evolution of development strategies in parasitic wasps

2 Nov 2005 13:7 AR ANRV263-EN51-11.tex XMLPublishSM(2004/02/24) P1: KUV10.1146/annurev.ento.51.110104.151029

Annu. Rev. Entomol. 2006. 51:233–58doi: 10.1146/annurev.ento.51.110104.151029

Copyright c© 2006 by Annual Reviews. All rights reservedFirst published online as a Review in Advance on July 26, 2005

EVOLUTION OF DEVELOPMENTAL STRATEGIES

IN PARASITIC HYMENOPTERA

Francesco Pennacchio1 and Michael R. Strand2

1Dipartimento di Biologia, Difesa e Biotecnologie Agro-Forestali, Universita dellaBasilicata, 85100 Potenza, Italy; email: [email protected] of Entomology, University of Georgia, Athens, Georgia 30602-2603;email: [email protected]

Key Words parasitoid, wasp, host regulation, venom, polydnavirus

■ Abstract Parasitoid wasps have evolved a wide spectrum of developmental inter-actions with hosts. In this review we synthesize and interpret results from the phyloge-netic, ecological, physiological, and molecular literature to identify factors that haveinfluenced the evolution of parasitoid developmental strategies. We first discuss the ori-gins and radiation of the parasitoid lifestyle in the Hymenoptera. We then summarizehow parasitoid developmental strategies are affected by ecological interactions and as-sess the inventory of physiological and molecular traits parasitoids use to successfullyexploit hosts. Last, we discuss how certain parasitoid virulence genes have evolved andhow these changes potentially affect parasitoid-host interactions. The combination ofphylogenetic data with comparative and functional genomics offers new avenues forunderstanding the evolution of biological diversity in this group of insects.

INTRODUCTION

Parasitoids occur in several orders of insects (Diptera, Coleoptera, Lepidoptera,Trichoptera, Neuroptera, Strepsiptera), but they are especially common in the Hy-menoptera, for which recent estimates suggest that 10% to 20% of all insects maybe parasitoid wasps (58, 117, 160). This high species diversity is almost matchedby an equally wide spectrum of interactions with hosts. Most parasitoids are re-stricted to attacking a particular host life stage (eggs, larvae, pupae, or adults).Parasitoids also divide themselves between idiobionts, whose hosts cease devel-opment after parasitism, and koinobionts, whose hosts continue to develop as theparasitoid’s offspring matures (5). Idiobionts are either ectoparasitoids that para-lyze their hosts or endoparasitoids that attack sessile host stages such as eggs orpupae. Most koinobionts are endoparasitoids of larval stage insects, although afew are ectoparasitic.

Among the foremost challenges in the study of parasitoids is understandingthe origins and basis for this diversity in developmental strategies. Because theinteractions between parasitoids and hosts are primarily controlled by genes,

0066-4170/06/0107-0233$20.00 233

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2 Nov 2005 13:7 AR ANRV263-EN51-11.tex XMLPublishSM(2004/02/24) P1: KUV

234 PENNACCHIO � STRAND

approaching this question requires the integration of recent findings from the phys-iological and molecular literature into the larger framework of evolutionary history.This framework derives from many fields of study including paleontology, sys-tematics, morphology, and ecology. Thus, we begin this review by discussing theorigins of the parasitoid lifestyle and its radiation in the Hymenoptera based uponphylogenetic analyses. Next, we consider important ecological factors that affectparasitoid development and assess the inventory of physiological and moleculartools parasitoids use to successfully exploit hosts. We then examine how someparasitoid gene products have evolved and how these changes could influenceparasitoid-host interactions.

EVOLUTION OF THE PARASITOID LIFESTYLE

The Role of Ancestry

In forming a picture of how such a wide variety of interactions evolved betweenparasitoids and hosts, it is important to consider first the origin and diversificationof the parasitoid lifestyle itself. The first hymenopterans appear in the fossil recordat least 220 million years ago (mya) and the first parasitoids appear around 160 mya(119, 158). The Hymenoptera thereafter underwent substantial radiation in parallelwith diversification of flowering plants and other insect taxa, such that all of the ma-jor lineages present today existed by 65 mya (45, 119, 158). Phylogenetic analysesusing morphological datasets or morphological combined with molecular datasets(45, 158) divide the Hymenoptera into several herbivorous groups within Symphyta(sawflies and woodwasps, e.g., Xyeloidea, Megalodontoidea, Tenthredinoidea,Cephoidea, and Siricoidea), and the monophyletic Apocrita, which contains morethan 95% of the estimated total number of species (Table 1). On the basis ofmolecular datasets and Bayesian phylogenetic approaches, Castro & Dowton (22)divide the Apocrita into two large clades (Figure 1). The first clade splits into theIchneumonoidea and Evaniomorpha +Aculeata, and the second is the Proctotrupo-morpha, which contains the Cynipoidea, Chalcidoidea, Platygastroidea, and Proc-totrupoidae. Most of these large groups are composed of parasitoids (Table 1).

Current phylogenies lack the resolution necessary to discern the exact origins ofall the life history transitions that have evolved in the different apocritan lineages.Nonetheless, certain higher level consistencies suggest some broad conclusions(22, 45, 48, 117, 158, 160). First, parasitism in the Hymenoptera likely has asingle early origin in the common ancestor of the Orussoidea + Apocrita. Thisancestral parasitoid was almost certainly an ectoparasitic idiobiont on concealedwood-boring beetle larvae, as orussoids and several basal apocritan lineages sharethese habits (Table 1). Second, many other developmental strategies have evolvedfrom this ground plan. The Ichneumonoidea is divided into the Braconidae andIchneumonidae. Most ectoparasitic ichneumonoids are idiobionts that still de-velop on concealed hosts (156), but a few groups, such as the Polysphinctini

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PARASITOID DEVELOPMENTAL STRATEGIES 235

TABLE 1 Species richness and biological habits of the major superfamilies of Hymenoptera

SuborderSuperfamily

Estimated numberof speciesa

Biological habits and developmentalstrategies

SymphytaXyeloidea 60 Phytophagous as immatures

Megalodontoidea 300 Phytophagous as immatures

Tenthredinoidea 7000 Phytophagous as immatures, some gallformers, some predators as adults

Cephoidea 100 Stem-boring herbivores as immatures

Siricoidea 200 Phytophagous and mycophagous as immatures

Orussoidea 70 Idiobiont ectoparasitoids of beetles(Buprestidae)

