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Parasitoid Wasps: Neuroethology F Parasitoid Wasps: Neuroethology F. Libersat, Institut de Neurobiologie de la Me´ diterrane´ e, Parc Scientifique de Luminy, Marseille, France ã 2010 Elsevier Ltd. All rights reserved. Introduction prey usually inflict a single or double sting to the prey item. This typically results in deep paralysis by affecting, for Predators as diverse as snakes, scorpions, spiders, insects, example, the peripheral nervous system (i.e., the neuromus- and snails manufacture venoms to incapacitate their prey. cular junction: synapse between the motoneurone terminals Most venoms contain a cocktail of neurotoxins and each and the muscle). In those species of wasps where the paral- neurotoxin is designed to target-specific receptors in the yzing venom is injected into the hemolymph of the prey, as nervous and muscular systems. Most neurotoxins act per- in the beewolf (the Egyptian digger wasp Philanthus trian- ipherally and interfere with the ability of the prey’s nervous gulum), the venom has been shown to affect the peripheral system to generate muscle contraction or relaxation, result- nervous system (Figure 1). P. triangulum feeds its larvae ing in immobilization and often death of the prey to be almost exclusively with Honeybees (Apis mellifera). The consumed immediately. However, in a few species of pred- beewolf paralyzes bees by stinging them on the ventral atory wasps, venoms appear to act centrally to induce side of the thorax through the membrane between the first various behaviors. These venomous wasps use mostly and second segments. These wasps are sufficiently strong to other insects or spiders as food supply for their offspring. airborne cargo the prey item back to the nest (Figure 1(a)). Most parasitoid wasps eat only nectar from flowers and After provisioning the nest with a few bees, the wasp lays other small insects, but as larvae they eat something totally an egg in it and seals it. The venom of the beewolf different. Many of these wasps paralyze their prey and then contains potent neurotoxins known as philanthotoxins, lay one or more eggs in or on the host, which serves as a which evoke neuromuscular paralysis in the bee prey. food source for the hatching larvae. In a few instances, the Such philanthotoxins interfere presynaptically and post- parasitoid wasp often manipulates the host’s behavior in a synaptically with glutamatergic synaptic transmission manner that is beneficial to and facilitates the growth and (Figure 1(b)). Because glutamate is the neurotransmitter development of its offspring. Although the alteration of at the insect neuromuscular junction, philanthotoxins host behavior by parasitoids is a widespread phenomenon, in the venom block the neuromuscular transmission the underlying neuronal mechanisms are only now begin- to induce flaccid paralysis of the prey. One potent com- ning to be deciphered. As of today, only a few behavioral ponent of the Philanthus venom is d-philanthotoxin, alterations can be unambiguously linked to alterations in which blocks open ionotropic glutamate receptors in the central nervous system (CNS). the insect neuromuscular junction (Figure 1(b)). Para- The direct manipulation of the host nervous system and doxically, the very same d-philanthotoxin blocks gluta- behavior may take several forms. In some instances, the mate uptake (it interferes with the glutamate transporter) venom is purely paralytic, affecting either the peripheral at the insect neuromuscular junctions thereby, pro- or CNS to induce partial or total paralysis, which can be longing the presence of glutamate at the neuromuscular transient (seconds to minutes) or long-term (hours to days). junction (Figure 1(b)). This venom-induced hyperexci- In other instances, the venom might affect behavioral sub- tation of muscle contraction is presumably responsible for routines to produce finer manipulations of the host behav- the initial tremor, which immobilizes the prey until flaccid ior. In this article, I will discuss selected case studies where paralysis begins. Hyperexcitation preceding flaccid paraly- the neural mechanisms underlying host manipulation by sis is a common venom strategy seen in several types of parasitoid wasps have been identified. I will then focus on venomous animals, such as octopus, spiders, coelenterates, one case study where a wasp hijacks the brain of its host to and some cone snails where the hyperexcitation is produced control its motivation to perform specific behaviors. by different classes of substances. Apparently, the hyperex- Most ectoparasitoid wasps incapacitate their prey and citation immediately immobilizes the prey, so that it cannot then drag it to a burrow or a nest. In this protected nest, get out of reach of the predator, until the slower acting the wasp lays its egg on the prey and seals the burrow with flaccid paralysis begins. The wasp paralyzes several bees the inert prey inside. When the larva later hatches, it feeds and drags them into a concealed burrow. It then lays an on the host, ultimately killing