More About This Article - Instituto de Zoología y ...izt.ciens.ucv.ve/ecologia/Archivos/ECO_POB...

Subscriber access provided by Ben Gurion University Library

is published by the American Chemical Society. 1155 Sixteenth Street N.W.,Washington, DC 20036

Manipulation of Host Behavior by Parasitic Insects and Insect ParasitesFrederic Libersat, Antonia Delago, and Ram Gal

Annual Review of Entomology, Annu. Rev. Entomol., ento, 2009, 54 (189-207 • DOI: 10.1146/annurev.ento.54.110807.090556

Downloaded from http://pubs.acs.org on December 12, 2008

More About This Article

Additional resources and features associated with this article are available within the HTML version:

• Supporting Information• Access to high resolution figures• Links to articles and content related to this article• Copyright permission to reproduce figures and/or text from this article

Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.

http://arjournals.annualreviews.org/doi/full/10.1146/annurev.ento.54.110807.090556

ANRV363-EN54-10 ARI 23 October 2008 11:38

Manipulation of HostBehavior by Parasitic Insectsand Insect ParasitesFrederic Libersat,1 Antonia Delago,2 and Ram Gal21Institut de Neurobiologie de la Mediterranee, Parc scientifique de Luminy, BP13,13273 Marseille cedex 09, France; email: [email protected] of Life Sciences, Ben-Gurion University of the Negev, P.O. Box 653,Be’er Sheva, 84105 Israel

Annu. Rev. Entomol. 2009. 54:189–207

The Annual Review of Entomology is online atento.annualreviews.org

This article’s doi:10.1146/annurev.ento.54.110807.090556

Copyright c© 2009 by Annual Reviews.All rights reserved

0066-4170/09/0107-0189$20.00

Key Words

wasp, worm, brain, neurons, amines

AbstractParasites often alter the behavior of their hosts in ways that are ulti-mately beneficial to the parasite or its offspring. Although the alterationof host behavior by parasites is a widespread phenomenon, the under-lying neuronal mechanisms are only beginning to be understood. Here,we focus on recent advances in the study of behavioral manipulationvia modulation of the host central nervous system. We elaborate on afew case studies, in which recently published data provide explanationsfor the neuronal basis of parasite-induced alteration of host behavior.Among these, we describe how a worm may influence the nervous sys-tem of its cricket host and manipulate the cricket into committing sui-cide by jumping into water. We then focus on Ampulex compressa, whichuses an Alien-like strategy for the sake of its offspring. Unlike most ven-omous hunters, this wasp injects venom directly into specific cerebralregions of its cockroach prey. As a result of the sting, the cockroachremains alive but immobile, but not paralyzed, and serves to nourishthe developing wasp larva.

189

Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


INTRODUCTION

Parasites alter host behaviors such as photo-taxis, locomotion, behavioral fevers, foragingbehavior, reproduction, and a variety of socialinteractions, to name only a few (43, 65, 74).Although such alteration of host behavior byparasites is a widespread phenomenon, the un-derlying mechanisms are only beginning to bedeciphered. Effects of parasites on host behav-ior can be direct, for example by manipulat-ing the nervous system, or indirect by manipu-lating the immune or endocrine system or themetabolism of the host (2, 43). In this review,we survey the effects of parasites on host behav-ior that result from directly hijacking the host’snervous system. Our focus is on parasitic insectsand insect parasites. Two intriguing examples ofsuch extreme manipulation have been investi-gated intensively. The first example is the sui-cidal behavior of crickets infected by Gordianworms, and the second is the zombification ofcockroaches by jewel wasps. We describe thesetwo case studies in detail to exemplify neuro-chemical strategies used by parasites to manip-ulate the behavior of their insect hosts.

Parasites have evolved remarkable strategiesto manipulate the behavior of their hosts in or-der to perpetuate their own genes. Among themost dramatic cases of such manipulation arethose that take place in parasitized insects. Be-cause it is the nervous system that generatesbehavior, for a given behavioral manipulationto occur, parasites must manufacture chemicalsthat in one way or another affect the CNS oftheir hosts. Over time, several extreme forms ofbehavioral manipulation have evolved in whichthe parasite eventually controls the ‘free will’ ofits host.

HOST MANIPULATION LEADINGTO SUICIDE

Some parasitic fungi and worms manipulatetheir hosts in a way that ultimately leads tosuicidal behavior. For example, an ant fallingvictim to a parasitic fungus of the genus Cordy-ceps is manipulated in its behavior to facilitate

dispersal of the fungus, thereby optimizing theparasite’s chances of reproduction. To this end,Cordyceps fungi produce chemicals that alter thenavigational sense of their ant hosts (39, 40).It begins with the attachment of the sporesof the fungus to the cuticle of the ant. Thespores then germinate and break into the ant’sbody by diffusing through the tracheae. Fungalmycelia then grow by feeding on the host’s or-gans, avoiding vital ones. The fungus then pro-duces certain, yet unidentified, chemicals thatcause the ant to climb to the top of a tree orplant and clamp its mandibles around a leaf orleafstalk to stay in place. When the fungus isready to sporulate, it eventually feeds on theant’s brain and thus kills it. The fruiting bodiesof the fungus then sprout out of the cuticle andrelease capsules filled with spores (Figure 1a).The airborne capsules explode on their descent,spreading the spores over the surrounding areato infect other ants and thus start anothercycle.

Ants, such as Formica fusca, can fall vic-tim to another, phylogenetically distant parasitethat has adapted a similar strategy to disperse.The lancet liver fluke (Dicrocoelium dendriticum)takes over the ant’s navigational skills and co-erces it into climbing to the tip of a blade ofgrass (31, 42). Clamped there, the infected antawaits to be devoured by a cow or some othergrazer passing by. For this parasite the cyclestarts with a mature lancet fluke that settles intothe liver of its final host. There, it produceseggs that are washed out in the bile and endup in the digestive system of the grazer to exitin its droppings. The first intermediate host, aterrestrial snail, feeds on such droppings andswallows the eggs, which then hatch in the in-testines. The larvae (cercariae) drill through thewall of the snail’s gut and settle in its digestivetract, where they develop into a juvenile stage.The snail then excretes the parasites in a ballof slime. Ants, the second intermediate hosts,swallow these slime balls loaded with hundredsof lancet flukes, thereby allowing the parasitesto enter the ant’s gut and for a while wan-der through its body in the hemocoel. Then,the most peculiar thing happens as all but one

190 Libersat · Delago · Gal

Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


a

c

b

Figure 1Examples of fatal interactions between parasites and their insect hosts. (a) The Camponotus ant, mandibleslocked onto a leafstalk, with Hirsutella, the anamorph of Cordyceps unilateralis, emerging from the cuticle(courtesy and copyright of L. Gilbert). (b) The hairworm Tellinii spinochordodes emerging from a host cricket,Nemobius sylvestris, after inducing suicidal behavior in the host (courtesy and copyright of F. Thomas). (c) Thecockroach Periplaneta americana stung in the brain by Ampulex compressa (courtesy and copyright of R. Gal).

cercaria encyst in the hemocoel. This individu-alist/altruist migrates to penetrate into and en-cyst in the subesophageal ganglion (SEG) (inCamponotus it sometimes settles in the brain;37, 38, 52). When evening approaches and theair cools, the infested ant leaves the colony andmoves upward to the top of a blade of grass.Once there, it clamps its mandibles onto the topof the blade and stays, waiting to be devouredby some grazer. At the break of day, if the antwas spared during the night, it returns to theground and acts as if nothing happened. Whenevening comes again, the fluke takes over oncemore and sends the ant back up the grass foranother attempt (58). The chemicals that thefluke releases to manipulate the behavior of theant, as in the previous example, have not beencharacterized, yet.

SEG: subesophagealganglion

Another example of behavioral manipula-tion that ultimately leads to suicidal behaviorof the host is observed in insects infected bynematode worms. Land insects do not usuallyjump into water, but infection by a nematodeof the genus Mermis has exactly this effect onthe behavior of parasitized ants. Infected antswill seek water, jump in, and eventually drown(38). Similar abnormal suicidal behavior is ob-served in grasshoppers and crickets infected byGordian worms (Figure 1b). Once the para-site reaches maturity, infected crickets seek outwater and obligingly commit suicide by drown-ing. Researchers assume that the larvae pro-duce certain chemicals that directly affect thehost’s brain, a hypothesis that might hold truefor other parasitic species as well. There is someevidence that the worm releases chemicals that

www.annualreviews.org • Manipulation of Host Behavior by Parasitic Insects and Insect Parasites 191

Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


Parasitic wasps: anumber of families ofwasps that lay theireggs inside or outsideof the larvae, pupae, oradult host arthropods

Parasitoid: anorganism that spends asignificant portion ofits life history attachedto or within a singlehost organism, whichit ultimately kills

disrupt the geotactic sense of its terrestrial host,causing it to jump into water so that the matureparasite, which is aquatic, can emerge (5).

HOST MANIPULATIONFOR OFFSPRING CARE

The caterpillar of the butterfly Maculinea rebeliis a parasite of ants that lives inside the broodchambers of ant nests, excreting chemicals thatmanipulate the ants to accept, nurture, and pro-tect the caterpillar as if it were their own. Thecaterpillar itself, however, also serves as hostfor the parasitoid wasp Ichneumon eumerus. Tosafely reach the caterpillar, which is protecteddeep within the ant colony, the wasp releasesagonistic chemicals to induce fighting betweenworker ants, locking the colony into combat andthus leaving its caterpillar host defenseless andavailable for oviposition (68).