ApocritaStephanoidea 100 Idiobiont ectoparasitoids of wood-boring

beetles and wasps

Megalyroidea 100 Ectoparasitic idiobionts of beetles

Trigonalyoidea 100 Parasitoids oviposit on plants. Eggs eaten byLepidoptera but only develop if lepidopteranlarva is parasitized and thus developendoparasitically, possibly ashyperparasitoids

Aculeata 92,000 Basal lineages idiobiont ectoparasitoids. Nestprovisioning with adults providing multipleprey to offspring that feed as ectoparasitoidsalso common. Other species are predators orpollin/nectar feeders; many social species

Evanioidea 1200 Ectoparasitic idiobionts or cleptoparasites(Gasteruptiidae), endoparasitic koinobionts ofbeetles (Aulacidae), or egg predators(Evaniidae)

Ceraphronoidea 2000 Both ectoparasitic and endoparasitic; biologypoorly known

Ichneumonoidea 100,000 Basal lineages ectoparasitic idiobionts;multiple origins of endoparasitic koinobionts;polydnaviruses associated with selectedadvanced lineages

Chalcidoidea 100,000 Extremely diverse habits that includeectoparasitism, endoparasitism, predation,gall formation, seed feeding, and other formsof phytophagy

(Continued)

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TABLE 1 (Continued )

SuborderSuperfamily

Estimated numberof speciesa

Biological habits and developmentalstrategies

Platygastroidea 10,000 Endoparasitic idiobionts of eggs (Scelionidae)or endoparasitic koinobionts of larvae(Platygastridae)

Cynipoidea 4000 Basal lineages of endoparasitic koinobiontsthat complete their development asectoparasitoids. Derived lineages includeendoparasitic koinobionts (Figitidae) or gallformers (Cynipidae)

Proctotrupoidea 6000 Endoparasitic koinobionts of diverse hosts

Total 280–320,000 More than 75% of known species areparasitoids

aData extracted from References 45, 158, 160.

(Ichneumonidae, Pimplinae), are koinobionts that parasitize mobile hosts suchas spiders (129). Endoparasitism has also arisen multiple times in the Ichneu-monoidea (13, 156). Some of these endoparasitoids remain idiobionts, whereasothers are koinobionts that parasitize larvae or eggs. In some taxa, such as roga-dine braconids, the switch from an idiobiont to a koinobiont habit parallels theswitch from attacking concealed hosts to attacking exposed hosts (156). In othertaxa, endoparasitic koinobionts continue to develop in concealed hosts or haveeven switched from parasitizing exposed hosts back to concealed hosts (13).

Many aculeates are ectoparasitic idiobionts (Chrysidoidea, some Vespoidea andApoidea) or have evolved closely related provisioning strategies (Vespoidea andApoidea) in which females provide progeny with multiple paralyzed prey items(Figure 1). Several novel habits including pollination, predation, and sociality havealso evolved (Table 1). However, endoparasitism is extremely rare (possibly a fewchrysidids) (158). Unlike other apocritans, the egg canal of aculeates is separatefrom the ovipositor, which has become specialized into a “sting” for delivery ofvenom and other secretions. Loss of the ovipositor as an egg delivery apparatusis likely a major constraint that prevents aculeates from inserting eggs into thebodies of hosts. However, evolution of a specialized sting does allow predacious,pollinating, and social aculeates to inject venom into prey or to use venoms asdefensive secretions against other organisms.

The basal-most members of the Proctotrupomorpha appear to be endoparasiticidiobionts of eggs (6). Most platygastroids retain this plesiomorphic biology, al-though endoparasitic koinobionts that are egg-larval or larval parasitoids have alsoevolved. Cynipoids and chalcidoids, in contrast, have undergone levels of diversi-fication that rival ichneumonoids (Table 1). Idiobiont ectoparasitoids, koinobionts,

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Figure 1 Biological transitions during the evolution of the Apocrita inferred by parsimonyand using Orussoidea as an outgroup. Ground plan biologies were obtained from prior anal-yses (22, 45, 158) (Reproduced with permission from M. Dowton and J. Whitfield).

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and secondary herbivores (gall formers, seed wasps, and fig wasps) have all arisen,although the direction of these changes is unclear because of poorly resolved phy-logenetic relationships.

The Role of Ecological and Life History Factors

Parasite lineages are often predicted to parallel those of their hosts (19). Stud-ies of fig-pollinating wasps (Chalcidoidea, Agaonidae), which originated from aparasitoid ancestor, exhibit clear patterns of cophylogeny with their host plants(91). Taxa such as the Braconidae and Platygastroidea also show host group speci-ficities that strongly suggest that diversification patterns have been influenced byhost phylogeny (6, 156). In contrast, most studies of individual species have foundlittle evidence for parasitoid-host cophylogeny but do suggest that parasitoid hostranges are affected by other factors (5, 61, 160). Among these is whether para-sitoids develop as idiobionts or koinobionts (5, 48, 129, 130). For example, studiesof leafminer communities indicate that idiobionts have broad host ranges and par-asitize almost all hosts of suitable size in a given search environment. In contrast,koinobionts have narrower host ranges and tend to parasitize species that feed onthe same plant (5, 127, 129). Shaw (129) suggested these patterns arise becausethe more specialized developmental interactions between koinobionts and hostsfavor the evolution of specialized foraging behaviors that minimize encounterswith unsuitable species. In contrast, idiobionts maintain broader search habits andcan parasitize nearly all hosts of appropriate size they encounter.

Another consideration that affects parasitoid developmental strategies is mor-tality risks (114, 137). Among the most important trade-offs faced by organismsis whether to grow larger at the cost of increased development time or to developmore rapidly at the cost of reduced size (1). In the case of herbivores, conditionsthat increase development time often increase mortality risks (14, 115), which ex-tend to parasitoids if the herbivore is already parasitized (18). Although adult sizeis usually considered the primary target for selection in parasitoids (58, 92, 93,150), consideration of mortality risks leads to the alternative prediction that para-sitoids facing high mortality risks favor short development times over size, whereasspecies facing low mortality risks favor size at the cost of increased developmenttime. Parasitoids that attack exposed foliar-feeding species appear to experiencehigher levels of intraguild competition than do species that attack concealed hosts(63, 64), and, correspondingly, parasitoids attacking exposed hosts have shorterdevelopment times than do species attacking concealed hosts (16, 62). Parasitoidfecundity would also be expected to increase as opportunities to find hosts rise andthe probability of offspring surviving to adulthood declines (114). Because earlyhost stages (eggs, young larvae) are more abundant and, in general, more exposedthan late stages (pupae), parasitoids attacking younger hosts are predicted to havefecundities larger than those of parasitoids attacking older hosts. By similar logic,parasitoids attacking concealed hosts are predicted to have fecundities lower thanthose of parasitoids attacking exposed hosts. Given that parasitoids of young larvae

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are mostly endoparasitic koinobionts, which are better competitors for small hosts,higher fecundities also are more often associated with koinobionts, whereas lowerfecundities are associated with idiobionts that parasitize older stage hosts such aspupae (96).

