Archives of Insect Biochemistry and Physiology 13:3-27 (1990) How Parasitoids Deal With the Immune System of Their Host: An Overview S. Bradleigh Vinson Department of Entomology, Texas ADM University, College Station, Texas Insects have evolved many mechanisms that reduce their potential for serving as hosts for entomophagous species. Some of these mechanisms involve escape, mimicry, and repellancy, which are effective defense mechanisms against both predators and parasitoids. But, insects have a second line of defense against parasitoids and parasites. These may include repellancy and a cuticular barrier t o invasion but they include several internal defenses that are collectively referred to as immune mechanisms. The current understanding of insect immunity is reviewed as background to examining the ways in which insect parasitoids have evolved to successfully handle the immune system of the host. The various means that parasitoids utilize to handle the insect immune systems have been divided into five approaches. These five approaches are described and current knowledge of the mechanisms used by parasitoids to deal with the immune system of their host is explored. Key words: internal defense, immune evasion, immune supression, inverterbrate immunity, host-parasitoid relationships INTRODUCTION The immune system of insects has fascinated invertebrate physiologists since the early work of Metchnikoff [l]. However, the insect immune system remains poorly understood in spite of the extensive research conducted over the last several decades [2-61. If the insect immune system was understood and ways to interfere with the system were known, a powerful manipulative tool would be available to biological control practioners. One approach for understanding the insect immune system is to determine how insect parasitoids deal with the defense systems of their host. However, this requires some information about the insect defense system. Acknowledgements: Approved as TA 24959 by the Texas Agricultural Experiment Station. Appreciation is extended to Heather McAuslane and Clint Ready for editorial suggestions and to Pauline Lawrence for her patience. Received July 14,1989; accepted September 23,1989. Address reprint requests to Dr. S. Bradleigh Vinson, Department of Entomology, Texas A&M University, College Station, TX 77843-2475. 0 1990 Wiley-Liss, Inc. 4 Vinson Insects represent a very large, diverse class of organisms. Most studies of the insect immune system have utilized Diptera, Orthoptera, or Lepidoptera, yet aspects of the immune-competent circulatory system of these orders differ. The hemolymph of some orders have cellular forms absent in others, the hemolymph of some species melanizes on exposure, while in others the hemolymph coagulates with little melanization. We may predict that aspects of the insect immune system among the various orders may also differ. How parasitoids deal with the different host insect defense systems also varies. I plan to 1) summarize the different host insect defenses against parasitoids emphasizing the host immune system and 2) examine what is known about how parasitoids deal with the defensive systems. THE INSECT DEFENSE SYSTEM Insect defenses involve a number a behavioral and physiological adaptations that reduce the chance of the organisms becoming a host. In this overview, I concentrate on the physiological defenses, emphasizing the immune system. It was initially assumed that the insect immune system was a less complex form of the vertebrate system although today we know that the antigen-antibody system of vertebrates is absent in insects. The insect system is complex and responds differently to allogenic and xenogenic tissue transplantation  as well as to various viruses, microorganisms (bacteria, protozoa, fungi), multicellular organisms, and abiotic material [3,6]. Further, our understanding of the insect immune system remains largely descriptive, although the mechanisms involved in insect immune responses and how pathogens, parasites, and parasitoids evade or interfere with the system are beginning to emerge. These defensive physiologial responses are outlined in Table 1 and can be divided into those that have an external result and those that occur internally. TABLE 1. Physiological Insect Defense Mechanisms External Deterrents and anti-microbial agents Cuticular barrier Internal-external Reflex bleeding Cuticular encystment Internal Coagulation Humoral Inducible factors Antibacterial proteins Lysozymes Constitutive factors Lectins (agglutinins) Phenyloxidases Cellular Phagocytosis Nodule formation Encapsulation parasitoid Host Immune Resistance 5 External Defense System Many insects produce or acquire and release a variety of compounds from a variety of glands that deter attack by predators and probably parasitoids [8,9]. These same defensive compounds can be used as host-locating cues by parasitic species [lo]. For example, trans-p-farnesene [ll]is an aphid alarm pheromone  that also acts as a searching kairomone for Aphidius ervi (F. Pennacchio, personal communication). Some Lepidoptera regurgitate droplets that contain secretions that act as kairomones, but these secretions also can deter attack . In some cases these secretions are antimicrobial. For example, the imported fire ant, Solenopsis invictu, releases several antimicrobial dialkylpiperidines . The cuticle also serves as a barrier to potential invading