Probably the most exquisite alteration of be-havior ever attributed to a parasitoid wasp isthe manipulation of spiders by the ichneumonidwasp Hymenoepimecis (12, 13). In this uniqueexample, the parasitoid wasp takes advantageof the natural behavior of the host. Whereasmost ectoparasitoid wasps completely paralyzethe host and drag it to an existing burrow ora burrow they dig themselves, H. argyraphagamakes the host construct the shelter for its fu-ture larva. The wasp stings its host, Plesiometaargyra (Araneidae), on the spider’s web. Thesting evokes a total but transient paralysis dur-ing which the wasp lays its egg on the para-lyzed spider. After recovery from the sting thespider resumes apparently normal activity. Itbuilds normal orb webs to catch prey while thewasp’s egg hatches and the larva grows by feed-ing on the spider’s hemolymph. After approx-imately two weeks, just before the wasp larvais about to kill it, a dramatic behavioral changeoccurs in the spider: Motivated by a so far un-known cause, it starts weaving a unique webwith a design tailored to fit the needs of the larvafor its next stage in development, the metamor-phosis. The new web is different from the nor-mal orb-shaped web of P. argyra and is designedto support the wasp’s cocoon so that it is sus-

pended in the air. The wasp larva consumes thespider, ultimately killing it, and then pupates,suspending itself on the newly formed web. Itappears that the larva chemically manipulatesthe spider’s nervous system to cause the exe-cution of only one subroutine of the full orbweb construction program while repressing allother routines. The nature of the chemicals in-volved in this extreme alteration of the spider’sbehavior remains to be explored.

Most ectoparasitoid wasps do not use suchcomplicated strategies to manipulate host be-havior. They often incapacitate their prey andthen drag it into a burrow or nest. There,where the host is relatively concealed fromother potential predators, the wasp lays an eggon the prey and seals the burrow with theinert prey inside. When the larva hatches, itfeeds on the host, ultimately killing it, and pu-pates in the nest sheltered from predators thatmight harm the cocoon. The hunting and host-manipulation strategies of these wasps are di-verse and, at least to some extent, depend onthe natural behavior of the host. As a generalrule, there is a good correlation between the sizeof the prey and its ability to damage the wasp,and the complexity of the hunting strategy andthe resulting behavioral manipulation. Huntersof relatively small or harmless prey usually in-flict a single or double sting. This results indeep paralysis or sometimes the death of theprey by affecting, for instance, neuromuscularjunctions. The bee wolf (or the Egyptian diggerwasp, Philanthus triangulum) is one well-studiedexample of a paralysis-inducing wasp. Its venomcontains potent neurotoxins known as philan-thotoxins that evoke neuromuscular paralysis inthe bee prey (48). The wasp paralyzes severalbees and drags them into a concealed burrow.It then lays an egg on one of the bees, sealsthe burrow, and leaves. The hatching larva isthereby provided with a large, paralyzed foodsupply to feed on until pupation.

Pompilid wasps (such as the tarantula hawkPepsis formosa) are the fearsome enemies of spi-ders, but they also face, like others that hunt onlarge prey, considerable danger during hunt-ing (44, 62). These wasps usually first disarm


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


the spider of its most formidable weapon, thefangs, with multiple, deeply paralyzing stingsinto the cephalothorax and sometimes directlyinto the mouth. After a complete stinging se-quence the spider is entirely paralyzed, whichallows the wasp to drag it back to the nest, walk-ing backward facing the huge prey. Once thehost is concealed, the wasp lays a single eggon the abdomen of the spider and seals the en-trance to the nest. Depending on the species,the spider may recover from paralysis within afew hours to two months. If an egg is laid, how-ever, the larva hatches after two days and feedson the entombed spider for 5–7 days. The sa-tiated larva then pupates inside the nest, safefrom predators and scavengers.

Like pompilids, sphecid wasps often huntlarge and potentially harmful prey, typicallyorthopteroids (such as crickets, katydids, andgrasshoppers). They usually sting their prey toevoke total transient paralysis, although in someinstances a more specific manipulation takesplace (62). One example of total transient paral-ysis can be found in the Larra wasp–mole cricketsystem (8). Mole crickets spend most of theirtime in a burrow. A larrine wasp (Larra anath-ema, for example) in hunting mood penetratesthe underground refuge of the cricket and at-tacks it. The frightened cricket may emerge inpanic from its burrow. The wasp wrestles withits prey to inflict multiple stings mainly in thethoracic region, inducing total transient paral-ysis of the legs that lasts just a few minutes. Itthen feeds on the cricket’s hemolymph, lays asingle egg, and leaves. The cricket soon fullyrecovers from the paralysis and burrows backinto the ground, resuming normal activity. Itseems that the wasp simply utilizes the naturaltendency of the cricket to burrow, which prob-ably eliminates the need for long-term paralysisand nesting of the host. The egg soon hatchesand the larva starts feeding on the cricket af-ter piercing the cuticle with its mandibles.The development from egg laying to pupa-tion lasts between two weeks to one month,during which the mole cricket behaves nor-mally, demonstrating complete recovery fromparalysis.

In a different species of a sphecid parasitoid,the wasp Liris niger first orients visually towardits nonfossorial cricket prey (usually Acheta do-mesticus) and touches it briefly with the antennalflagella, where chemical cues probably revealthe suitability of the prey. The wasp then grabsthe cricket and stings it close to the base of thehind legs or in the metathorax. Then it stingsthree more times, once into the prothorax, onceinto the mesothorax, and finally into the neck.The stings induce total transient paralysis of thelegs and the stung cricket becomes inert andunable to maintain posture for several minutes(21, 61, 62). The wasp then drags the paralyzedcricket to a burrow, glues an egg between itsfore- and middle legs, and seals the burrow withsoil particles or pebbles. After the burrow hasalready been sealed, the cricket’s legs fully re-cover from paralysis and the cricket can main-tain posture and even walk. Nevertheless, thestung cricket never attempts to escape the bur-row but rather, although not paralyzed, staysmotionless in its tomb. The wasp larva, afterhatching from the egg, feeds on the lethargiccricket and then pupates. Thus, the Liris venominduces not only total transient paralysis in thelegs but also a partial and irreversible paralysisthat renders the cricket prey submissive in itsfuture grave. It has been suggested that the lat-ter effect of the Liris venom is a result of theneck-sting, which is, in comparison, not typicalfor the mole cricket–hunting Larra, which doesnot evoke such long-term effects.

The currently best-understood direct ma-nipulation of a host behavior occurs betweenthe sphecid wasp Ampulex compressa and itscockroach prey (31, 72). After grabbing acockroach (usually Periplaneta americana) at thepronotum or the base of the wing, the waspinflicts a first sting into the thorax, renderingthe prothoracic legs transiently (1–2 min)paralyzed, and then a second sting into theneck, which is much more precise and time-consuming (Figure 1c). After the neck-stingthe cockroach is not physically paralyzed but itwaits at the stinging site, grooming itself fran-tically. Just as the grooming period is almostover, the wasp cuts the cockroach’s antennae


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


Cerebral ganglia:ganglia located in thehead of arthropods

with its mandibles, feeds on the hemolymph,and grabs one of the cockroach’s antennalstumps to lead the host to a preselected burrowfor oviposition, walking backward facing theprey. The stung cockroach follows the wasp ina docile manner. After gluing an egg onto thecuticle of the prey, the wasp exits the burrowand blocks the entrance with small pebbles col-lected nearby, sealing the lethargic host inside.The hatching larva then feeds on the livinghost, until it pupates inside the cockroach ab-domen, roughly eight days after the egg is laid.The host-handling behavior of A. compressa iscomplex and time-consuming. A recent studyshows that host-handling generally follows anordered sequence of events and that A. com-pressa females do not perform the host handlingsequence faster or manage to complete it morefrequently as they gain experience (32). Thesefindings support the hypothesis that the host-handling behavior of A. compressa is primarilygenetically programmed rather than learned.

Importantly, the long-lasting lethargic stateof the cockroach occurs only when the venomis injected into the head but not when it is in-jected solely into the thorax (16). In most soli-tary sphecid wasps, the host stinging sequence isrelatively constant and stings are usually appliedin close proximity to and in the same segmentof the paralyzed appendages. A common strat-egy applied by these wasps is a series of stings inthe location of different thoracic ganglia, some-times accompanied by a sting into the neck ofthe prey (16, 21, 47, 62). In all known cases, thefirst sting is directed at ganglia involved in lo-comotion and defense, thereby disarming theprey by inducing 2–60 min of total paralysis(62). For example, L. niger first stings in thedirection of the third thoracic ganglion, whichcontrols the jumping/kicking legs of the crickethost (15, 62), and Tachysphex costi and Stizus ru-ficornis, both of which prey on mantids, beginthe stinging sequence with a sting into the firstthoracic ganglion, rendering the front, raptoriallegs dangling paralyzed.