While many gaps in our knowledge base remain, the phylogenetic and ecolog-ical literature overall suggest three key points. First, ectoparasitic idiobionts rep-resent the ancestral ground plan for the parasitoid lifestyle and from which otherdevelopmental strategies subsequently evolved. Second, endoparasitoids developin more intimate contact with host immune and developmental factors which haveoverall favored greater specialization, particularly of koinobionts. The ability toadapt to a more specialized host environment has also generally favored narrowerhost ranges in koinobionts than in idiobionts. Third, environmental factors such asintraguild competition and host mortality risks have affected other developmentaltraits such as offspring development times and adult fecundities.

PARASITOID DEVELOPMENTAL STRATEGIES

Successful parasitism of hosts by parasitoids usually depends on gene products thatthe adult wasp injects at oviposition or that offspring produce during the course ofdevelopment. These factors often induce complex physiological alterations in hoststhat benefit development of the parasitoid. As a result, the alterations parasitoidsinduce are sometimes called host regulation (148a). Most reviews on parasitoidphysiology focus on describing the identity of these factors and the effects theyhave on the host (10, 128, 154). In contrast, less attention has been paid to howthese gene products vary in relation to parasitoid ancestry and ecology. By nomeans does the phylogenetic literature allow researchers to unambiguously trace allevolutionary transitions in the biological habits of parasitoids. Nonetheless, giventhat the earliest parasitoids were likely ectoparasitic idiobionts, we can apply thephysiological literature to draw inferences about the sources and characteristicsof the regulatory molecules ancestral parasitoids produced and how this basal“toolkit” of gene products has changed with other developmental strategies.

The Basal Developmental Strategy: Idiobiont Ectoparasitoids

Quicke (117) describes several morphological adaptations in the Hymenoptera thatarose in association with the parasitoid lifestyle. Among these was a shift from alaterally compressed and short ovipositor, as found in sawflies, to a more circularmorphology of varying length. Internally, all female hymenopterans have meroisticovaries and secretory organs that include the venom (i.e., poison), Dufour’s, andcolleterial glands. Only the venom gland appears to produce factors that are injectedinto hosts or prey or that can be injected into intruders as defensive secretions.Comparative morphology therefore points to the venom gland as the most likelysource of effector molecules that ancestral ectoparasitic idiobionts introduce intohosts.

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The best characterized hymenopteran venoms are from aculeates that are euso-cial (honeybee) or ectoparasitic idiobionts that provision offspring with multiplehosts (Vespoidea and Apoidea) (Table 1). Although social species use venomsas defensive secretions, comparative analyses suggest their venoms are qual-itatively similar to those produced by parasitic aculeates. All produce blendsof biogenic amines (histamine and dopamine), peptides (melittins, mastoparans,and bradykinin-like), enzymes (phospholipases, hyaluronidases, and serine pro-teases), and paralytic toxins (philanthotoxins and pompilidotoxins) (37, 112).Philanthotoxins block postsynaptic glutamate and nicotinic receptors (101), andthe bradykinin-like peptides presynaptically block acetylcholine release (112).Dopamine in the venom of the parasitoid Ampulex compressa (Sphecidae) altershost behavioral activity prior to the onset of permanent paralysis (155).

Characterization of venoms produced by ectoparasitic idiobionts in other wasplineages is largely restricted to the braconid Habrobracon hebetor and the chalci-doids Eupelmus orientalis (Eupelmidae) and Nasonia vitripennis (Pteromalidae).In H. hebetor, paralytic activity is mediated by three partially characterized pro-teins that presynaptically block glutaminergic transmission (152), and other un-known factors affect host endocrine and metabolic activity (24, 95). The factorsin E. orientalis venom that cause paralysis are unknown, but enzymatic activities(phospholipase) similar to those in aculeate venoms are described (43). No venomcomponents from N. vitripennis have been characterized. However, physiologicalstudies indicate that its venom induces paralysis, disrupts hemocyte adhesion andmelanization of hemolymph, and causes several metabolic alterations including in-creases in lipid, protein, and amino acid levels in hemolymph (123–125). Changesin host nutrients occur when the heaviest feeding of offspring begins, which sug-gests they enhance progeny fitness (123, 124). The immunosuppressive effects ofvenom also support prior predictions that ectoparasitoids are likely to disrupt hostimmune responses that could interfere with feeding by offspring (141).

Modification of the Basal Strategy: Ectoparasitic Koinobionts

Ectoparasitic koinobionts are relatively uncommon and restricted to selected taxaof ichneumonoids and eulophids (Chalcidoidea) that parasitize concealed sawflies,larval Lepidoptera, or spiders (55, 117). All known species lay their eggs in prox-imity to hosts or strongly attach their eggs to inaccessible locations on the host.Progeny then feed externally. The venoms of koinobiont ectoparasitoids either aretransiently paralytic or have no paralytic activity. However, their venoms alwaysprevent the host from molting. Parasitoids in the genera Euplectrus and Eulophus(Eulophidae) inhibit host molting by altering ecdysteroid titers and metabolismand possibly reducing the sensitivity of host tissues to 20-hydroxyecdysone (20E)(75, 94). A 66-kDa protein that has a similar molt-blocking activity as crude venomhas been partially purified from Euplectrus comstockii, but the gene encoding thisfactor has not been identified (75). Hosts parasitized by E. comstockii also ex-hibit metabolic alterations such as precocious increases in hemolymph storage

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proteins (75). Venom from Euplectrus sp. near plathypenae similarly increaseshemolymph proteins and elevates lipid levels via enzymes that digest the fat body(100). Trypsin-like enzymes in the saliva of the parasitoid larva also contribute tothis process (99). The venoms of ectoparasitic koinobionts have not been impli-cated in suppression of the host immune response. However, Eulophus pennicornislarvae secrete factors while feeding on hosts that affect hemocyte adhesion andphagocytosis (122).