organisms. Many bacteria and protozoa are unable to penetrate the host cuticle and are only pathogenic when the cuticle's integrity is breached [15,16]. For example, a number of parasitoid hymenoptera transmit pathogens via their ovipositor [15,17] and certain symbiotic bacteria are introduced into the host by their nematode symbionts [MI. The cuticle, or chorion of eggs, also influences the success of certain parasitoids. For example, some species of Trichogrummu are unable to penetrate the thicker chorion of some host eggs [19-211 and the thicker cuticle of older larvae has been reported to reduce the success of parasitism by several species of parasitic hymenoptera . Internal-External Defensive System Some insect defense mechanisms involve internal factors that have an external effect. One of these is reflex bleeding, which is most common in Coleoptera and Orthroptera. When the insect is attacked hemolymph escapes from limb joints, the base of the wings, and other membranous areas of the body . The released hemolymph often contains compounds that also have repellent properties , but in other cases the hemolymph works by rapidly coagulating, entanghng the predator  and presumably a parasitoid. A second defense mechanism, cuticular encystment, involves internal factors that have an external result. Cuticular encystment, first described by Arthur and Ewen , has been reported in a few lepidoptera  as a result of internal parasitization. In the host TrichopIusiu ni, the eggs of Bunchusfluvescens hatch and the larvae appear to migrate to a bubble-like cyst that develops between the cuticle and epidermis on the dorsum of the penultimate segment of the host. The cyst begins to form prior to egg hatch and Ewen and Arthur  reported that the cyst also formed in response to venom gland fluid injected by the parasitoid but not to either implanted eggs or other tissues. However, Curnpoletis sonorensis eggs artificially into T. ni not only stimulated cyst formation but the cyst contained the egg . These results suggest that cyst forrnation is not a unique property of the venom gland contents, but a defensive phenomena of the host in response to certain kinds of foreign material. How the foreign material ends up in the cyst is unknown. A similar phenomenon, referred to as expulsion , occurs when cysticeroid or nematode parasites are first encapsulated and then are secreted through the epidermis and shed. Expulsion has not been considered a host defense because the organism is presumably lulled; however, expulsion has many similarities to 6 Vinson cuticular encystment. Metalnikov  also reported a form of expulsion. Working with bacteria he found that nodules that formed were sometimes attached to the body wall and discharged. He  considered these abscesses a form of defense. Internal Defense System The internal insect defensive systems consists of both humoral and cellular responses, many of which are interrelated (Table 1).Some may be passive structural barriers similar to the cuticle, such as the peritrophic membrane that lines the midgut. The more active components include circulating hemocytes of various types, numerous proteins, complex carbohydrates, and other biochemicals. Some of the biochemicals are innately present and others are synthesized in response to invasion . But first the invading organism must penetrate the structural barriers, usually the cuticle. Insects respond to integumental damage by coagulation of the hemolymph, which serves to seal the wound and initiate wound repair . Whether endo- or ectoparasitic, most parasitoids must breach the integument either to deposit their eggs and inject venoms (endoparasitoids) or to inject venoms and feed through the integument (ectoparasitoids). For the endoparasitoids the coagulation of hemolymph around the wound and wound repair are of little concern other than alerting the internal defense systems to the invasion. For the ectoparasitoidsboth coagulation and wound repair may be of importance. Coagulation. Coagulation of insect hemolymph involves two distinct processes. Cell agglutination involves coagulocytes(granularhemocyte) which form long cytoplasm strands that result in a fiberous network that entraps other hemocytes to seal the wound. Plasma coagulation is where the plasma jells in response to factors released by granular hemocytes [Z]. Gregoire and Goffinet  divided the coagulation process into four types depending on the way the process is initiated. Although the nature and origin of the clottableproteins and the factors that initiate the coagulation process are unknown ,Brehelin  reported a clotting protein which he suggests is a high-molecular-weight lipoglyco-protein complex. This clotting protein appears to require both a cellderived and a plasma coagulogen [37l. The plasma coagulogen may involve a lipophorin  while the cellular coagulogen may involve a disulphide-linked protein . It has been suggested that hemocytes involved in coagulation and wound repair respond to an injury factor . The purification of an injury factor has been reported , but the role of such a factor is yet unknown. Humoral. The hemolymph of insects containshumoral factors important in the immune responses. Some are normally present in the hemolymph or are released by cells in response to infection without de novo synthesis; others appear to be inducible and require de novo synthesis. The latter of these, the inducible