The effects of the venoms of the aforemen-tioned wasps on their host’s behavior suggestthat, in some instances, the venom affects tar-

gets within the CNS. In fact, venoms of soli-tary wasps usually consist of a cocktail of pro-teins, peptides, and subpeptidic components,some of which are unlikely to cross the thick andrather selective sheath around the nervous gan-glia (the arthropod blood-brain barrier). Thus,it is most unlikely that neurotoxins in the venommake their way into the CNS by simple diffu-sion from the hemolymph. It was suggested thatsome wasps use a common strategy of drug de-livery, injecting venom directly into a specificganglion of the nervous system. Using such astrategy, these wasps would achieve a local cen-tral paralysis to facilitate subsequent stings (intothe neck for example) uninterrupted or to ma-nipulate behavior in ways that are ultimatelybeneficial to their offspring (with the sting intothe head).

The issue of whether or not venom is in-jected directly inside the prey’s CNS was re-solved in the Ampulex/cockroach system. “Hot”wasps were produced by injecting them witha mixture of C14-radiolabeled amino acids,which were incorporated into the venom. Incockroaches stung by hot wasps, most of the ra-dioactive signal was found in the thoracic gan-glion and inside the two cerebral ganglia: thesupraesophageal ganglion (the brain) and theSEG. Only a small amount of radioactivity wasdetected in the surrounding, nonneuronal tis-sue of the head and thorax (26). A high concen-tration of radioactive signal was localized to thecentral part of the brain (posterior to the cen-tral complex and around the mushroom bod-ies) and around the midline of the SEG, butnot in the periphery of these ganglia. These ex-periments represent, to date, the only unequiv-ocal demonstration that a wasp injects venomdirectly into the CNS of its prey. The preciseanatomical targeting of the wasp’s sting throughthe body wall and ganglionic sheath and intospecific areas of the brain is thus akin to themost advanced stereotactic delivery of drugs(26). A. compressa is almost certainly not theonly wasp that injects venom directly into theCNS, although the use of such a method of drugdelivery in other wasp species remains to beproven.


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


GORDIAN WORMS DRIVE THEIRINSECT HOSTS TOSUICIDAL BEHAVIOR

A striking example of behavioral manipulationthat leads to suicidal behavior in the host isobserved between hairworms, nematomorphs,and insects. Adult hairworms of the class Gordi-ida are free-living in water. The juveniles, how-ever, are parasitic in land-dwelling arthropodssuch as insects and spiders. Hairworms, there-fore, have to make two critical transitions dur-ing their life cycle. The first transition is thatfrom an aquatic larva to the terrestrial definitivehost, and the second is from the definitive hostback into water.

The first transition is ruled by chance andbears a high risk. It occurs when a definitivehost ingests parasitic larvae directly or indi-rectly through an intermediate host, typicallyaquatic organisms such as insect larvae (22,23). During development inside the definitivehost, the initially microscopic larvae grow to be-come large worms, the size (primarily length) ofwhich eventually exceeds that of the host by aconsiderable amount (three to four times). Be-cause the usual hosts are terrestrial arthropods,the second transition, back into water, is a chal-lenging task for most hairworm species. Insectsharboring mature hairworms display a behav-ior in favor of the parasite that is originally ab-sent from the host’s usual repertoire—they seekwater and jump in (66). The adult worm thenemerges from the host (Figure 1b) and activelyleaves it by swimming away to find a matingpartner. Infected hosts usually show unalteredbehavior during daytime; only at night do theinsects go in search of water.

NEW TOOLS TO STUDY THEBIOCHEMICAL CROSS-TALKBETWEEN HOST AND PARASITE

How does the parasite interfere with the hostto lead it to suicide? Is it thirst motivated bymanipulation through the parasite that resultsin water-seeking behavior? Does the worm hi-jack the host’s nervous system and override all

Proteome: the entirecomplement ofproteins expressed by agenome, cell, tissue, ororganism at a giventime under definedconditions

Parasitoproteomics:the study of thereaction of the hostand parasite genomesthrough the expressionof the host andparasite proteomes

endogenous behavior? Is a small change in oneparticular brain center, protein, or gene enoughto lead to such a dramatic effect? Although thereis some evidence for parasite interference withhost neuroendocrine signaling systems (1, 10,29, 30, 45), in most cases the mechanisms thatunderlie such a dramatic behavioral change areunknown.

Biron and colleagues (4) looked into themechanisms underlying the observed behav-ioral change in the insect host using pro-teomics. Proteomics is a rather young disci-pline that marks the postgenomic era. It hasbeen initiated to complement physical genomicresearch and can be defined as the qualita-tive and quantitative comparison of proteomes(genome operating systems) under differentconditions to unravel biological processes. Al-though proteomics offers a variety of tools andapproaches, one of its major drawbacks stilllies in the qualitative analysis of the collecteddata. Like RNA microarrays, proteomics oftenproduces a vast amount of data, the interpre-tation of which leads to more questions thananswers. Nevertheless, it is the opportunity tostudy the host-parasite interaction during themanipulative process that makes proteomicsa unique and well-suited tool for exploringthe proximate mechanisms responsible for hostmanipulation.

SIGNIFICANT CHANGES INTAURINE LEVELS DURINGTHE MANIPULATION PHASE

To determine how the Gordian worm manip-ulates the behavior of its host, Biron and hiscolleagues used parasitoproteomics to charac-terize proteins synthesized by the host and theparasite and to look into potential cross-talk(4, 5). They detected many proteins that inter-fere with the neurotransmitter systems involvedin the geotactic behavior of the host species(4–6). The genes encoding these proteins arecontained in the worm’s genome but have a di-rect effect on the host CNS when they are ex-pressed. The relationship between the Gordianworm and its host, therefore, is a good example


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


Monoamines:a group ofneurotransmitters andneuromodulators thatcontain one aminogroup connected to anaromatic ring by atwo-carbon chain

5HT:5-hydroxytryptamine(serotonin)

DA: dopamine

of what Dawkins (9) designated the “extendedphenotype,” whereby genes expressed by oneorganism have an effect on the appearanceand/or behavior of another. Another examplewould be entomopathogenic fungi and theirhosts (55).

Thomas et al. (67) first looked more gen-erally at the level of polyamines, monoamines,and amino acids in hosts and parasites. Theauthors defined different groups of individu-als by whether or not the host was infectedand the time when individuals were capturedby the observers. They found that spermi-dine, which is involved in cellular metabolism,showed significant differences in expression be-tween infected and noninfected individuals andbetween day and night. The study did not de-tect serotonin (5HT) variations and only slightday/night variations in the levels of dopamine(DA).

During the manipulation process the aminoacids taurine, valine, and tyrosine showed sig-nificant changes. However, it remains unclearif these changes are causes or consequencesof the manipulative process. Infected cricketsdisplayed the highest concentrations of tau-rine during the day. Taurine is an importantneurotransmitter in insects: It is one of themost abundant free amino acids in the insectbrain and participates in neurotransmission inthe mushroom bodies (3, 59). Several neu-rophysiological experiments suggest that tau-rine plays an excitation-reducing neuromod-ulatory role in the insect nervous system (11,73). Furthermore, taurine also regulates manybiological phenomena including brain osmo-protection (57). The authors thus speculated,although they found no definitive proof, thathairworms cause thirst in their host during theday to convince it to move to the water atnight.

Tyrosine is a precursor of DA, but as no ob-vious changes in DA content were observed inthe different experimental groups, its role in theprocess of host manipulation, as well as that ofvaline, appears more difficult to explain. Fur-ther studies are still needed to determine theexact function of these three amino acids in

the manipulation process and their potential toalter the behavior of infected hosts.

MOLECULAR MIMICRYOF HOST PROTEINS

Biron et al. (4, 5) found that adult hairwormsproduce host mimetic proteins that have knownfunctions in the development of the CNS.These mimetic proteins could be injected intothe host CNS via the hemolymph and passthrough the ganglionic sheath, or they could beinjected directly into the brain. Alternatively,the hairworm might absorb host proteins. Sofar there is no evidence that clarifies which ofthese hypotheses reflects the true mechanism.However, the authors found six protein fami-lies, all of which are directly or indirectly in-volved in CNS development, that are specif-ically expressed in the CNS of manipulatedhosts. In the katydid Meconema thalassinum,parasitized by Spinochordodes tellinii, two of thedetected protein families are linked to neu-rotransmitter release and to the regulation ofapoptosis. However, a large number of theseproteins have yet to be further characterized.The Wnt proteins compose one family of pro-teins that is well known and was overexpressedduring the nocturnal manipulation phase. Wntproteins form a family of highly conserved sig-naling molecules that regulate cell-to-cell in-teractions during embryogenesis (27, 28). Thefunctions of Wnt proteins have been character-ized in vertebrates as well as in invertebrates. Inmice, for example, many Wnt genes have beenspecifically mutated, leading to defined and spe-cific developmental defects (46, 69).

In the heads of Nemobius sylvestris (par-asitized by Paragordius tricuspidatus; 6) andM. thalassinum (parasitized by S. tellinii; 5),differential Wnt protein expression could belinked to the contribution of the mimetic Wntprotein synthesized by the hairworm. Themimetic Wnt proteins suggest an action of thehairworm on the host CNS that can lead toan alteration of the host behavior either di-rectly or indirectly via a host genome response.In insects Wnt proteins are involved mainly in


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


brain development. The same is true for BIR;2,Clathrin Ig ch, actins, and ATPase, which alsowere detected at high levels in the host CNSduring the expression of water-seeking behav-ior (6). The BIR;2 family is overexpressed inthe head of parasitized crickets, with the highestvalues again seen during water-seeking behav-ior. Given the role of BIR;2 in cellular apop-tosis inhibition, this result suggests an inhibi-tion of apoptosis and an increased number ofcells in infected N. sylvestris brains. Abnormalneuronal production most likely interferes withnormal neural circuitry. Therefore, the analy-sis of environmental cues by the cricket mightbe perturbed, leading to aberrant behavioralresponses (33, 67).