Diversification of Developmental Strategies: Endoparasitoids

As previously discussed, the shift from ectoparasitism to endoparasitism has arisenindependently multiple times in apocritan Hymenoptera. Several novel traits havealso likely evolved in response to offspring developing inside of another arthropod.For example, terrestrial insects, including ectoparasitoids, lay hydropic eggs, whichhave rigid chorions, which protect the embryo from desiccation, and prepackagedyolk sources. In contrast, many endoparasitoids lay anhydropic eggs (alecithal),with thin chorions and little or no yolk (41, 137). For adults, the reduced ener-getic costs of anhydropic eggs favor increases in fecundity, whereas the higherenergetic costs of hydropic eggs favor traits such as host feeding (67). For off-spring, anhydropic eggs correlate with the formation of specialized membranesfrom embryonic or polar body cells that envelop the developing parasitoid em-bryo (146). Once formed, these membranes allow the embryo to rupture out ofthe chorion and increase greatly in size by absorbing nutrients from the host (60,136). In some taxa (Scelionidae, certain Braconidae, and a few Aphelinidae), thesemembranes differentiate into cells called teratocytes that are released into the hostwhen the parasitoid first instar ecloses (33, 105). In other taxa (certain encyrtids,braconids, and platygastrids), extraembryonic membranes have likely favored theevolution of polyembryony (139). Larval stage endoparasitoids also exhibit noveltraits that facilitate movement in an aquatic environment or combat against inter-and intraspecific competitors (18, 138).

The second factor that has strongly affected trait evolution in endoparasitoidsis the increased risks progeny face from the host’s immune system. The activity ofsome ectoparasitoid venoms suggests that some ectoparasitic idiobionts producedimmunosuppressive molecules prior to the evolution of endoparasitism itself. Onceendoparasitism arose, however, other adaptations for circumventing host immunedefenses evolved. These include the development of surface features that protectendoparasitoids from host immune factors or the acquisition of symbionts thatproduce immunosuppressive molecules (128, 141). The best known of these sym-bionts are viruses in the family Polydnaviridae, which are divided into bracoviruses(BVs) and ichnoviruses (IVs) on the basis of their association with selected sub-families of phylogenetically advanced braconids (Microgastrinae, Cardiochilinae,and Cheloninae) and ichneumonids (Campopleginae and Banchinae) (78, 154). Allpolydnaviruses (PDVs) persist as stably integrated proviruses in the genome of as-sociated wasps and replicate in the ovaries of females. When the wasp oviposits,

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she injects a quantity of virus that infects host hemocytes and other tissues. PDVsdo not replicate in the wasp’s host, but expression of viral gene products has severaleffects on host physiology. The PDV-parasitoid association arose 73 ± 11 myaand has likely contributed greatly to the success and high species diversity of thewasp lineages that carry them (159). Although much less studied, endoparasitoidsin other lineages have formed associations with other types of viruses (15, 46, 87)as well as with yeast and bacteria (88, 97, 135, 162).

The picture that collectively emerges is that endoparasitism has favored impor-tant changes in parasitoid development that affect both adults and offspring. Theevolution of novel cell types such as teratocytes and the establishment of symbioticassociations have shifted parasitoids from relying on venom glands as the primarysource of molecules for manipulating host physiology. Symbiotic associations alsoprovide opportunities for shifting genes from the parasitoid to the symbiont, aswell as for acquiring novel genes from other organisms. Below, we summarizethe major interactions that occur between endoparasitic idiobionts, endoparasitickoinobionts, and hosts.

ENDOPARASITIC IDIOBIONTS Endoparasitic idiobionts parasitize sessile hoststages such as pupae and eggs. Pupal endoparasitoids are restricted primarily toa few subfamilies of Ichneumonidae (55, 158). The best-studied species from aphysiological perspective is Pimpla hypochondriaca, which injects a venom thatparalyzes and immunosuppresses its host (34, 152). Random sequencing of a P.hypochondriaca venom gland cDNA library identified several enzymes (trehalase,phenoloxidase, and serine proteases) and small cysteine-rich proteins similar toatracotoxins and omega-conotoxins (103, 104). Neither embryos nor feeding-stagelarvae of P. hypochondriaca appear to play a role in altering host development orimmune defenses.

Endoparasitoids that parasitize eggs have diversified more extensively than havepupal endoparasitoids. Three families of Hymenoptera are exclusively egg par-asitoids, Scelionidae (Platygastroidea), Trichogrammatidae (Chalcidoidea), andMymaridae (Chalcidoidea), and many species in other taxa have also evolved thishost usage strategy (6, 117, 136) (Figure 1) (Table 1). Unlike pupae, insect eggsinitially lack functional immune or endocrine systems, which develop during thecourse of embryogenesis. This may explain why most egg parasitoids prefer toparasitize young eggs rather than old eggs (26, 136). The greater abundance andvulnerability of eggs, compared with pupae, has also contributed to the larger di-versity of egg parasitoids. Egg parasitoids are among the smallest insects, however,and, as a consequence, little is known about their physiological interactions withhosts. The trichogrammatid Trichogramma pretiosum injects at the oviposition avenom with protease and phosphatase activity that digests yolk and the host em-bryo (136). As a result, newly hatched T. pretiosum larvae feed as saprophytes.In contrast, studies with the scelionid Telenomus heliothidis indicate that factorsinjected by the adult arrest host development and that proteolytic enzymes releasedfrom teratocytes mediate lysis of host tissues (136, 140).

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ENDOPARASITIC KOINOBIONTS Endoparasitic koinobionts have evolved in mosthymenopteran lineages. Most species oviposit into larvae or eggs of holometabolo-us insects, and offspring complete their development during the host’s larval or,more rarely, pupal stage (55, 117, 158) (Table 1). As previously discussed, hostapparency, predation risks, and competition favor oviposition into early instarhosts. That several egg-larval parasitoids facultatively oviposit in newly hatchedhost larvae (117) further suggests that the egg-larval or egg-pupal habit representsthe extreme of an evolutionary gradient toward early colonization of the host. Mostphysiological studies on endoparasitic koinobionts have focused on PDV-carryingbraconids and ichneumonids that parasitize Lepidoptera (10, 78, 128, 154). Amore limited but significant physiological literature has also accrued on figitids(Cynipoidea) in the genus Leptopilina and braconids in the genus Asobara thatparasitize Drosophila melanogaster (20, 21), aphidiine braconids that parasitizeaphid nymphs (39, 51, 52, 106, 108), and polyembryonic encyrtids (Chalcidoidea)that parasitize Lepidoptera (139).