antibacterial factors first reported by Briggs  and Stephens , have been isolated and characterized as a group of proteins, the cercopins (about 4,000 kD") and the larger actins . These proteins have received considerable attention and are the subject of several reviews [4,44,45]. Lysozyme has also been claimed as an important antibacterial factor  *Abbreviations used: CsV = Campoletis sonorensis polydnarivus; ER = endoplasmic reticulum; = granular hemocyte, kD = kilo-Dalton; Oe = oenocytoid, PDS = plasmatocyte depletion factor; PL = plasmatocye, PO = phenoloxidase; PPAE = prophenyloxidase activating enzyme; PPO = prophenyloxidase; Pr = prohemocyte; PTU = phenylthiourea; RF = recognition factor; Sp = spherule cell; Th = thrombocytoid; VLP = virus-like particle. FB = foreign body; Gr Parasitoid Host Immune Resistance 7 but its importance has been debated [47,48]. It is suggested that lysozyme digests the peptidoglycan layer of the bacteria after actins have attacked the outer membrane and the cercopins have worked synergistly as detergents on the exposed inner membrane . The peptidoglycan acts as an inducer of the antibacterial protein . The lectins (hemaglutinins) have long been known in both plants and animals and Bernheimer  demonstrated their presence in a number of lepidoptera. Most of the purified insect lecints have galactose specificity . Although the occurrence and characteristics of the galactose specific lectins have been the subject of a number of studies [52,53], lectins of other specificities are probably present . Lectins may play a role in hemocyte recognition and removal of foreign material  although details of their role at present are not clear [5,56]. Acid mucopolysaccharides are also present in insect hemolymph and have been reported around stressed granulocytes and sphemlocytes . More recently, Anderson and Chain  have reviewed the release of an acid mucopolysaccharide by the granulocytes of Galleria upon exposure to Bacillus cereus. The cells hypersecrete a mucus which coats and entraps the bacteria prior to nodule formation and phagocytosis. The injection of certain bacteria such as B. cereus is also reported  to cause a deletion of circulatingplasmatocytes-a plasmatocyte depletion factor. PDS is suspected to be released from certain exposed hemocytes which cause the plasmatocytes to attach to the hemal lining where they are able to move to inflammatory foci . The prophenoloxidase-phenoloxidasesystem in insects has been implicated in humoral immunity , in the formation of melanotic capsules [61,62], in cellular capsule formation [63,64], and in recognition of foreign materials [65,66]. Severalreviews [67-691 discuss the humoral phenoloxidases while other reviews  discuss the cuticular Po's, and the differences and similarities between the two PO systems have also been critically reviewed . Seybold et al.  identified a number of components in the production of Po's leading them to propose that a cascade of reactions was involved. This cascade was considered analogous to the mammalian coagulation-fibrinolytic-complement system . A prophenoloxidase-activating enzyme that appears to be a serine proteinase has been isolated 173-751. A PPO-activating enzyme has also been proposed , but the function of the resulting peptide  is yet unknown. Although a number of factors activate PPO in vitro, what triggers the system and its control in vivo is not clear. Both P-1,3-glucans and lipopolysaccharides appear to activate the system , possibly through an intermediary such as a serine protease . Heat can also activate the PO cascade in a different manner and appears to operate at the latter step of the cascade . One result of the cascade is the production of melanin [SO]. The existence of cell-free or humoral melanin encapsulation has been confirmed [81,82] and is characterized by a low electron-dense deposit over the foreign surface followed within hours by the occurrence of high election-dense granules within the homogenous layer. Gotz and Boman  concluded that humoral encapsulation primarily occurs in insects (such as certain dipteran genera) that have few circulating hemocytes. The melanin capsule represents a protein-polyphenol complex produced by the action of phenoloxidases . The importance of this system is due to its implicated role as an opsonin 8 Vinson , a plasma molecule involved in recognition and preparation of a foreign object for attachment of phagocytic cells, but the situation is not clear. Ratcliffe and Gagen  reported that granulocytes release a factor upon contact with foreign material that attracts plasmatocytes entangling them at the localized clot. Ratner and Vinson  reported that a encapsulation-promoting factor is released from hemocytes of Heliothis, which is a small peptide . Whether this protein is part of one of the sticky proteins generated by PPO activation or comes from some other source is of interest because one factor released upon PPO activation is a peptide . The involvement of PO’S in the cellular encapsulation of parasitoids has been implicated [63,64] by using phenylthiourea, an inhibitor of the phenoloxidases. In each case, more parasitoids survived or encapsulation was more impaired in PTU-injected hosts than controls. While it is increasingly clear that the PPO system is involved in the immune response, the mechanisms that trigger and regulate the cascade of changes and their specific role in the