The proteins from the Clathrin Ig ch familyare the major coat-forming proteins and are in-volved in membrane trafficking within eukary-otic cells. Detection of proteins from this familysuggests an increased neurotransmitter activityand also a higher absorption of macromoleculesby endocytosis during the expression of water-seeking behavior by the host. The overexpres-sion of the actin family in the head of infectedcrickets, especially during manipulation, mightbe linked to an increased activity of synapticvesicle coating and also to the overproductionof brain cells. Furthermore, CRAL TRIO andPCI;1, which are connected to the visual sys-tem, are differentially expressed. In the parasiteitself, PCI;1 appears to be involved in the alter-ation of host behavior. This finding indicatesan induced change in the visual system of themanipulated host.

Proteomics in fact appears to be well suitedfor the closer investigation of the mechanismsunderlying this particular form of parasitismthat leads to such a significant alteration of hostbehavior. However, all the present results anddata are rather speculative. It will be necessaryto further confirm that these protein familiesare in fact the manipulating agents, for exam-ple, by isolating and injecting them into the hostCNS. Furthermore, it will be necessary to iden-tify the mechanisms by which the hairwormssecrete the mimetic proteins into the CNS ofthe host.

HOST BEHAVIORMANIPULATION BYA PARASITOID WASP

Many ectoparasitoid wasps use insects as foodsources for their larvae. To do so, the waspmust manipulate the behavior of its host to en-able oviposition and to make the host a suit-able substrate from which the larva can feed.Such behavioral manipulation is achieved, insome cases, by neurotoxins that directly affectthe central or peripheral nervous system. In thissection we focus on what is, to date, the mostextensively studied example of behavioral ma-nipulation of an insect host by a parasitoid wasp,namely, A. compressa and its host, the cockroachP. americana. Because the wasp affects somewell-characterized behavioral and neurophysi-ological mechanisms in its insect prey, this casestudy provides a unique window into the mech-anisms of behavioral manipulation of one insectby another, as a product of millions of years ofcoevolution. Moreover, because this manipula-tion is designed to affect specific subsets of hostbehavior, understanding its nature provides apowerful tool for the study of the neural con-trol of insect behavior in general.

A. compressa is a tropical ampulicine waspthat hunts cockroaches, typically P. americana.The wasp stings the cockroach twice: first intothe prothorax and then into the neck. Thethoracic sting induces a transient paralysis ofthe forelegs, which enables the second stingwith which the wasp penetrates the head cap-sule and injects venom into the cerebral gan-glia. This head-sting has two behavioral conse-quences in the cockroach host: first, after theleg paralysis wears off, the cockroach enters anexcessive (30 min) self-grooming phase. Then,as the grooming phase ends, the cockroachenters a long-term hypokinetic state. In thelatter state the cockroach fails to initiate spon-taneous locomotion and does not respond ap-propriately to external stimuli. However, thestung cockroach is not paralyzed, as all mo-tor systems appear to be functioning properly.In fact, the stung cockroach can be figurativelydescribed as a submissive zombie that does not


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


resist as the wasp cuts its antennae, feeds on itshemolymph, and then grabs an antennal stumpand walks backward into a burrow, with thezombified cockroach following in a docile man-ner. While being led by the wasp, the cock-roach shows normal walking coordination. Thewasp then lays an egg on the cockroach’s legand seals the burrow using debris and pebbles.The stung cockroach does not try to fight orescape its tomb. The larva emerging from theegg feeds on the hemolymph of the zombifiedcockroach, then enters its body, devours theinternal organs, and eventually pupates insidethe abdomen. Ampulex venom thus exerts threeconsecutive effects on host behavior: transientparalysis of the forelegs, excessive grooming,and long-term hypokinesia. Whereas paralysisis a hunting strategy common to many para-sitoid wasps, the long-term nonparalytic hy-pokinesia is a rather unusual neurotoxic effectand the venom-induced grooming is, to the bestof our knowledge, a phenomenon unique to theAmpulex/Periplaneta system.

HOST PARALYSIS

Paralyzing the host is a widespread strategyamong parasitoid wasps. Some wasps, such asthe beewolf Philanthus triangulum, supply theirlarvae with paralyzed hosts as food supply (47,49, 50). Other wasps inflict a transient paralysisthat serves merely as a first stage to an eventuallymore complex behavioral manipulation. Whilewasps of the former type typically incapacitatethe prey with neurotoxins that target the centraland/or peripheral nervous system, wasps of thelatter type characteristically target mostly theCNS and are believed to inject venom directlyinto the host’s nerve cord. The most extensivelystudied examples of wasps using transient paral-ysis are A. compressa and the cricket-huntingLiris niger, both of which ultimately supply theirlarvae with hypokinetic nonparalyzed hosts. Toultimately induce hypokinesia, the wasps needto apply a precisely targeted head-sting. There-fore, the transient paralysis serves to incapaci-tate the prey’s legs, which might otherwise beused as powerful defensive weapons.

L. niger applies four consecutive stings to itscricket prey, each directed at a different bodysegment. The wasp first disarms the strongmetathoracic (kicking) legs by stinging into themetathoracic segment, presumably into themetathoracic ganglion. Then the other pairs oflegs are paralyzed by stings into the respectivethoracic segments. Paralysis that sets in almostimmediately and lasts 4–30 min renders thecricket helpless and incapable of maintainingposture or fighting the wasp. At this stage, in-serting its stinger into the cricket neck towardthe SEG, the wasp applies the last sting thatrenders the cricket hypokinetic for a few days,until it is devoured by the wasp’s larva (61, 62).Neurophysiological studies revealed that thetoxins in the L. niger venom completely abolishspontaneous and evoked activity in the affectedneurons by blocking voltage-dependent inwardcurrents (probably sodium currents) and byincreasing leak currents. Moreover, there issome evidence that the venom blocks synaptictransmission.

A similar short-term paralysis is induced incockroaches stung by A. compressa, althoughthe underlying mechanisms appear differentfrom those of L. niger. A. compressa stings twice,first into the prothoracic ganglion and then,for a longer time and more precisely, into thecerebral ganglia. The first sting paralyzes theprothoracic legs for 1–2 min, during whichthe wasp applies the second sting. Similarto the Liris venom, the Ampulex venom is acomplex cocktail of proteins, peptides, andsubpeptidic components. It appears that onlycomponents of low molecular weight (<2 kDa)are responsible for the transient leg paralysis.The toxins found in fractions of low molecularweight abolish neuronal activity by blockingacetylcholine- and gamma-aminobutyric acid(GABA)-mediated synaptic transmission,rendering the stung host completely unableto resist as the wasp’s stinger penetrates thecerebral ganglia (25, 41).

EXCESSIVE GROOMING

Almost immediately after the second sting,A. compressa leaves the cockroach to search for


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


a suitable burrow. By this time the paralyzingeffect of the venom has worn off and the cock-roach starts to groom itself excessively. Thegrooming phase lasts approximately 20–30 minnonstop (70). At the end of this period the waspreturns to the grooming cockroach, cuts the an-tennae to feed on the hemolymph, and thendrags the willing victim to the chosen burrow.

Apart from its exceptionally long duration,venom-induced grooming is in every respectsimilar to normal grooming and involves the co-ordinated movement of different appendages.Grooming behavior is evoked only if venom isinjected into the head; it cannot be accountedfor by the stress of the attack, the contact withthe wasp, mechanical irritation, or venom in-jection into a location other than the cerebralganglia (16). Thus, the venom appears to en-gage a central neuronal circuit in the cerebralganglia responsible for grooming, somewhatsimilar in concept to the aforementioned ma-nipulation of spider-weaving behavior by Hy-menoepimecis. In insects, modulation of neuronalcircuits that elicit well-defined behaviors hasbeen associated with specific neuromodulators,in particular monoamines. Therefore it seemslikely that the venom manipulates monoamin-ergic systems inside the sub- and/or suprae-sophageal ganglion to elicit (or prevent the ter-mination of ) grooming behavior.

Experimental manipulation of monoamin-ergic systems, in particular the dopaminergicsystem, can induce excessive grooming inunstung cockroaches. Injection of DA or DA-receptor agonists induced excessive groomingsimilar to venom-induced grooming (70).Moreover, injection of a DA-receptor antago-nist prior to a sting markedly reduced venom-induced grooming (70). Immunohistochemicalstudies revealed that the cerebral ganglia of thecockroach house a rather large population ofdopaminergic neurons, some of which have ex-tensive terminal branches within the ganglion(36). Thus, it is likely that manipulation ofdopaminergic pathways in the cockroach cere-bral ganglia is responsible for venom-inducedgrooming. Moreover, gas chromatogra-phy/mass spectrometry identified a DA-like

substance in the venom that was later con-firmed by HPLC (70). This substance might beresponsible for direct stimulation of grooming-releasing circuits within the cerebral ganglia viaDA receptors. In support of this finding, a stungand hypokinetic cockroach does not engage inthe stereotypic grooming behavior if stung asecond time (71) and, similarly, injection of DAinto stung cockroaches fails to evoke groom-ing. These results further demonstrate thatdopaminergic pathways, and probably DA re-ceptors, are involved in venom-induced groom-ing. Nevertheless, it cannot be excluded thatthe venom also contains other substances thatmodulate levels of neuromodulators in the headganglia indirectly and thus elicit grooming.