DEVELOPMENTAL AND NUTRITIONAL INTERACTIONS Endoparasitic koinobiontseither paralyze hosts transiently or not at all when ovipositing (129). After oviposi-tion, however, parasitized hosts exhibit a wide variety of developmental alterations(10). Focusing on PDV-carrying wasps, all of the ichneumonids are solitary (oneoffspring produced per host), whereas the braconids are either solitary or gregar-ious (multiple offspring per host). Most species parasitize multiple instars of thehost but their offspring either obligately delay development until the host’s finalinstar or develop rapidly and complete development in an earlier instar. Again, thisdichotomy likely reflects differences among species in the mortality risks they face(62). Almost without exception, hosts parasitized by solitary species exhibit se-vere reductions in weight gain, delays in molting, and the inability to pupate. Hostsparasitized by gregarious species are also inhibited from pupating but usually ex-hibit less severe alterations in weight gain. The exception is chelonine braconids(Chelonus and Ascogaster spp.), which are all solitary, egg-larval parasitoids.These wasps cause hosts to initiate precocious metamorphosis one instar earlierthan normal but prevent the host from actually pupating (81). The parasitoid thencompletes its larval development and emerges to pupate from the prepupal stageof the host.

These developmental alterations are almost always associated with changesin host endocrine physiology (10). The most common endocrine changes are in-creases in juvenile hormone (JH) titers and a failure of 20E titers to rise, as occursin nonparasitized hosts. Few studies indicate that increases in the JH titer are dueto alterations in JH synthesis by the host’s corpora allata (28, 89). More often, ele-vated JH titers correlate with reductions in the activity of host metabolic enzymessuch as JH esterase (7, 31, 40) or the release of JH from the parasitoid larva (28).Changes in host ecdysteroid titers involve several factors including altered synthe-sis and release of prothoracicotropic hormone (PTTH) (65, 142), insensitivity ofprothoracic glands (PTGs) to PTTH stimulation (73), reduced biosynthetic activity

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of PTGs (107, 110, 142), PTG cell death (44), and altered ecdysteroid metabolism(10). Alterations in levels and storage of neurohormones and neurotransmitters thatpotentially affect development have also been reported (102, 165). Fewer studieshave been conducted with PDV-carrying egg-larval parasitoids, but experimentswith different Chelonus spp. indicate that precocious metamorphosis occurs be-cause JH titers decrease earlier than normal through a combination of corporaallata inactivation, increased JH esterase activity, and an altered ecdysteroid titer(72, 81, 120).

PDV infection contributes to many of these endocrine changes, although otherfactors, including teratocytes, venom, and the parasitoid larva itself, are also im-portant (10, 78, 154). For example, the parasitoid larva is essential for inductionof precocious metamorphosis in the Chelonus inanitus–Spodoptera littoralis sys-tem (111) and also influences the expression of C. inanitus bracovirus genes inhost’s tissues (17). In some PDV-carrying braconids, factors produced by PDVsand teratocytes interact to alter host development (10, 109); in others venom af-fects PDV gene expression (164). At present, little is known about the specificPDV and parasitoid genes products that cause these developmental alterations.Expression of protein tyrosine phosphatase (PTP) genes encoded by Toxoneuronnigriceps bracovirus (TnBV) in host PTGs (P. Falabella, P. Caccialupi, P. Varric-chio, C. Malva & F. Pennacchio, unpublished results) may be responsible for thedisruption of PTTH signaling via altered phosphorylation of pathway components(53, 109, 110), and two novel genes encoded by C. inanitus bracovirus (CiBV)are upregulated at the onset of precocious metamorphosis in S. littoralis larvae(71). In addition, the cys-motif gene family encoded by Campoletis sonorensisichnovirus (CsIV) has been implicated in altered translation of host proteins (132,133). Another protein (TSP14) secreted by teratocytes from Microplitis croceipesshares limited homology with the cys-motif genes and exhibits similar biologicalactivity (32, 153).

PDV-carrying wasps also alter host nutritional physiology (144, 145). Thesemetabolic alterations could indirectly arise as a result of the changes that occur inhost endocrine physiology. For example, elevating host JH titers and blocking therise in 20E levels could be partially responsible for increasing host hemolymphprotein titers (109, 149). On the other hand, some hosts exhibit specific changesin nutritional physiology that suggest PDV- or teratocyte-produced gene productshave more selective effects. For example, infection of hosts by CsIV greatly reducesthe abundance of arylphorin but does not affect other hemolymph proteins such aslipophorin and transferrin (132, 133). Triglycerides and glycogen deposits in fatbody are also greatly reduced in hosts parasitized by C. sonorensis, but trehalosetiters in hemolymph actually increase (148). In contrast, Cotesia kariayi enricheshost hemolymph via breakdown of the host fat body by factors released fromteratocytes (98).

Endoparasitic koinobionts other than PDV-carrying species also affect hostdevelopment. This is well illustrated by aphidiine braconids that disrupt host re-production by causing degeneration of the ovaries (39, 106, 113). In Aphidius ervi,

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host castration is also associated with increases in protein, amino acid, and acyl-glycerol levels in the hemolymph that coincide with the exponential growth phaseof the parasitoid larva (106, 118). A dimeric protein in A. ervi venom, homologousto gamma glutamyl transpeptidases, has been implicated in ovary degeneration(P. Falabella, L. Riviello, P. Caccialupi, C. Malva & F. Pennacchio, unpublishedresults), while changes in host nutritional physiology are due in part to increasesin the biosynthetic activity of bacterial endosymbionts (Buchnera) that provideessential nutrients for the aphid (27, 108, 118). Venom-mediated castration is alsocomplemented by factors from teratocytes that extraorally digest host reproductivetissues and transport host fatty acids to the parasitoid (51, 52, 147).