immune process are unknown. Cellular. The cellular immune response (Table 1)involves three similar processes that differ primarily in the size and numbers of foreign material encountered. Phyocytosis involves the recognition, attachment, and internalization of small foreign material [2-31. Nodule formation involves the agglutination of small particles which are then encapsulated . Encapsulation (and in some cases nodule formation) is a common response of host insects to invading foreign organisms (bacteria, fungi, protozoa, parasitoid eggs, or larvae), as well as inert materials (glass, Sephadexm, cotton threads, or thorns) which are enclosed by several layers of hemocytes. Most capsules became several layers thick with the inner most cells being very flattened and interconnected  while the outer cells are more rounded and may reenter circulation . Capsule thickness varies depending on the nature of the encapsulated surface . The inner layers of the capsule around living organisms often melanize  although this is not always the case , and melanization is less common when inert materials are encapsulated . Understanding encapsulation depends on understanding the functions of the various types of hemocytes involved; however, confusion exists. Confusion arises from three major problems in hemocyte identification. First, classification is largely dependent on a physical description of the different cell types , which is influenced by different methods of collection and preparation for observation [3,94]. Second, there is a lack of understanding of the functions of the various cell types and intermediate cell forms [3,6,95]. A third problem derives from the diversity of insect species and attempts to classify the cells of Lepidoptera, for example, consistent with those effects of Diptera [3-5,94,95]. While confusion remains, the more commonly recognized forms of hemocytes types are provided in Table 2. The encapsulation process has been variously described, but based on current concepts (Table 3) the process can be described as follows. Foreign material is randomly contacted by hemocytes  although others argue that the foreign object is attractive . If it is a granular hemocyte that contacts the foreign object, it recognizes the object as foreign and degranulates [98,99]. The recognition of the foreign body must occur at the cell membrane but the mech- ParasitoidHost Immune Resistance 9 TABLE 2. Major Types of Insect Hernocytes* Prohemocytes (Pr.tsmal1, rounded cells with a high nuclear-cytoplasmic ratio; weak rough endoplasmic reticulum (ER) Plasmatocytes (P1)-spindle or flattened cells, free ribosomes, and well-developed rough ER; pseudopodia sometimes present Oenocytoids (0e)-large cells with a low nuclear-cytoplasmicratio, eccentric nucleus, poorly developed organules, but many free ribosomes; sometimes crystals or fibers are present, ”crystal cells” of Diptera Spherule cells (Sp)-large cells with numerous inclusions, irregular in shape, well-developed rough ER Thrombocytoids (Th)-irregular shaped cells with plasma membrane invaginations, found in Diptera Granular hemocytes (Grtdiverse group of medium-sized, rounded cells containing membrane-bound electron-dense microtubular or heterogenous bodies that increase near pupation; includes coagulocytes, phagocytes, and spherule cells ‘Adapted from references [2,5,87]. anism is not clear. Cell-bound receptor molecules, agglutinins, components of the phenyloxidase system, and differences in electrical changes are all possible factors [3-6]. The attached granular hemocyte degenerates and releases factors assumed to attract plasmatocytes [3,90]. The degenerating granular hemocyte also is presumed to release factors that coat the foreign object that allows the plasmatocyte to attach [loo]. The plasmatocytes attach and flatten out accompanied by the formation of desmosomes, microtubules, and microfilaments between neighboring cells that probably contribute to the growing layer of plasmatocytes that make up the capsule . CIRCUMVENTING THE HOST DEFENSE SYSTEM While insects have a complex and effective defensive system against pathogens, parasites, and parasitoids, these organisms have also evolved ways to evade or circumvent the system. As noted by Bayne [loll, while the resistant mechanisms in immunoparasitology are of interest, the susceptible condition is of equal or greater interest. Host susceptibility implies the provision of a suitable environment (the host) and the ability of the parasite (parasitoid) to evade or suppress the host’s defensive immune responses. In order to be successful parasitic forms must not only effectively deal with the host’s immune system, but having done so, must either be in a suitable environment or modify that environment [102,103]. TABLE 3. Theory of Encapsulation* Stage 1. Stage 2. Stage 3. Stage 4. Stage 5. Stage 6. Stage 7. Stage 8. Stage 9. Foreigh body (FB) randomly contacted by a granulocyte (Gr) Gr recognizes FB Gr degranulates and material sticks to FB Additional Gr attach to FB Gr lyses releasing a recognition factor (RF) RF attracts plasmatocytes (1%) PISattach to FB & RF complex Pls spread over FB surface Pls form cell to cell contract via desmosomes and microtubules *Adapted from references [2-41. 