So far we can only speculate about the adap-tive significance of the grooming phase of en-venomation. Possibly, the atypically excessivegrooming is merely a side effect of the venom.If the DA-like substance in the venom were in-volved in inducing the long-term hypokineticstate, for example, grooming might have noadaptive value to the wasp. However, it is alsopossible that excessive grooming serves to cleanoff ectoparasites on the host’s exoskeleton suchas bacteria or fungi that might be harmful tothe developing wasp larva. Alternatively, exces-sive grooming might ensure that the cockroachstays in place while the wasp searches for a suit-able burrow. While grooming, unstung cock-roaches are little responsive to external stim-uli and show no spontaneous locomotion (7).Because the long-lasting hypokinetic phase be-gins to develop concomitantly with the termi-nation of the grooming phase, the groomingphase might be a means for keeping the cock-roach in place until the long-lasting hypokineticstate fully develops.

NONPARALYTIC HYPOKINESIA

The third phase of cockroach envenomationby A. compressa is probably the most interest-ing in terms of host behavioral manipulationand in understanding the neural mechanismsthat underlie host behavior. After the groom-ing phase is over, the cockroach shows no signs


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


GI: giant interneuron

of paralysis, although it behaves like a submis-sive automaton that does not initiate sponta-neous or evoked locomotion. This is of ob-vious adaptive value to the wasp because itenables resistance-free host feeding, trans-portation to the burrow, and oviposition (32). Ifthe egg is removed experimentally, the venom-induced hypokinesia persists for several days,after which the cockroach resumes normal ac-tivity. In nature, however, the cockroach meetsits inevitable fate as the larva emerges from itsegg, perforates the cockroach cuticle, and feedson its hemolymph (20). The venom reducesthe metabolic rate of the cockroach (24) andthus, although it does not feed or drink whileit is sealed within its tomb, ensures a fresh andnutritional meal for the larva throughout de-velopment. After approximately four days thelarva penetrates the cockroach and consumesits internal organs for another 1–2 days. It isonly at this stage that the cockroach actuallydies. The larva then pupates inside the cock-roach abdomen and emerges from the cocoonapproximately four weeks later.

The hypokinetic state is characterized by lit-tle spontaneous or provoked activity, an im-portant hallmark of which is the inability ofthe stung host to produce a normal escape re-sponse. In cockroaches stung by A. compressa,and similarly in crickets stung by L. niger, long-term hypokinesia is induced only if the host isstung in the brain. Hence, the observed reduc-tion in host locomotion cannot be accountedfor by a direct effect of the venom on locomo-tor centers that reside in the thoracic ganglia.How does a venom injection into the cerebralganglia affect locomotor centers in the thorax?This issue has been studied extensively in theAmpulex/cockroach system.

Stung hypokinetic cockroaches show nodeficits in spontaneous or provoked grooming,righting behavior, or the ability to fly in a windtunnel (16, 17). Hence, rather than affectingbehavior in general, for example, by decreas-ing the level of overall arousal, the head-stingaffects specific subsets of motor behavior.Moreover, stung cockroaches seem to have anincreased threshold for walking rather than be-

ing unable to initiate or maintain this behav-ior. Interestingly, swimming behavior (whichin cockroaches parallels walking with respectto the motor pattern) can be induced in stungcockroaches by immersing individuals in wa-ter. Although the motor pattern during activeswimming is identical in control and in stungcockroaches, in stung cockroaches the dura-tion of swimming is dramatically decreased, asif they despair faster (19). Accumulating evi-dence suggests that the venom modulates theprobability that a particular stimulus evokeswalking-related behavior. In other words, thevenom appears to modulate circuits in the cock-roach cerebral ganglia that are involved specif-ically in determining the motivation to initi-ate walking-related behaviors. The wasp injectsits venom directly into the SEG and into thecentral complex and mushroom bodies withinthe brain (26), all considered higher neuronalcenters modulating the initiation of locomotion(51, 56). Recent studies in cockroaches demon-strated that the two cerebral ganglia also senda descending tonic signal to the thoracic motorcenters, providing further evidence of their rolein the motivational state of the insect (18).

In stung cockroaches, wind stimuli appliedto the cerci, tactile stimuli to the antennae, ortactile stimuli to the anal plates, each recruit-ing different premotor pathways that usuallyproduce strong escape responses, are no longereffective (16, 17, 19, 35). Under uncompro-mised circumstances, wind-sensitive hairs onthe abdominal cerci detect minute air move-ments, as produced for instance by a preda-tor’s strike, and excite giant interneurons (GIs)in the terminal abdominal ganglion to medi-ate escape running (Figure 2). A caudal tac-tile stimulus recruits a different population ofGIs that also mediates escape running. In bothcases, the GIs activate various interneurons inthe thoracic locomotor centers that in turn ex-cite various local interneurons or motoneuronsassociated with escape running. In addition,escape running can be triggered by tactile stim-uli applied to the antennae, which recruits spe-cific interneurons descending from the headto the thorax. Thus, touch- or wind-sensitive


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


input from rostral and/or caudal stimuli is car-ried by three distinct populations of interneu-rons (Figure 2 shows two of them). These even-tually converge on the same thoracic circuitrythat evokes running leg movements in nor-mal, but not in stung, cockroaches (Figure 2).Experiments on stung cockroaches revealed

−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→Figure 2Current model of the neurophysiological eventsleading to venom-induced hypokinesia incockroaches stung by Ampulex compressa. Schematicand simplified drawing of a cockroach nervoussystem depicting circuitries that affect walking-related behaviors. The walking pattern generatorthat orchestrates leg movements is located in thethorax. It consists of motor neurons innervating legmuscles (A), ascending neurons from sensorystructures on the legs (not shown) and type-Athoracic interneurons (TIAs; B), which synapse ontothe motor neurons directly and indirectly via localinterneurons (C). The TIAs receive inputs fromseveral interneurons. For example, sensory neurons(D) in the antennae or cerci recruit descending(E) or ascending (F ) giant interneurons, whichconverge directly onto the TIAs to ultimately evokeescape responses. In addition, neurons of the patterngenerator receive input from thoracicneuromodulatory cells (G). One example of these isthe dorsal unpaired median (DUM) neurons, whichsecrete octopamine and modulate the efficacy ofpremotor-to-motor (B-to-A) synapses. Theneuromodulatory cells, in turn, receive tonic inputthrough interneurons descending from the brain(H) and subesophageal ganglion (SEG) (not shown).This tonic input affects the probability of theoccurrence of specific motor behaviors bymodulating the different thoracic patterngenerators. The wasp A. compressa injects its venomcocktail directly into both cerebral ganglia tomodulate some specific yet unidentified cerebralcircuitries. The current hypothesis states that in theSEG the venom suppresses the activity of brain-projecting DUM neurons (I), which control theactivity of brain descending interneurons (H) thatmodulate, either directly (not shown) or indirectlyvia the neuromodulatory cells (G), the walkingpattern generator. Hence, the venom injected intothe cerebral ganglia decreases the overall excitatoryinput to the thoracic walking pattern generator. As aresult, walking-related behaviors are specificallyinhibited and stimuli to the antennae or cerci fail toevoke normal escape responses.

that the head-sting affects neither the responseof the ascending GIs nor that of the descend-ing interneurons (35). Moreover, thoracic in-terneurons receive comparable synaptic drivefrom the GIs in control and stung animals (35).Thus, the ultimate effect of venom injectedinto the cerebral ganglia must take place at theconnection between some thoracic interneu-rons and specific motoneurons that control legmovements.

In unstung cockroaches, escape runningrequires the recruitment of both fast andslow motoneurons in the thorax. Under nat-ural conditions, when a stung cockroach isstanding on a solid surface, tactile or windstimuli do not recruit fast motoneurons (17,35). However, the same motoneurons can be

Subesophagealganglion

Thoracic ganglia

Cerci

Last abdominalganglion

Venom

Antennae

Brain

Circumesophagealconnectives

Neck connectives

Leg muscles

D

D

EH

I

GA

B

C

F


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


OA: octopamine

DUM: dorsalunpaired median

recruited experimentally during other behav-iors. When cockroaches are placed on theirback, for instance, these fast motoneurons arefully active and enable the rapid and strongleg movements required for righting. The samemotoneurons are also recruited when submerg-ing a stung cockroach into water to induceswimming behavior, which also requires strongand fast leg movements. Owing to their bifunc-tional nature, these motoneurons are also re-cruited during flying when a stung cockroachis placed inside a wind tunnel (19, 34). Theseobservations suggest that the descending con-trol from the cerebral ganglia on the thoracicwalking circuitry is exerted on thoracic pre-motor circuits. Thus, it seems that the specificeffect of the venom on walking-related behav-iors requires inhibition of thoracic premotor-to-motor elements by descending input in-volved in modulating walking-related behaviors(Figure 2). In support of this, it was shownthat in stung cockroaches the discharge rate ofslow-muscle potentials during active swimmingbouts are also decreased compared with thatof control cockroaches. The descending inputfrom the cerebral ganglia thus seems to bear in-formation regarding the motivation to initiateor maintain walking-related behaviors.