IMMUNE INTERACTIONS Nonpermissive hosts often eliminate endoparasitoids byencapsulation, which involves adhesion of hemocytes to the parasitoid egg or larva(85, 128, 141). Larval endoparasitoids evade encapsulation and other host defensespassively and/or by suppressing the host’s immune system (83, 128, 141). Passivestrategies include oviposition or development in host tissues that are inaccessi-ble to host hemocytes. Many platygastrids, for example, oviposit into the host’sgut or ganglia (141), while some braconids (Asobara spp.) lay eggs that embedthemselves in the host fat body (20). Other endoparasitoids oviposit in the host’shemocoel but passively evade encapsulation because their progeny have surfacefeatures that are not recognized as foreign or to which the hemocytes are unableto bind (128). For example, immunoevasive ovarial proteins coat the eggs of sev-eral braconids in the genera Cotesia and Toxoneuron (4, 36, 66, 128, 143). Incontrast, eggs from Cotesia congregata are fully susceptible to encapsulation anddepend on C. congregata bracovirus (CcBV) infection for protection, but larvaehave surface features that protect them from encapsulation, independent of virusinfection (84). Other parasitoids, such as the polyembryonic encyrtid Copidosomafloridanum, remain enveloped by their extraembryonic membrane throughout de-velopment, which is required for both nutrient absorption and protection from thehost’s immune system (29, 56).

Most PDV-carrying parasitoids also immunosuppress their hosts by killing ordisrupting the ability of hemocytes to form capsules (35, 83, 84, 90, 128, 141,154). In some parasitoid-host systems these changes occur in response to directvirus infection of hemocytes (8, 9), whereas in others, secreted viral proteins affectimmune function (154). Viral infection also appears to disrupt encapsulation ofthe wasp only in some species (42), whereas in others infection has more globalimmunosuppressive effects that disrupt the ability of host immune cells to encap-sulate or phagocytize any foreign target (128, 141, 154). PDV-carrying parasitoidsalso suppress humoral immune responses such as melanization and antimicrobialpeptide production (11, 42, 86, 134). Melanization depends in part on conversionof the inactive zymogen prophenoloxidase to active phenoloxidase via serine pro-tease cascades (23). A serine protease in the venom of Cotesia rubecula that blocksmelanization was recently identified (163), while CsIV reduces melanization byinhibiting enzymes in the melanization pathway at the posttranscriptional level

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(131). Outside of PDV-carrying wasps, endoparasitoids in the genus Leptopilina(Figitidae) inject material from the venom ( = long) gland that blocks hemocyteadhesion and capsule formation by their drosophilid hosts (46, 79, 126). Notably,the long gland of Leptopilina boulardi contains virus-like particles, but whethersuppression of encapsulation is due to a factor encoded by these particles, otherlong gland molecules, or a combination thereof is unclear.

Relatively few genes conclusively mediate immunosuppression of hosts. Sup-pression of phagocytosis and encapsulation by MdBV is mediated by expressionof a virally encoded mucin called glc1.8 on the surface of infected hemocytes(8, 9), while two proteins (CrV1 and CrV2) encoded by CrBV are expressed andsecreted from virus-infected host fat body that binds to hemocytes (2, 3). How-ever, it is unclear whether CrV1 actually blocks host hemocytes from binding to orencapsulating any foreign target. T. nigriceps bracovirus encodes a gene (TnBV1)that has apoptosis-like effects on cells that may contribute to the alterations thatoccur in host hemocytes after parasitism by T. nigriceps (82).

Other PDV genes are indirectly implicated in immunosuppression because theyshare homology with genes that have immune functions in insects or other organ-isms. These include genes identified in several bracoviruses and ichnoviruses,which encode products with homology to inhibitor κB (IκB) proteins (49, 154),that regulate NF-κB transcription factors (69); PTPs (25, 116, 154) homologousto bacterially encoded PTPs that block phagocytosis by vertebrate immune cells(30); and C-type lectins, which have been implicated in insects as humoral patternrecognition receptors (57, 74). Candidate immunosuppressive genes identified out-side of PDVs include RhoGAP-like proteins in the venom secretions of L. boulardi(80, 126, 157) and virus-like particles of Venturia canescens (121).

PARASITOID DEVELOPMENTAL STRATEGIES:CONSENSUS FEATURES

The preceding discussion makes clear that the gene products parasitoids produce,their delivery, and their effects on hosts vary with developmental strategy. De-spite this variation, we suggest two features of parasitoid-host interactions areconserved. First, most if not all endoparasitoids have evolved traits for evasion ordisruption of the host’s immune response. Whereas the earlier literature generallyignored the significance of host immune defenses to ectoparasitoids, recent studiesindicate they often immunosuppress their hosts. The coevolutionary processes ofhost immune resistance and parasitoid virulence in turn have greatly affected thegenetic structure and population dynamics of natural populations (54, 59, 76, 77).

The second feature we see as shared among parasitoids relates to nutritionalphysiology. Parasitoids cause a diversity of developmental alterations in hosts thatat first glace have little in common. Upon closer inspection, however, we suggestthe diversity of tactics parasitoids have evolved to exploit host resources sharethe goal of synchronizing host nutrient availability with key phases in offspring

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development. Parasitoids achieve this goal by altering host metabolism, mobi-lizing stores of nutritional resources, and/or disabling metabolic sinks such asmetamorphosis, reproduction, or both. Parasitoids in effect redirect energetic re-sources away from host tissues and toward their progeny. For example, koinobiontendoparasitoids almost always juvenilize their larval stage hosts in a manner thatcauses nutrient availability in the hemolymph to increase and that disrupts nutrientuptake by host tissues (149). Ectoparasitic koinobionts such as E. comstockii (75)or egg-larval parasitoids such as Chelonus spp. (72) similarly alter host endocrinephysiology in a manner that causes hosts to precociously produce nutrients suchas storage proteins. Parasitoids that attack nymphal or adult hosts confront a dif-ferent host environment, but the goal of manipulating host nutritional physiologyis similar to that of larval parasitoids. This is well illustrated by aphid parasitoidssuch as A. ervi. The primary metabolic sink of its host is reproduction, and notsurprisingly A. ervi produces gene products that suppress host reproduction (39,106). Thus, in our view the primary adaptive significance of altering host endocrinephysiology and reproduction is metabolic, whereas arrested development or inhi-bition of metamorphosis is an indirect consequence of the parasitoid redirectinghost nutritional resources. Notably, suppression of host reproductive activity andredirection of host nutritional physiology occur in many other parasites (70). Insectherbivores also exhibit many ecological, behavioral, and physiological adaptationsto compensate for the improper balance of carbon and nitrogen in plants (38, 50).