10 Vinson The location of potential host insects by parasitoids involves odors, sight, or sound , the parasitoids often utilizing externally released chemicals (pheromones or defensive secretions) that are important to the biology of the host [lo,1051. The parasitoids are either insensitive to the defensive secretions or avoid coming into contact with such compounds. However, the allelochemical and behavioral interactions between parasitoids and their hosts are beyond the scope of this overview. Once the host (or suitable oviposition site) has been located, the parasitoid must overcome the cuticular barrier. The parasitic Diptera have evolved to deal with the cuticular barrier in two general ways. One is to oviposit micro-eggs that the host insect consumes, the egg hatching and the larvae burrowing into the gut wall ; or secondly, the first-instar larvae burrows through the cuticle [107,108]. In a few tachinids the ovipositor is modified to allow it to tear open the cuticle where eggs are deposited . In the parasitic Hymenoptera the evolution of the sting not only may have allowed the Hymenoptera to develop sociality , but may have allowed them to radiate through Insecta by allowing them to break the cuticular barrier to either lay their eggs inside the host (endoparasitoids) or to inject factors that permit the eggs to develop externally (ectoparasitoids). Salt [ 1111examined the various resistance mechanisms of insect parasitoids to the defense reactions of their hosts. He divided these mechanisms into six subcategories (Table 4). Many strides have been made since his review of the problem, which stimulated much of the research. For this overview, I have divided the immune resistance mechanisms into five subcategories (Table 5). Avoidance Many parasitoids simply avoid the immune system of their host. An example includes parasitoids that attack insect eggs which do not appear capable of mounting an immune response [lll].Insect eggs appear to rely on protection from oophages through their concealment or protected placement [1121. TABLE 4. The Resistance of Insect Parasitoids to the Defense Reactions of Their Host as Presented by Salt [1111 I. Resistance due to a protective coating a. Coating an egg b. Coating a larvae 11. Resistance by host attrition a. Rapid development and feeding by host b. By teratocytes c. By pseudogerms d. By gregarious habit 111. Resistance by organ occupation IV. Resistance by an enveloping membrane a. Parasitoid embryonic membrane b. Host derived membrane V. Resistance due to the stage of host attacked a. Insect eggs b. Young larvae VI. Resistance by the activity of parasitoid a. By a parasitoid secretion b. By physical repulsion of defense reaction ParasitoidHost Immune Resistance 11 TABLE 5. Ways in Which Parasitoids May Handle the Insect Immune System 1. Avoidance a. Ectoparasitoids b. Egg parasitoids c. Development within host tissues 2.Evasion a. Molecular mimicry b. Cloaking (Stealth) c. Rapid developmentin host d. Target proliferation 3. Destruction a. Blockage of the immune system b. Attrition c. Destruction of responding cells 4. Supression a. Interfere with recognition b. Interfere with response 5.Subversion a. Develop despite host response b. Development aided by host response Developing externally is another way to avoid the host’s internal immune system. However, the ectoparasitoid Hymenoptera may be exposed to some aspects of the host’s internal immune system. Larvae generally feed through either a wound made orally in the cuticle or through an ovipositional puncture. While the mechanical action of the mouth may help keep the wound open, it is likely either that the ovipositing female injects factors at the time of oviposition or the developing larvae secrete factors that prevent hemolymph coagulation. However, parasitoid-derivedanticoagulants have not been described, although acetic and formic acids have anticoagulant activity  and are a common component of various insect defensive secretions IS]. A third method of avoidance, applicable to endoparasitoids, is the placement of the egg by the parasitoid in select tissues where the egg hatches to develop out of reach of the immunocompetent hemolymph system [114,115]. For example, Klomp and Teerink  reported that two parasitoid diptera and one ichneumonid, all parasitic on the pine looper Bupulus piniurius, develop between the cuticular intima or peritrophic membrane and the epithelium of the digestive system, thus avoiding the immune system. Another example, provided by Silvestri , is where the eggs of Plufygustes dryomyiue deposited in host ganglia develop, but are rapidly encapsulated when placed in the host body cavity. Other multicellular parasites are also known to enter and develop in host tissues, presumably to escape the immune system [118-1221. Evasion Another way to deal with the immune system is to evade the recognition system. Parasitoids could evade their host’s immune recognition system by evolving the same surface characteristics as found in the host, molecular mimicry . Another approach is to evolve a surface that is different than the host, but fails to elicit a response, being hidden (cloaking or stealth) from the host‘s immune recognition system. Without understanding the insect recognition system or having identified the components involved, it is difficult to 12 Vinson separate molecular mimicry or cloaking (stealth) from a blockage of the recognition system. In all three cases no evidence of a response would be evident. However, there is increasing evidence that some parasitoids fail to elicit an immune