the cockroach’s brain is not necessary for the head-stinging behavior; and (b) mechanical (but probably not chemical) cues are necessary for brain recognition and venom injection. The fact that TTX-injected and brain-homogenized cockroaches were behaviorally indistinguishable and showed the same behavior as “brainless” cockroaches (see [28]) indicates that behavioral cues also do not mediate the brain-recognition process. The specific chemosensory role of DS sensilla is therefore a subject for future study and may include, for example, monitoring venom concentrations proximal to the tip of the stinger during venom injection; determining host health-related factors or hyperparasitism, and more.

Bottom Line: Extracellular electrophysiological recordings from stinger afferents show increased firing rate in response to mechanical stimulation with agarose.This response is direction-selective and depends upon the concentration (density) of the agarose, such that the most robust response is evoked when the stinger is stimulated in the distal-to-proximal direction (concomitant with the penetration during the natural stinging behavior) and penetrating into relatively hard (0.75%-2.5%) agarose pellets.We conclude that the parasitoid jewel wasp uses at least mechanosensory inputs from its stinger to identify the brain within the head capsule of the cockroach prey.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Sciences and the Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva, Israel.

ABSTRACT
The parasitoid jewel wasp uses cockroaches as live food supply for its developing larva. To this end, the adult wasp stings a cockroach and injects venom directly inside its brain, turning the prey into a submissive 'zombie'. Here, we characterize the sensory arsenal on the wasp's stinger that enables the wasp to identify the brain target inside the cockroach's head. An electron microscopy study of the stinger reveals (a) cuticular depressions innervated by a single mechanosensory neuron, which are presumably campaniform sensilla; and (b) dome-shaped structures innervated by a single mechanosensory neuron and 4-5 chemosensory neurons, which are presumably contact-chemoreceptive sensilla. Extracellular electrophysiological recordings from stinger afferents show increased firing rate in response to mechanical stimulation with agarose. This response is direction-selective and depends upon the concentration (density) of the agarose, such that the most robust response is evoked when the stinger is stimulated in the distal-to-proximal direction (concomitant with the penetration during the natural stinging behavior) and penetrating into relatively hard (0.75%-2.5%) agarose pellets. Accordingly, wasps demonstrate a normal stinging behavior when presented with cockroaches in which the brain was replaced with a hard (2.5%) agarose pellet. Conversely, wasps demonstrate a prolonged stinging behavior when the cockroach brain was either removed or replaced by a soft (0.5%) agarose pellet, or when stinger sensory organs were ablated prior to stinging. We conclude that the parasitoid jewel wasp uses at least mechanosensory inputs from its stinger to identify the brain within the head capsule of the cockroach prey.

Show MeSH
Related in: MedlinePlus