EVOLUTION OF PARASITOID VIRULENCE GENES

The variation in parasitoid developmental strategies we describe in this reviewrequires that genetic differences exist in the molecules that different parasitoidsproduce and introduce into hosts. One source of this genetic variation could be inthe structure and biochemical function of these molecules, and another could bein how these molecules are regulated at the transcriptional, translational, or post-translational level. No parasitoid genomes have been fully sequenced, but studiesof selected genes and genomic information on symbionts, such as PDVs, provideinsights into how parasitoid virulence genes evolve. Because of the importanceof PDVs to the biology of many koinobiont endoparasitoids, the genomes of BVsassociated with C. congregata and M. demolitor and an IV from C. sonorensishave been fully sequenced and a few other PDVs have been partially sequenced(49, 154). Sequence comparisons of these isolates suggest that BVs and IVs sharelittle sequence identity. Combined with phylogenetic studies, this suggests the as-sociation of BVs with braconids and IVs with ichneumonids arose independently(154, 161).

However, IVs and BVs share several organizational features that likely reflecttheir analogous roles in parasitism. First, PDV genomes encode relatively few typesof genes that are expressed in parasitized insects (i.e., putative virulence genes).For example, CsIV encodes four recognizable gene types, MdBV encodes five, and

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CcBV encodes nine (49, 154). Second, genes have exon/intron structures and otherfeatures that suggest they are of eukaryotic rather than viral or prokaryotic origin.One obvious source of gene acquisition is from a shared wasp ancestor or novelacquisition(s) from their current wasp host. An example of ancestral acquisitionin IVs is a class of virulence genes called rep genes that have been identified inseveral different IV species (78, 154). Likewise, genes encoding putative PTPsfrom several species of BVs have been identified (25, 116, 154). Examples ofpotentially more recent gene acquisitions would be the glc genes, known only fromMdBV, and the vinnexin genes, which are found only in CsIV (154). PDV genessuch as PTP and vinnexin are homologous to genes from other insects, includinghymenopterans such as the honey bee, which suggests that orthologs of these genesalso exist in braconid and ichneumonids that carry these viruses. Some PDV genesare also related to gene products that are introduced into hosts by other parasitoids,which suggests some virulence genes encoded by PDVs are potentially producedby other wasp tissues. For example, the cys-motif genes encoded by CsIV arehomologous to a protein (TSP14) secreted by teratocytes from M. croceipes and tocysteine-rich proteins present in the venom secretions of pimpline ichneumonids(32, 104).

PDVs encode relatively few distinct types of genes, but these factors haveundergone extensive duplication and divergence to produce large gene families(78, 154). Some of these genes exist as closely linked gene pairs on the same viralsegment, which suggests they arose from tandem duplication events; others arelocated on different viral genomic segments and potentially derived from crossoverevents. Several gene families have also diversified greatly, both within and betweenspecies, to produce many novel gene variants. For example, CsIV encodes 28different rep genes; CcBV, MdBV, and TnBV encode 24, 14, and 8 different PTPs,respectively (68, 116, 154). Sequence divergence among the CcBV PTPs in turnis higher than the PTP diversity of many vertebrates, whose family members havedifferent biological functions (25, 49, 116, 154). Sequence analysis also suggeststhat expansion of gene families has produced proteins with novel functions. Forexample, several PTP family members in the CcBV and MdBV genomes lackcatalytic sites, which suggests they are no longer phosphatases but may functionas traps for phosphorylated tyrosine proteins (116).

Associated with these gene duplication events have been shifts in the abundanceof viral gene segments and apparent alterations in regulatory elements that affectthe abundance and spatial expression patterns of different virulence genes. PDVgenome segments vary in molarity, which results in unequal gene copy numberand protein titers for different virulence genes. Comparative studies with MdBVand CsIV also indicate that genes located on high copy number segments areabundantly and globally expressed in parasitized insects, whereas genes locatedon low copy number segments are usually expressed at low abundance in specifichost tissues (154).

Overall, these patterns indicate that virulence genes encoded by PDVs have un-dergone a large-scale expansion that has led to new or modified genetic programs

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for mediating interactions with hosts. The developmental complexity and highlevels of species diversity that have evolved in the parasitoid lineages that carryPDVs may also reflect the exploitation of the large number of virulence genesthat have evolved from diversification. Further complexity has arisen potentiallyvia acquisition of novel genes from a given wasp or host. Although regulatorydomains are poorly characterized, that specific PDV gene family members aredifferentially expressed in specific host tissues suggests that regulatory elementevolution is another important factor in diversifying virulence gene function. Forexample, although the biochemical function of many PTP genes may be similar,their roles in parasitism may well be different depending on the host tissue in whichthey are expressed and the particular substrate with which they interact. Althoughour knowledge of virulence gene evolution in parasitoids is largely restricted toPDV-carrying species, gene loss, acquisition, and diversification events likely un-derlie the shifts in developmental strategies and host usage patterns of all otherparasitoids.

CONCLUDING REMARKS

This chapter has explored the diversity in parasitoid-host developmental inter-actions from the perspective of ancestry and ecological history, physiology, andgenomics. We fully recognize that many gaps exist in our understanding of hy-menopteran phylogenetic history and that relatively few species of parasitoids havebeen studied from a physiological and molecular perspective. The limited knowl-edge we have nonetheless does provide important insights into the evolution of theparasitoid lifestyle.

Future advances require more robust phylogenies than are currently available formany taxa. Comparative genomic data on selected species, within major parasitoidlineages, are strongly needed as are comparative data on the regulatory networksand function of virulence genes. Recent insights into the diversification and regu-lation of PDV gene families suggest that expansion of virulence gene families incombination with shifts in regulatory domains is important in generating geneticvariation among parasitoid species. We speculate this variation underlies adap-tive radiation in many parasitoid lineages but whether these gene families derivefrom genes encoded by non-PDV-carrying parasitoid ancestors or whether theywere acquired from hosts, other viruses, or some combination thereof is unclear. Ifancestors of PDV-carrying wasps produce orthologous virulence factors, we nextneed to ask whether expression of these factors has shifted from the venom glandin more primitive lineages composed of idiobionts to other delivery mechanismssuch as teratocytes or PDVs in lineages of koinobionts, which would allow thesefactors to persist in the host for longer periods. It is also unclear whether similaror different virulence genes have diversified in other lineages of parasitoids suchas chalcidoids that also exhibit levels of species richness similar to those of PDV-carrying ichneumonoids. The combination of phylogenetic data with increasingly

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powerful tools for comparing genomes and gene expression is in our view thebest option for understanding the evolution of biological diversity in this complexgroup of insects.