response. Eggs of the endoparasitoid Curdiochiles nigriceps are encapsulated in Heliothis zeu (Lepidoptera Noctuidae) but not in H. virescens . The eggs of this parasitoid are coated with a 0.5-1.0 pm-thick fibrous material which is rapidly removed (within 2 h) in H. tea but persists for 12 to 24 h in H. virescens . Evidence was provided  to suggest that the hemolymph of H. zeu may contain enzymes or provide conditions that strip the egg’s outer layer in preparation for encapsulation. Eggs stripped of the fibrous layer in H. zed hemolymph are readily encapsulated when injected into H . virescens . Davies and Vinson , using an in vitro encapsulation system which encapsulates many biotic and abiotic targets with the exception of allogenic tissue, were unable to obtain the encapsulation of mature fibrous-layer-coated C. nigriceps eggs whether alive or killed by ultraviolet radiation. In contrast, mature eggs removed with the follicle cells covering the fibrous layer or eggs treated with driselase to remove the fibrous layer were readily encapsulated by using the in vitro system. Similarly, modification of the fibrous layer by exposure to fibrous layer antibodies promoted encapsulation in vivo I1281 as did driselasetreated or follicle-cell-coveredeggs . The nature of the fibrous layer was examined  by using histochemical techniques. These studies revealed the absence of acidic mucoprotein or glycosaminoglycanswhich were expected since negative charged particles usually only elicit a weak encapsulation response [130,131]. Further, the fibrous layers of the braconid Cofesiu (Apunteles)glomerutus  and the ichneumonid Venturiu cunescens  have histochemical properties of an acidic mucoprotein. The fibrous layer histochemical staining of C. nigriceps was consistent with the characteristics of a neutral glyco- or mucoprotein . The egg chorions of insects reflect a wide range of complexity and often serve as protection against desiccation, predation, and temperature extremes and at the same time do not hinder gaseous exchange or larval eclosion . However, the eggs of endoparasitoids are placed in a nutrient-rich, stable environment and often lack their own yolk; they depend on the host hemolymph for nutrients and possess thin hydropic chorions . Roles for the chorion of parasitoids include faciliation of oviposition  and attachment to host tissues . An additional role for the chorion is the evasion of encapsulation [127-1291. The egg chorion of C. nigriceps bares similarities to other larval endoparasitoids such as the braconid C. glomerutus and Microplitis mediutor and the ichneumonid Cumpoletis sonorensis  and V. canescens . However, the chorion of the eggs of the egg parasitoids Telenomzis heliothidis and Trichogrummu pretosum (Strand, unpublished) and the pupal parasitoid Nusoniu vitripennis lack a fibrous layer. A second form of evasion appears to be a form of molecular mimicry, the study of which began with Salt  working with Venturiu ( = Nemeritus) cunescens. He reported that parasitoid eggs acquired a property that prevented their encapsulation as they passed through the genital tract. The source of the responsible factor was traced to the calyx region of the reproductive system Parasitoid Host Immune Resistance 13 , which was shown  to contain oblong membrane bound particles about 1,300 A across. These particles provide a particulate coat over the eggs , which led Salt  to suggest that the particles either blocked host recognition or suppressed the response. The particles were reported to consist of a mucoprotein .However, the discovery of DNA-containing particles in other parasitoids [145,146] led several researchers to reinvestigate these particles. Although it has been suggested that Vesturia particles contain linear DNA , these results have not been confirmed . Because of the similarity of the occurrence and assembly in the nuclei of calyx epithelial cells , the V. canescem particles are being referred to as virus-like particle. The V. canescens VLP's are reported to consist of four proteins (a 35, 52, 60, and a minor protein band of 80 kD) which cross-reacted with particle-specific antibodies. The 52, 60, and 80 kD VLP-specific antibodies were found to also cross-react with a 42-kD protein (P-42)from the fat body of unparasitized Ephestia . The P-42 protein occurs in the basal lamina of fat-body cells and in hemocytes of the host , suggesting that the parasitoid may evade recognition through molecular mimicry. However Berg et al.  found that the titer of P-42 proteins in hosts exposed to VLP's increased. This indicates that the host has recognized the invasion and the VLP's may act by interfering with either the recognition system or the responding system. Further, the P-42 protein is reported similar [ 1501 to the P-4 (48-kD proteins) induced by bacterial infection in Hyalophoru cercopin [1521. A third evasive technique is to develop before the host's immune system can respond. One of the best-described examples is the ichneumonid Phalogenes nigridens, which completes its first three larval stages within 1day . However, this approach appears to be uncommon. Another evasive technique is to provide a large number of targets that dilute the host's immune system. Salt  suggested that teratocytes (cells of the embryonic membrane of the developing parasitoid) provide so many targets that the immune system is unable to focus an effective attack. The same