Mechanisms of Venom Injection and Behavioral Modulation of a Cockroach Prey by a Parasitoid Wasp

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Mechanisms of Venom Injection and Behavioral Modulation of a Cockroach Prey by a Parasitoid Wasp Mechanisms of Venom Injection and Behavioral Modulation of a Cockroach Prey by a Parasitoid Wasp Thesis submitted in partial fulfillment of the requirements for the degree of “DOCTOR OF PHILOSOPHY” by Ram Gal Submitted to the Senate of Ben-Gurion University of the Negev March 2010 Beer-Sheva Mechanisms of Venom Injection and Behavioral Modulation of a Cockroach Prey by a Parasitoid Wasp Thesis submitted in partial fulfillment of the requirements for the degree of “DOCTOR OF PHILOSOPHY” by Ram Gal Submitted to the Senate of Ben-Gurion University of the Negev Approved by the advisor ___________________ Approved by the Dean of the Kreitman School of Advanced Graduate Studies ____________ March 2010 Beer-Sheva This work was carried out under the supervision of Prof. Frederic Libersat In the Department of Life Sciences Faculty of Natural Sciences Acknowledgments Throughout my seven years at the Libersat lab, more than a few people have helped and supported me personally and scientifically. I would like to thank a handful of them. First and foremost, I would like to express my utmost gratitude to my advisor, Prof. Frederic Libersat, for his invaluable help and support throughout my studies. I consider myself privileged to have been given the opportunity to work and learn from Fred for so long. His high standards and ambition, as well as his vast knowledge and sincere passion for science, have inspired me throughout the years and have shaped my perception of science for years to come. I would also like to thank Jose Gustavo Glusman for his technical help, valuable advice and companionship throughout the years; Gal Haspel, who was my mentor as a young scientist, for teaching me the very essentials of the scientific rationale and academic writing; the Zlotowski Center for Neuroscience for providing help, financial support and a fruitful scientific environment; and the Journal of Experimental Biology for granting me a travel fellowship for a two-month research project in The Netherlands. A special thanks to former colleagues and students in the lab, to my friends (and especially Yael Lavi, Idan Harpaz and Rotem p. Uzan) and to my brother Idan and my sister Bar, for brainstorming, advice and help throughout the years. Last, but not least, I want to thank my loving parents, without whose support I would have never made it through. This work is dedicated to them. To my parents, Gidi and Orit Gal, who made it possible. Table of Contents List of abbreviations................................................................................................................ i List of figures ..........................................................................................................................ii Abstract .................................................................................................................................... 1 1. General introduction 1.1. Background .................................................................................................................... 4 1.2. From stimulation to action: a behavioral model........................................................... 11 1.3. Prior mechanistic investigations of the venom-induced hypokinesia........................... 15 1.4. Research goals.............................................................................................................. 16 2. Published work 2.1. Synopsis of the published work.................................................................................... 17 2.2. New vistas on the initiation and maintenance of insect motor behaviors revealed by specific lesions of the head ganglia 2.3. A parasitoid wasp manipulates the drive for walking of its cockroach prey 2.4. A wasp manipulates neuronal activity in the sub-esophageal ganglion to decrease the drive for walking in its cockroach prey 2.5. Parasitoid wasp uses a venom cocktail injected into the brain to manipulate the behavior and metabolism of its cockroach prey 3. Unpublished work: Sensory mechanisms mediating host CNS localization 3.1. Background .................................................................................................................. 21 3.2. Materials and Methods ................................................................................................. 22 3.3. Results and Discussion 3.3.1. Behavioral experiments......................................................................................... 30 3.3.2. Electron Microscopy ............................................................................................. 32 3.3.3. Electrophysiology.................................................................................................. 