ACKNOWLEDGMENTS

We thank Andy Austin, Mark Dowton, Carla Malva, Jim Whitfield, and BruceWebb for sharing manuscripts and information with us during the preparation ofthis review, and Maria Guarino for editorial assistance. We also thank Gildo Trem-blay and Brad Vinson for introducing us to the study of parasitic Hymenoptera andfor many stimulating discussions over the years. Some aspects of our own researchreported herein were funded by grants from the U.S. Department of AgricultureNational Research Initiative, National Science Foundation, and National Institutesof Health to M.R.S., and from the Ministry of University and Research, Ministryof Agriculture, and European Union to F.P.

The Annual Review of Entomology is online at http://ento.annualreviews.org

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November 2, 2005 13:47 Annual Reviews AR263-FM

Annual Review of EntomologyVolume 51, 2006

CONTENTS

SIGNALING AND FUNCTION OF INSULIN-LIKE PEPTIDES IN INSECTS,Qi Wu and Mark R. Brown 1

PROSTAGLANDINS AND OTHER EICOSANOIDS IN INSECTS: BIOLOGICALSIGNIFICANCE, David Stanley 25

BOTANICAL INSECTICIDES, DETERRENTS, AND REPELLENTS INMODERN AGRICULTURE AND AN INCREASINGLY REGULATEDWORLD, Murray B. Isman 45

INVASION BIOLOGY OF THRIPS, Joseph G. Morse and Mark S. Hoddle 67

INSECT VECTORS OF PHYTOPLASMAS, Phyllis G. Weintrauband LeAnn Beanland 91

INSECT ODOR AND TASTE RECEPTORS, Elissa A. Hallem, AnupamaDahanukar, and John R. Carlson 113

INSECT BIODIVERSITY OF BOREAL PEAT BOGS, Karel Spitzerand Hugh V. Danks 137

PLANT CHEMISTRY AND NATURAL ENEMY FITNESS: EFFECTS ONHERBIVORE AND NATURAL ENEMY INTERACTIONS, Paul J. Ode 163

APPARENT COMPETITION, QUANTITATIVE FOOD WEBS, AND THESTRUCTURE OF PHYTOPHAGOUS INSECT COMMUNITIES,F.J. Frank van Veen, Rebecca J. Morris, and H. Charles J. Godfray 187

STRUCTURE OF THE MUSHROOM BODIES OF THE INSECT BRAIN,Susan E. Fahrbach 209

EVOLUTION OF DEVELOPMENTAL STRATEGIES IN PARASITICHYMENOPTERA, Francesco Pennacchio and Michael R. Strand 233

DOPA DECARBOXYLASE: A MODEL GENE-ENZYME SYSTEM FORSTUDYING DEVELOPMENT, BEHAVIOR, AND SYSTEMATICS,Ross B. Hodgetts and Sandra L. O’Keefe 259

CONCEPTS AND APPLICATIONS OF TRAP CROPPING IN PESTMANAGEMENT, A.M. Shelton and F.R. Badenes-Perez 285

HOST PLANT SELECTION BY APHIDS: BEHAVIORAL, EVOLUTIONARY,AND APPLIED PERSPECTIVES, Glen Powell, Colin R. Tosh,and Jim Hardie 309

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viii CONTENTS

BIZARRE INTERACTIONS AND ENDGAMES: ENTOMOPATHOGENICFUNGI AND THEIR ARTHROPOD HOSTS, H.E. Roy,D.C. Steinkraus, J. Eilenberg, A.E. Hajek, and J.K. Pell 331

CURRENT TRENDS IN QUARANTINE ENTOMOLOGY, Peter A. Follettand Lisa G. Neven 359

THE ECOLOGICAL SIGNIFICANCE OF TALLGRASS PRAIRIEARTHROPODS, Matt R. Whiles and Ralph E. Charlton 387

MATING SYSTEMS OF BLOOD-FEEDING FLIES, Boaz Yuval 413

CANNIBALISM, FOOD LIMITATION, INTRASPECIFIC COMPETITION, ANDTHE REGULATION OF SPIDER POPULATIONS, David H. Wise 441

BIOGEOGRAPHIC AREAS AND TRANSITION ZONES OF LATIN AMERICAAND THE CARIBBEAN ISLANDS BASED ON PANBIOGEOGRAPHIC ANDCLADISTIC ANALYSES OF THE ENTOMOFAUNA, Juan J. Morrone 467

DEVELOPMENTS IN AQUATIC INSECT BIOMONITORING: ACOMPARATIVE ANALYSIS OF RECENT APPROACHES, Nuria Bonada,Narcıs Prat, Vincent H. Resh, and Bernhard Statzner 495

TACHINIDAE: EVOLUTION, BEHAVIOR, AND ECOLOGY,John O. Stireman, III, James E. O’Hara, and D. Monty Wood 525

TICK PHEROMONES AND THEIR USE IN TICK CONTROL,Daniel E. Sonenshine 557

CONFLICT RESOLUTION IN INSECT SOCIETIES, Francis L.W. Ratnieks,Kevin R. Foster, and Tom Wenseleers 581

ASSESSING RISKS OF RELEASING EXOTIC BIOLOGICAL CONTROLAGENTS OF ARTHROPOD PESTS, J.C. van Lenteren, J. Bale, F. Bigler,H.M.T. Hokkanen, and A.J.M. Loomans 609

DEFECATION BEHAVIOR AND ECOLOGY OF INSECTS, Martha R. Weiss 635

PLANT-MEDIATED INTERACTIONS BETWEEN PATHOGENICMICROORGANISMS AND HERBIVOROUS ARTHROPODS,Michael J. Stout, Jennifer S. Thaler, and Bart P.H.J. Thomma 663

INDEXESSubject Index 691Cumulative Index of Contributing Authors, Volumes 42–51 717Cumulative Index of Chapter Titles, Volumes 42–51 722

ERRATAAn online log of corrections to Annual Review of Entomologychapters may be found at http://ento.annualreviews.org/errata.shtml

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evolution of development strategies in parasitic wasps

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