concept applies to polyembryonic species [111,255]. Although some hosts appear to be less effectivein encapsulating multiply parasitized hosts 1156,1571, there is no good evidence that target proliferation is effective. When a few (five or six) teratocytes are injected into hosts they are not encapsulated [1581and when five or six parasitoids occur within a host many are killed and encapsulated . The injection of aggregates of material such as India ink or fungal spores  results in the presence of thousands of targets which elicit an immune response in the form of nodules. Similarly, a number of injected neutral Sephadex" beads are also encapsulated [130,131]. These data suggest that the target proliferation concept is probably not a viable one. Destruction Destruction of the host immune system or even blockage of either the immune recognition system or blockage of the biochemical pathways that allow the system to function could have serious consequences of the parasitoid which depends on the host's health for survival . Although there is no evidence that the host's immune system is completely blocked, such blockage would 14 Vinson be possible if the parasitoid evolved a means of protecting its food supply after such a blockage by the secretion of toxins against such other invading organisms. The existence of such toxins has received little study but the idea holds promise. Antibacterial and antifungal agents have been described from adult and larval parasitoids [161,162]. Destruction can also refer to the overall nonspedc impairment of the immune system such as might be expected through attrition. The attrition or removal of the energy needed to mount an immune response was suggested by Salt [40,163]. Of these, teratocytes have been impliciated in having a role in weakening the immune system by attrition . Teratocytes are cells of the embryonic membrane of certain endoparasitoid hymenopteran eggs , primarily braconids and scelionids. Usually a specific number of cells are released which rapidly grow, often reaching several hundred micrometers in diameter. Many functions have been ascribed to teratocytes which range from serving as food to regulating the host‘s physiology [see 1031. Recent evidence indicates that teratocytes can be secretory [ 1641 and may have a feedback effect on the growth of the parasitoid [165,166]. The suggestion that teratocytes might block the immune system through the attrition of host resources needed to mount a defense reaction was proposed [ill] and later elaborated on by Salt .The idea was extended to pseudogerms (cells from the paranucleus ”polar body”) that are similar to teratocytes [111,167] and to gregarious species [lll]. However, present evidence, like the multiple target concept, argues against the concept of attrition of resources since the injection of a few teratocytes does not result in their encapsulation , and when a number of solitary endoparasitoids occur in a host all but one are killed and encapsulated . With the attrition of important components of the immune system or general weakening of the hosts’ defenses aside, teratocytes do appear to play a defensive role as suggested by Kitano  and others [lll].One suggestion includes evidence that the teratocytes secrete a fungicide . However, most authors have suggested that teratocytes interfere with the immune response. For example, the encapsulation of first-instar C. nigriceps larvae  was reduced by injections of either calyx fluid or teratocytes. Tanaka and Wag0  report that the young (4 day-old) teratocytes of Apunteles kuriyui synergize the effects of both calyx fluid and venom in reducing the encapsulation of larvae, although the calyx fluid and venom also had encapsulation-reducing effects . Kitano  and Wag0 and Kitano  reported that venom and the egg’s surface material acted synergistically to reduce encapsulation of eggs in the gregarious Apunteles glornerutus-host system. Further, both calyx fluid and venom appeared to be needed to prevent the encapsulation of newly hatched larvae when only a few eggs were present. Both calyx fluid and venom were not effective in reducing the encapsulation of parasitoid larvae 7 days after oviposition  and these authors suggest older teratocytes may be involved. Both Kitano et al.  and Tanaka and Wag0  report that only older teratocytes contained a phenoloxidase inhibitor, but the role of a phenoloxidase inhibitor in immunity is not clear. Whether the antiphenoloxidaseactivity is related to the antifungal activity reported from the teratocytes of A . glorneratus [169,176,177] is unknown. Although the question as to if or how teratocytes provide immune protec- Parasitoid Host Immune Resistance 15 tion remains unanswered, the question as to haw teratocytes themselves escape the response is also unknown. One aspect that is often commented on concerning teratocytes is the extensive microvillar surface (see ). Ubelaker et al. I1781 working with the metacestode of Hymenolepis diminutu located in the hemocoel of Tenebrio suggested that numerous surface microvilli of the metocestode lyse the hemocytes that contact it, thus providing protection. Lackie [1791, working with a resistant and susceptible orthropteran, interpreted the presence of debris at the metacestode surface as incidental or excretory products, but she  later suggested the debris was due to occasional lysis of granulocytes contacting an otherwise foreign