However, how could the venom act so se-lectively, manipulating only a particular sub-set of behaviors? One possible explanation isthat the venom targets a certain neuromodu-latory system that specifically controls certainbehaviors. This would imply that the venomchemically manipulates the output of specificpathways descending from the cerebral to thethoracic ganglia. Certain neuromodulatory sys-tems located in the thoracic ganglia are involvedin the initiation and/or execution of walking.The monoaminergic system is a likely candi-date at both sites of modulation, as alterationsin this system in both the thoracic and cerebralganglia affect specific subsets of behavior (36).In the following we describe how monoaminesmight mediate venom-induced motor deficitsfirst at the level of thoracic premotor cen-ters and then at the level of cerebral centers(Figure 2).

A recent study demonstrated that in stungcockroaches the activity of identified oc-topamine (OA) neurons in the cockroachthorax—the dorsal unpaired median (DUM)neurons, which modulate the excitability of spe-cific thoracic premotor neurons—is compro-mised (54). Thoracic DUM neurons in stungcockroaches differ from those in control cock-roaches in the following parameters: (a) a de-crease in resting membrane potential, (b) amarked decrease in spontaneous firing rate,(c) a larger amplitude of action potentials,(d ) a higher time constant, (e) a dramatic de-crease in responses to cercal- or antennal-evoked stimuli, and ( f ) decreased firing rateand increased latency in response to hyperpo-larizing pulses. However, there is no differencein the rate or amplitude of postsynaptic poten-tials and in the width of evoked action poten-tials between DUM neurons of stung versuscontrol cockroaches. The observed differencesindicate that it is probably calcium currentsthat are modulated in DUM neurons of stungcockroaches (54). A change in the neuromod-ulatory environment of DUM neurons, for ex-ample due to the removal of descending neuro-modulatory input from the head ganglia, couldaccount for this change. This effect could bedirect (e.g., by removal of input from descend-ing head neurons which directly synapse ontoDUM neurons) or indirect (e.g., by removal ofinput from descending head neurons that mod-ulate other thoracic neurons that in turn mod-ulate the DUM neurons).

Comparison of the activity of DUM neu-rons between stung and unstung cockroachesfrom which the brain has been surgically re-moved suggests that the effect of the venomon thoracic DUM neurons is indirect. Post-synaptic activity in DUM neurons of stungcockroaches was comparable to that of con-trol cockroaches, whereas the rate and ampli-tude of postsynaptic potentials were markedlydecreased as a result of brain removal. Thus,it appears that A. compressa alters descend-ing pathways in the cerebral ganglia thatindirectly affect, at the least, OA secretionfrom thoracic DUM neurons (Figure 2). The


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


thoracic DUM neurons dramatically affect lo-comotion, which can explain the long-lastinghypokinetic state induced in stung cockroacheson the level of the thoracic motor or premotorcircuits.

Which mechanisms at the level of the cere-bral ganglia could account for the observedchange in the cockroach motivation to initi-ate walking? OA seems to play a role here, too.A recent study showed that, in unstung cock-roaches, injection of an OA-receptor antago-nist into the brain significantly reduced walk-ing activity (53). Injection of an OA-receptoragonist rescued these cockroaches from theircatatonic state (53). Both effects point to theimportance of brain OA in the modulation ofthe motivation to initiate walking. Moreover,hypokinetic stung cockroaches injected with anOA-receptor agonist into the SEG showed in-creased walking durations compared with stungcockroaches injected with saline.

Recently, OA-immunoreactive neurons inthe SEG of Periplaneta were identified and theirprojection patterns described (60). The SEGcontains 16 OA-immunoreactive midline neu-rons, arranged in three dorsal midline clus-ters, and two bilateral clusters of five OA-immunoreactive somata located between theroots of the tritocerebral connectives. At leastthree of these SEG-DUM neurons providedense innervation in the protocerebral bridgeand ellipsoid body of the central complex,regions implicated in controlling locomotion(63, 64).

In stung cockroaches, as well as in cock-roaches lacking the SEG, the activity of tho-racic octopaminergic neurons is significantlychanged—which could be part of the mech-anism by which the wasp induces the changein the behavioral state of its prey (54). Alter-natively, venom injected into the SEG mightalter the activity of SEG-DUM neurons thatproject to the brain, thorax, or both, and thusalter the descending control from the cere-bral ganglia to the octopaminergic neurons inthe thorax. Taken together, it appears that thewasp manipulates, at the least, octopaminergic

circuits in the cockroach cerebral ganglia thatin turn manipulate octopaminergic circuits inthe thoracic ganglia to decrease walking-relatedbehaviors.

FUTURE PROSPECTS

In this review, we describe the wonderful worldof parasites and their insect hosts and, specif-ically, how certain parasites take control overthe brain of their host. Much work remains tobe done before the exact mechanisms of hostmanipulation are known. From the examplespresented in this review, it is clear that a mul-tidisciplinary approach combining moleculartechniques such as proteomics with cellularelectrophysiology and sophisticated behavioranalysis is necessary, if not essential, to reacha true understanding of host manipulation. Itis unfortunate that the scientific community,more often than not, perceives these extremeforms of behavioral manipulation by parasitesmerely as curiosities of nature rather than mod-els for investigating fundamental questions inbiology. Currently, most of these systems havebeen investigated by a single research groupwith slow progress in deciphering the cellularand molecular mechanisms underlying the re-spective manipulation. And yet (and rightly so)Edwards (14) notes that “parasites have evolved,through years of coevolution, a better ‘under-standing’ of the subtleties and regulation of theneuroendocrine systems of their insect hoststhan is at present understood by insect phys-iologists”. As we have seen here, some of theparasites described in this review know moreabout the brain than all neuroscientists com-bined. We can only hope that such host-parasiteinteractions will stimulate the interest and mo-tivation of young minds to investigate the neu-ronal basis of parasite-induced alterations ofhost behavior, with the goal of increasing ourunderstanding of the neurobiology of the initi-ation of goal-oriented behaviors and the neuralmechanisms underlying changes in responsive-ness, which are prime questions in the study ofarousal and motivation.


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


SUMMARY POINTS

1. Adult nematomorphs need an aquatic environment for successful reproduction. Infectedhosts are thus manipulated in their behavior to actively seek water and to jump in—whichleads to the host’s death.

2. Parasites interfere with the CNS of their hosts. In particular, certain free amino acids andcertain protein families involved in the brain development of the host undergo significantchanges during the manipulation process.

3. Parasitoproteomics revealed that parasite proteins are expressed in the brain of the host.This molecular mimicry includes Wnt proteins that are also primarily involved in braindevelopment.

4. The parasitoid wasp A. compressa hunts cockroaches as hosts to provide its offspring with alive yet immobile food supply. The wasp injects a cocktail of neurotoxins directly into thehost CNS to evoke three consecutive behaviors: transient paralysis of the legs, excessivegrooming behavior, and long-lasting hypokinesia.

5. The excessive grooming phase is evoked by a manipulation of the cockroach’s dopamin-ergic system inside the cerebral ganglia. This is probably due to a DA-like substance inthe wasp venom.

6. The hypokinetic phase is evoked by a chemical manipulation of neuronal circuits withinthe cerebral ganglia. These circuits affect neurons descending from the cockroach’s headto its thorax. At least one consequence of the chemical manipulation is the inhibition ofspecific OA-releasing neurons in the thorax. These neurons, in turn, affect a network as-sociated with the thoracic pattern generator responsible for walking. By this mechanism,the wasp manipulates specifically the occurrence of walking-related behaviors withoutaffecting nonrelated behaviors.

DISCLOSURE STATEMENT

The authors are not aware of any biases that might be perceived as affecting the objectivity of thisreview.

LITERATURE CITED

1. Adamo SA, Shoemaker KL. 2000. Effects of parasitism on the octopamine content of the central nervoussystem of Manduca sexta: a possible mechanism underlying host behavioural change. Can. J. Zool. 78:1580–87

2. Beckage NE, Gelman DB. 2004. Wasp parasitoid disruption of host development: implications for newbiologically based strategies for insect control. Annu. Rev. Entomol. 49:299–330

3. Bicker G. 1992. Taurine in the insect central nervous system. J. Comp. Biochem. Physiol. C 103:423–284. Biron DG, Joly C, Galeotti N, Ponton F, Marche L. 2005. The proteomics: a new prospect for studying

parasitic manipulation. Behav. Proc. 68:249–535. The findings suggestthat the adult wormalters the normalfunctions of the host’sCNS by producingcertain effectivemolecules.