it, and pupates in the nest, egg on one of the bees, seals the burrow, and leaves. The sheltered from predators that could harm the cocoon. The hatching larva is, thus, provided with a large, paralyzed hunting and host-manipulation strategies of these wasps food supply to feed on until pupation. are diverse and, at least to some extent, depend on the host On the other hand, wasps, which hunt on large prey natural behavior. Hunters of relatively small or harmless such as tarantula spiders, face a much more considerable 642 Parasitoid Wasps: Neuroethology 643 (a) (b) (a) Presynaptic motoneuron Ca++ Ca++ GLUT (c) (d) GLU - Figure 2 (a) The spider wasp, Tachypompilus ignitus, dragging GLU an immobilized Palystes spider to her nest. (b) The tomato Philanthus hornworm, Manduca, parasitized by the solitary braconid venom endoparasitoid wasp Cotesia pupae. (c) The normal web of the Na+ orb-weaving spider P. argyra. (d) The cocoon web of a spider GLU – R parasitized by the Ichneumonid wasp and wasp cocoon from above. K+ Muscle (b) fiber Figure 1 (a) A photograph of an air-borne Philanthus wasp egg after 2 days and feeds on the entombed spider for carrying its bee prey back to the nest. (b) Schematic 5–7 days. The satiated larva then pupates inside the nest, representation of the insect neuromuscular junction where safe from predators. Philanthus venom affects glutamatergic synaptic transmission. As we shall see in this article, some parasitoid wasps alter Calcium (Ca++) ions move in when an action potential (blue arrow) reaches the motoneuron terminal and facilitates the the behavior of their host to the finest degree. The unique vesicular release of glutamate (GLU). One potent component of effects of such wasp’s venom on prey behavior suggest that the Philanthus venom (d-philanthotoxin) blocks open ionotropic the venom targets the prey’s CNS. A remarkable example of glutamate receptors (GLUR) and glutamate uptake (GLUT)to such manipulation is that of the braconid parasitoid wasp induce muscular paralysis. (Glyptapanteles sp.) that induces a caterpillar (Thyrinteina leucocerae) to behave as a bodyguard of its offspring. After parasitoid larvae exit from the host to pupate, the host danger (Figure 2(a)). The tarantula-hawk (Pepsis) is the remains alive but displays stunning modifications in its fearsome enemies of spiders. These wasps usually first behavior: it stops feeding and remains close to the parasitoid disarm the spider of its most powerful weapon, the pupae to defend these against predators with violent head fangs, with multiple stings into the cephalo-thorax but swings. The parasitized caterpillar dies soon after while sometimes directly in the mouth. After this stinging unparasitized caterpillars do not show any of these behav- sequence, the spider is totally paralyzed, which allows ioral changes. In another example of host manipulation, the the wasp to drag the spider back to the nest, walking wasp Cotesia congregata and its host, the tobacco hornworm backwards facing its formidable opponent. Once the host Manduca sexta, we have some information about the under- is concealed, the wasp lays a single egg on the abdomen of lying mechanisms of manipulation. The female wasp injects the spider and seals the entrance to the nest. Depending a mixture consisting of venom, polydnavirus, and wasp eggs on the species, the spider would completely or nearly into its caterpillar host (Figure 2(a)). The wasp larvae hatch completely recover from paralysis within a few hours to and develop inside the host’s hemocoel, exit through the 2 months. If the tarantula survives what usually happens cuticle, and spin a cocoon which stays attached to the host. next, it can revive and continue living a normal life. But One day before exiting the host, host feeding and spontane- another fate awaits the spider as the larva hatches from the ous locomotion decline. The host remains in this torpor 644 Parasitoid Wasps: Neuroethology until death. The decline in host feeding and locomotion can from its burrow pursued by the wasp. The wasp then be induced by wasp larvae alone which, by an unknown wrestles with its prey to finally inflict multiple stings, chain of events, target the subesophageal ganglion (SEG) of mainly in the thoracic region. The stings induce a total the host to induce neural inhibition of locomotion. Further- transient paralysis of the legs, lasting just a few minutes. more, the change in host behavior is accompanied with an The wasp performs host feeding, sucking some hemo- elevation of CNS octopamine (OA), a neuromodulator, lymph before laying a single egg between the first and suggesting that alterations in the functioning of the octopa- second pairs of legs of the inert cricket. The wasp then minergic system may play a role in depressing host feeding leaves the cricket which fully recovers from paralysis and or locomotion. But, the most exquisite alteration of behavior burrows back into the ground, apparently resuming nor- ever attributed to a parasitoid wasp is probably the Ichneu- mal activity.
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