35 4. General discussion 4.1. Parasite-induced manipulation of host behavior in insects........................................... 38 4.2. Hunting strategies of parasitoid wasps......................................................................... 42 4.3. Overview and general discussion of the published work 4.3.1. The descending influence of cerebral ganglia on cockroach motor behaviors...... 45 4.3.2. The venom depresses the cockroach’s drive for walking...................................... 47 4.3.3. Involvement of the SEG in venom-induced hypokinesia...................................... 49 4.4. How the Jewel Wasp ‘hijacks the free will’ of cockroaches: Current mechanistic hypothesis............................................................................................................................ 50 6. References..............................................................................................................57 List of abbreviations CBC: central body complex CNS: central nervous system CPG: central pattern generator DA: dopamine Df: fast coxal depressor Ds: slow coxal depressor DUM: dorsal unpaired medial EMG: electromyogram GI: giant interneuron OA: octopamine SEG: sub-esophageal ganglion SEM: scanning electron microscope SupEG: supra-esophageal ganglion TAG: terminal abdominal ganglion TI: thoracic interneuron TEM: transmission electron microscope VNC: ventral nerve cord ~ i ~ List of figures Figure 1: The stinging behavior and life cycle of the Jewel Wasp, Ampulex compressa …………………………………………………………………………. 6 Figure 2: Ampulex compressa stings directly into the cerebral ganglia of its cockroach prey ……………………………………………………………………. 10 Diagram 1: A simplified model for the homeostatic control of behavior ……….. 12 Figure 3: The basic escape circuitry of the cockroach and hypothesized sites of action of the venom ………………………………………………………….... 14 Figure 4: Surgical procedures used throughout my research …………………….. 18 Figure 5: Wasp recording set-up ………………………………………………..... 29 Figure 6: Stinging duration after cockroach CNS lesions ……………………....... 31 Figure 7: SEM analysis of the wasp’s stinger ……………………..……………… 33 Figure 8: TEM analysis of the wasp’s stinger …………………………………….. 34 Figure 9: Stinger responses to mechanical stimulation …………………………… 36 Figure 10: Stinger responses to chemical stimulation ……………………………. 37 Figure 11: Examples of fatal interactions between parasites and their insect hosts ..……………………………………………………………………………... 41 Figure 12: Current model of the neurophysiological events leading to venom- induced hypokinesia in cockroaches stung by Ampulex compressa .……………… 55 ~ ii ~ Abstract The parasitoid Jewel Wasp Ampulex compressa hunts cockroaches as live food supply for its offspring. In doing so, the wasp stings a cockroach in the head and injects a venom cocktail directly and precisely into the cerebral ganglia, which are considered ‘higher-order’ neuronal centers in insects. The sting induces a unique behavioral manipulation of the cockroach prey. Although not paralyzed, the stung cockroach becomes hypokinetic and fails to initiate spontaneous or evoked locomotion for several days. The wasp grabs one of the cockroach’s antennae and steers the cockroach, walking backwards with the cockroach following in a docile manner like a dog on a leash, into a pre-selected nest or burrow. Intoxicated by the wasp’s venom, the stung cockroach does not put up a fight nor try to escape when the wasp lays an egg on its cuticle, seals the nest with debris and leaves. A larva hatches from the egg two days later and feeds on the live cockroach, protected in its nest from potential predators, for four more days. Then, when ready to pupate, the larva weaves a cocoon inside the abdomen of its cockroach host - which is at this stage not more than an empty shell - and undergoes metamorphosis. It hatches a month later as an adult ready to continue its life cycle. The purpose of my study was to characterize the mechanisms which allow the Jewel Wasp to induce this precise behavioral manipulation and ‘hijack the free will’ of its cockroach prey, rendering the cockroach a docile ‘automaton’ unwilling to escape its fate. As a first step, and since the sting is directed at the two cerebral ganglia of the cockroach prey, I explored how each of these ganglia individually regulate locomotion in non-stung cockroaches. To this end, I developed and validated a methodology for selectively removing descending inputs from each cerebral ganglion to thoracic motor centers in behaving cockroaches. By combining behavioral and electrophysiological tools, I constructed a functional model to describe how different stimuli evoke different motor patterns in cockroaches, and how these are separately regulated by each cerebral ganglion. I found that walking-related behaviors are differentially regulated by
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