5. Biron DG, Marche L, Ponton F, Loxdale HD, Galeotti N, et al. 2005. Behavioural manipulationin a grasshopper harbouring hairworm: a proteomics approach. Proc. R. Soc. London Sci. Ser. B

272:2117–266. Biron DG, Ponton F, Marche L, Galeotti N, Renault L, et al. 2006. ‘Suicide’ of crickets harbouring

hairworms: a proteomics investigation. Inst. Mol. Biol. 15:731–42


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


7. Camhi JM, Nolen TG. 1981. Properties of the escape system of cockroaches during walking. J. Comp.Physiol. A 142(3):339–46

8. Castner JL. 1988. Biology of the mole cricket parasitoid Larra bicolor (Hymenoptera: Sphecidae). InAdvances in Parasitic Hymenoptera Research, ed. VK Gupta, pp. 131–39. Leiden: Brill

9. Dawkins R. 1982. The Extended Phenotype. Oxford: Oxford Univ. Press10. De Jong-Brink M. 1995. How schistosomes profit from the stress responses they elicit in their hosts.

Adv. Parasitol. 35:177–25611. Dubas F. 1991. Action of putative amino acid neurotransmitters on the neuropile arborizations of locust

flight motoneurons. J. Exp. Biol. 6:337–5612. Eberhard WG. 2000. Spider manipulation by a wasp larva. Nature 406(6793):255–5613. Eberhard WG. 2001. Under the influence: webs and building behavior of Plesiometa argyra (Aranea,

tetragnathidae) when parasitized by Hymenoepimecis argyraphaga (Hymenoptera, Ichneumonidae).J. Arachnol. 29:354–66

14. Edwards JP, Weaver RJ, eds. 2001. Endocrine Interactions of Insect Parasites and Pathogens. Oxford: BIOSScientific

15. Ferber M, Consoulas C, Gnatzy W. 1999. Digger wasp versus cricket: immediate actions of the predator’sparalytic venom on the CNS of the prey. J. Neurobiol. 38(3):323–37

16. Fouad K, Libersat F, Rathmayer W. 1994. The venom of the cockroach-hunting wasp Ampulex compressachanges motor thresholds: a novel tool for studying the neural control of arousal? Zoology 98:23–34

17. Fouad K, Libersat F, Rathmayer W. 1996. Neuromodulation of the escape behavior of the cockroachPeriplaneta americana by the venom of the parasitic wasp Ampulex compressa. J. Comp. Physiol. A 178:91–100

18. Gal R, Libersat F. 2006. New vistas on the initiation and maintenance of insect motor behaviors revealedby specific lesions of the head ganglia. J. Comp. Physiol. A 192(9):1003–20

19. Suggests thatA. compressa modulatesthe motivation of itscockroach host toinitiate, specifically,walking-relatedbehaviors.

19. Gal R, Libersat F. 2008. A parasitoid wasp manipulates the drive for walking of its cockroachprey. Curr. Biol. 18(12):877–82

20. Gal R, Rosenberg LA, Libersat F. 2005. Parasitoid wasp uses a venom cocktail injected into the brain tomanipulate the behavior and metabolism of its cockroach prey. Arch. Insect. Biochem. Physiol. 60(4):198–208

21. Gnatzy W. 2001. Digger wasp vs cricket: (neuro-) biology of a predator-prey-interaction. Zoology103:125–39

22. Hanelt B, Janovy J. 1999. The life cycle of a horsehair worm, Gordius robustus (Nematomorpha:Gordioidea). J. Parasitol. 85:139–41

23. Hanelt B, Thomas F, Schmidt-Rhaesa A. 2005. Biology of the phylum Nematomorpha. Adv. Parasitol.59:243–305

24. Haspel G, Gefen E, Ar A, Glusman JG, Libersat F. 2005. Parasitoid wasp affects metabolism of cockroachhost to favor food preservation for its offspring. J. Comp. Physiol. A 191(6):529–34

25. Haspel G, Libersat F. 2003. Wasp venom blocks central cholinergic synapses to induce transient paralysisin cockroach prey. J. Neurobiol. 54:628–37

26. Demonstrates thatthe wasp stings directlyinto the target gangliain the head of its prey;first direct evidencedocumenting targeteddelivery of venom intothe CNS of a preyorganism.

26. Haspel G, Rosenberg LA, Libersat F. 2003. Direct injection of venom by a predatory wasp intocockroach brain. J. Neurobiol. 56:287–92

27. Hayden MA, Akong K, Peifer M. 2007. Novel roles for APC family members and Wingless/Wnt signalingduring Drosophila brain development. Dev. Biol. 305:358–76

28. Hayward P, Kalmar T, Arias AM. 2008. Wnt/Notch signalling and information processing duringdevelopment. Development 135:411–24

29. Helluy S, Holmes JC. 1990. Serotonin, octopamine, and the clinging behavior by the parasite Polymorphusparadoxus (Acanthocephala) in Gammarus lacustris (Crustacea). Can. J. Zool. 68:1214–20

30. Helluy S, Thomas F. 2003. Effects of Microphallus papillorobustus (Platyhelminthes: Trematoda) on sero-tonergic immunoreactivity and neuronal architecture in the brain of Gammarus insensibilis (Crustacea:Amphipoda). Proc. R. Soc. London Sci. Ser. 270:563–68

31. Hohorst W, Graefe G. 1961. Ameisen—obligatorische Zwischenwirte des Lanzettegels (Dicrocoeliumdendriticum). Naturwissenschaften 48:229–30

32. Keasar T, Sheffer N, Glusman G, Libersat F. 2006. Host handling: an innate component of foragingbehavior in the parasitoid wasp Ampulex compressa. Ethology 112(7):699–706


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


33. Klein SL. 2003. Parasite manipulation of the proximate mechanisms that mediate social behaviour invertebrates. Physiol. Behav. 79:441–49

34. Libersat F. 2003. Wasp uses venom cocktail to manipulate the behavior of its cockroach prey. J. Comp.Physiol. A 189:497–508

35. Libersat F, Haspel G, Casagrand J, Fouad K. 1999. Localization of the site of effect of a wasp’s venomin the cockroach escape circuitry. J. Comp. Physiol. A 184:333–45

36. Libersat F, Pflueger HJ. 2004. Monoamines and the orchestration of behavior. BioScience 54:17–2537. Lucius R, Romig T, Frank W. 1980. Camponotus compressiscapus Andre (Hymenoptera, Formicidae) an ex-

perimental second intermediate host of Dicrocoelium hospes Looss, 1907 (Trematodes, Dicrocoeliidae).Z. Parasitenkd. 63(3):271–75

38. Maeyama T, Terayama M, Matsumoto T. 1994. The abnormal behavior of Colobopsis sp. (Hymenoptera,Formicidae) parasitized by Mermis (Nematoda) in Papua New Guinea. Sociobiology 24(2):115–19

39. Mains EB. 1948. Entomogenous fungi. Mycologia 40:402–1640. Mains EB. 1949. Cordyceps bicephala Berk. and C. australis (Speg.) Sacc. Bull. Torrey Bot. Club 76(1):24–3041. Moore EL, Haspel G, Libersat F, Adams ME. 2006. Parasitoid wasp sting: A cocktail of GABA, taurine

and β-alanine opens chloride channels for transient synaptic block and paralysis of a cockroach host.J. Neurobiol. 66(8):811–20

42. Moore J. 1995. The behavior of parasitized animals. Bioscience 45(2):89–96

43. Compiles diversityof host-parasiteinteractions andorganizes them intodistinct categories toprovide a framework forinvestigating theultimate and proximatecausations of behavioralmodifications.

43. Moore J, ed. 2002. Parasites and the Behavior of Animals. Oxford: Oxford Univ. Press44. O’Neill KM, ed. 2001. Solitary Wasps: Behavior and Natural History. Ithaca, NY: Comstock45. Overli O, Pall M, Borg B, Jobling M, Winberg S. 2001. Effects of Schistocephalus solidus infection on brain

monoaminergic activity in female three-spined sticklebacks Gasterosteus aculeatus. Proc. R. Soc. London Sci.Ser. B 268:1411–15

46. Parr BA, Cornish VA, Cybulsky MI, McMahon AP. 2001. Wnt7b regulates placental development inmice. Dev. Biol. 237:324–32

47. Piek T. 1990. Neurotoxins from venoms of the Hymenoptera–twenty-five years of research inAmsterdam. J. Comp. Biochem. Physiol. C. 96(2):223–33

48. Piek T, Mantel P, Engels E. 1971. Neuromuscular block in insects caused by the venom of the diggerwasp Philanthus triangulum F. Comp. Gen. Pharmacol. 2(7):317–31

49. Piek T, Spanjer W. 1986. Chemistry and pharmacology of solitary wasp venoms. In Venoms of theHymenoptera, ed. T Piek, p. 161–307. London: Academic

50. Rathmayer W. 1962. Paralysis caused by the digger wasp Philanthus. Nature 196:1149–5151. Ridgel AL, Ritzmann RE. 2005. Effects of neck and circumoesophageal connective lesions on posture

and locomotion in the cockroach. J. Comp. Physiol. A 191(6):559–7352. Romig T, Lucius R, Frank W. 1980. Cerebral larvae in the second intermediate host of Dicro-

coelium dendriticum (Rudolphi, 1819) and Dicrocoelium hospes Looss, 1907 (Trematodes, Dicrocoeliidae).Z. Parasitenkd 63(3):277–86

53. Rosenberg LA, Glusman JG, Libersat F. 2007. Octopamine partially restores walking in hypokineticcockroaches stung by the parasitoid wasp Ampulex compressa. J. Exp. Biol. 210(24):4411–17

54. Describes the effectof A. compressa’s venomon identifiedOA-releasing neuronsin the thorax of thecockroach host andshows that the headsting has a dramaticeffect on thespontaneous and evokedactivity of OA-releasingneurons.

54. Rosenberg LA, Pfluger HJ, Wegener G, Libersat F. 2006. Wasp venom injected into the prey’sbrain modulates thoracic identified monoaminergic neurons. J. Neurobiol. 66(2):155–68

55. Roy HE, Steinkraus DC, Eilenberg J, Hajek AE, Pell JK. 2006. Bizarre interactions and endgames:entomopathogenic fungi and their arthropod hosts. Annu. Rev. Entomol. 51:331–57

56. Schaefer P, Ritzmann RE. 2001. Descending influences on escape behavior and motor pattern in thecockroach. J. Neurobiol. 49(1):9–28

57. Schaffer S, Takahashi K, Azuma J. 2000. Role of osmoregulation in the actions of taurine. Amino Acids10:527–46

58. Schneider G, Hohorst W. 1971. Wanderung der Metacercariae des Lanzett-Egels in Ameisen.Naturwissenschaften 58:327–28

59. Sinakevitch I, Farris SM, Strausfeld NJ. 2001. Taurine-, aspartate- and glutamate-like immunoreactivityidentifies chemically distinct subdivisions of Kenyon cells in the cockroach mushroom body. J. Comp.Neurol. 439:352–67


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.


60. Sinakevitch I, Niwa M, Strausfeld NJ. 2005. Octopamine-like immunoreactivity in the honey bee andcockroach: comparable organization in the brain and subesophageal ganglion. J. Comp. Neurol. 488:233–54

61. Steiner AL. 1976. Digger wasp predatory behavior (Hymenoptera, Sphecidae) II. Comparative studyof closely related wasps (Larrinae: Liris nigra, Palearctic; L. argentata and L. aequalis, Nearctic) that allparalyze crickets (Orthoptera, Gryllidae). Z. Tierpsychol. 42:343–80

62. Steiner AL. 1986. Stinging behaviour of solitary wasps. In Venoms of the Hymenoptera, ed. T Piek,pp. 63–160. London: Academic

63. Strausfeld NJ. 1999. A brain region in insects that supervises walking. Prog. Brain Res. 123:273–8464. Strauss R. 2002. The central complex and the genetic dissection of locomotor behaviour. Curr. Opin.

Neurobiol. 12(6):633–3865. Thomas F, Adamo S, Moore J. 2005. Parasitic manipulation: Where are we and where should we go?

Behav. Proc. 68(3):185–99

66. First scientificdescription of thebehavioral change inorthopteran insectsinfected by Gordianworm.

66. Thomas F, Schmidt-Rhaesa A, Martin G, Manu C, Durand P, Renaud F. 2002. Do hairworms(Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? J. Evol. Biol.

15:356–6167. Thomas F, Ulitsky P, Augier R, Dusticier N, Samuel D, et al. 2003. Biochemical and histological changes

in the brain of the cricket Nemobius sylvestris infected by the manipulative parasite Paragordius tricuspidatus(Nematomorpha). Int. J. Parasitol. 33:435–43

68. Thomas JA, Knapp JJ, Akino T, Gerty S, Wakamura S, et al. 2002. Parasitoid secretions provoke antwarfare. Nature 417:505–6

69. Traister A, Abashidze S, Gold V, Yairi R, Michael E, et al. 2004. BMP controls nitric oxide-mediatedregulation of cell numbers in the developing neural tube. Cell Death Diff. 11:832–41

70. Describes theinvolvement of thedopaminergic system inthe excessive groomingbehavior induced incockroaches byA. compressa.

70. Weisel-Eichler A, Haspel G, Libersat F. 1999. Venom of a parasitoid wasp induces prolongedgrooming in the cockroach. J. Exp. Biol. 202:957–64

71. Weisel-Eichler A, Libersat F. 2002. Are monoaminergic systems involved in the lethargy induced by aparasitoid wasp in the cockroach prey? J. Comp. Physiol. 188:315–24

72. Williams FX. 1942. Ampulex compressa (Fabr.), a cockroach hunting wasp introduced from New Caledoniainto Hawaii. Proc. Hawaii. Entomol. Soc. 11:221–33

73. Witton PS, Nicholson RA, Strang RH. 1998. Effect of taurine on neurotransmitter release from insectsynaptosomes. J. Neurochem. 51:1356–60

74. Zimmer C, ed. 2001. Parasite Rex: Inside the Bizarre World of Nature’s Most Dangerous Creatures. NewYork: Free Press


Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.

AR363-FM ARI 7 November 2008 10:51

Annual Review ofEntomology

Volume 54, 2009Contents

FrontispieceEdward S. Ross � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � xiv

Lifelong Safari: The Story of a 93-Year-Old Peripatetic Insect HunterEdward S. Ross � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Ecology and Geographical Expansion of Japanese Encephalitis VirusAndrew F. van den Hurk, Scott A. Ritchie, and John S. Mackenzie � � � � � � � � � � � � � � � � � � � � � � �17

Species Interactions Among Larval Mosquitoes: Context DependenceAcross Habitat GradientsSteven A. Juliano � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �37

Role of Glucosinolates in Insect-Plant Relationships and MultitrophicInteractionsRichard J. Hopkins, Nicole M. van Dam, and Joop J.A. van Loon � � � � � � � � � � � � � � � � � � � � � � � �57

Conflict, Convergent Evolution, and the Relative Importance ofImmature and Adult Characters in Endopterygote PhylogeneticsRudolf Meier and Gwynne Shimin Lim � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �85

Gonadal Ecdysteroidogenesis in Arthropoda: Occurrenceand RegulationMark R. Brown, Douglas H. Sieglaff, and Huw H. Rees � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 105

Roles of Thermal Adaptation and Chemical Ecology in LiriomyzaDistribution and ControlLe Kang, Bing Chen, Jia-Ning Wei, and Tong-Xian Liu � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 127

Fitness Costs of Insect Resistance to Bacillus thuringiensisAaron J. Gassmann, Yves Carrière, and Bruce E. Tabashnik � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 147

Insect Herbivore Nutrient RegulationSpencer T. Behmer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 165

Manipulation of Host Behavior by Parasitic Insects and Insect ParasitesFrederic Libersat, Antonia Delago, and Ram Gal � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 189

Bionomics of Bagworms (Lepidoptera: Psychidae)Marc Rhainds, Donald R. Davis, and Peter W. Price � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 209

vii

Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.

AR363-FM ARI 7 November 2008 10:51

Host-Parasitoid Associations in StrepsipteraJeyaraney Kathirithamby � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 227

Biology of the Parasitoid Melittobia (Hymenoptera: Eulophidae)Robert W. Matthews, Jorge M. González, Janice R. Matthews, and Leif D. Deyrup � � � 251

Insect Pests of Tea and Their ManagementLakshmi K. Hazarika, Mantu Bhuyan, and Budhindra N. Hazarika � � � � � � � � � � � � � � � � � � 267

New Insights into Peritrophic Matrix Synthesis, Architecture,and FunctionDwayne Hegedus, Martin Erlandson, Cedric Gillott, and Umut Toprak � � � � � � � � � � � � � � � � 285

Adaptation and Invasiveness of Western Corn Rootworm: IntensifyingResearch on a Worsening PestMichael E. Gray, Thomas W. Sappington, Nicholas J. Miller, Joachim Moeser,and Martin O. Bohn � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 303

Impacts of Plant Symbiotic Fungi on Insect Herbivores: Mutualismin a Multitrophic ContextSue E. Hartley and Alan C. Gange � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 323

A Study in Inspiration: Charles Henry Turner (1867–1923) and theInvestigation of Insect BehaviorCharles I. Abramson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 343

Monogamy and the Battle of the SexesD.J. Hosken, P. Stockley, T. Tregenza, and N. Wedell � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 361

Biology of Subterranean Termites: Insights from Molecular Studiesof Reticulitermes and CoptotermesEdward L. Vargo and Claudia Husseneder � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 379

Genetic, Individual, and Group Facilitation of Disease Resistancein Insect SocietiesNoah Wilson-Rich, Marla Spivak, Nina H. Fefferman, and Philip T. Starks � � � � � � � � � � 405

Floral Isolation, Specialized Pollination, and Pollinator Behaviorin OrchidsFlorian P. Schiestl and Philipp M. Schlüter � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 425

Cellular and Molecular Aspects of Rhabdovirus Interactionswith Insect and Plant HostsEl-Desouky Ammar, Chi-Wei Tsai, Anna E. Whitfield, Margaret G. Redinbaugh,and Saskia A. Hogenhout � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 447

Role of Vector Control in the Global Program to EliminateLymphatic FilariasisMoses J. Bockarie, Erling M. Pedersen, Graham B. White, and Edwin Michael � � � � � � � 469

viii Contents

Ann

u. R

ev. E

ntom

ol. 2

009.

54:1

89-2

07. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by B

en G

urio

n U

nive

rsity

Lib

rary

on

12/1

2/08

. For

per

sona

l use

onl

y.

More About This Article - Instituto de Zoología y ...izt.ciens.ucv.ve/ecologia/Archivos/ECO_POB...

Documents

Transcript of More About This Article - Instituto de Zoología y ...izt.ciens.ucv.ve/ecologia/Archivos/ECO_POB...