surface that fails to elicit a host response. It is possible that teratocytes similarly destroy responding hemocytes, depleting their number, but no such evidence exists. Richards and Arme  suggest that some of the metacestode microvilli are impaired, and it is these impaired micovilli that are phagocytized by plasmatocytes resulting in the debris. However, this issue is not resolved. Suppression In contrast to the destruction or blockage of the immune systems, parasitoids appear to suppress the system in more specific ways. For example, when parasitized insects are colonized by other foreign material they specifically respond , and when competitors are attached, the losers, whether conspecific or not, are encapsulated [28,159]. These results suggest that if parasitoids are actively affecting the host’s immune system, the effect is more specific than general destruction. How parasitoids accomplish the more specific suppression of the immune response is beginning to emerge. In the case of some pathogenic bacteria, such as Bacillus tkuringrensis, an immune inhibitor is released that appears to destroy the cercopins [183,184]. A similar immune inhibitor that destroys the cercopins is released by one of the entomophilic nematodes, NeopEectuna curpocupsue, which protects the cercopin-sensitive bacterium Xenarhbdus nernutophilus which is symbiotic with the nematode . If the prophenoloxidase cascade is involved in the immune response then successful parasitoids might be expected to suppress this system. Brewer and Vinson , using the PO inhibitor PTU, reported reduced encapsulation of Curdiockiles nigriceps eggs. Both Salt  and Nappi  reported more surviving parasitoids emerging from PTU-contaminated hosts. These studies have been further supported by Stoltz and Cook , who reported that the polydnavirus (associated with certain parasitoids) could inhibit the activation or activity of the phenoloxidase although the enzyme was present. Although inhibition of phenoloxidase activity may be important in evading the immune system, the evidence is not convincing. Sroka and Vinson  could not detect any early changes in phenoloxidase activity after parasitism with three different species although a decrease in melanin production occurred in the host later in the parasitoid’s development. These authors also noted that phenoloxidase-related changes often occurred several days after the vulnerable period of the parasitoid, several days after egg hatch. Also, both Tanaka and Wag0  and Kitano et al.  report phenoloxidase inhibition by teratocytes late in the parasitoids development. These changes in phenol- 16 Vinson oxidase would appear to serve some other function than suppression of the immune response. With several parasitoid-host systems the parasitoid appears to interfere with plasmatocytes. These studies include three different lepidopteran host systems and one dipteran host system involving Drosophila. A significant amount of research has been conducted concerning the immune system of Drosophila and the mechanisms used by several parasitic cynipids to deal with the system. This effort has been conducted by several active groups and several recent reviews are available [187-1911. These studies have been augmented through the use of several melanotic tumor mutant Drosophila strains  which showed that host tissues covered with a basement membrane fail to elicit a tumor immune response [191,193].Observationsalso demonstrated that plasmatocytes were transformed into lamellocytes which increased in the hemolymph, while crystal cells decreased in response to: foreign parasitoids [194-1971, tumors [191,193-1991, and basement membrane lacking allographs . These studies provide a background for interpreting the results of studies with the successful parasitoid Leptaphilina heterotoma = Pusedocoila bochei), a cynipid. Walker reported fewer lamellocytes in parasitized Drosophila larvae and she suggested that the wasp egg interfered with lamellocyte differentiation. Cross-protection studies  demonstrated that L. heterotoma provided protection for another Drosophilla parasitoid normally encapsulated. The results suggested that either the female injected a substance or an egg released a factor that suppressed encapsulation. The observations of Walker were confirmed and extended to include several other; Drosophila species . The Rizkis reexamined the Drosophila-L. heterotoma system and observed that lamellocytes in unparasitized host larvae were discoidal and readily adhere to each other while lamellocytes of parasitized hosts shed some of their cytoplasm, were elongate, and lost their adhesiveness. The responsible parasitoid factor, present in the accessory (poison) gland of L. heterotoma, was referred to as "lamellolysin" . Rizki and Rizki speculate that lamellolysin may affectmicrotubule formation. A second system involves the ichneumonid Pimpla turionellae L., a pupal parasitoid attacking a variety of lepidoptera . The reproductive system of the female, in addition to the ovary, consists of a poison gland, a Dufour's gland, and uterus gland, each of which Osman and Fuhrer  examined histochemically. They reported that the uterus (oviduct) gland contained an acid mucopolysaccharide and a lipoprotein, the poison gland contained a natural mucopolysaccharide or mucroprotein, while Dufour's gland contained both a cholesterol ester and a lecithin-likephospholipid .All three glands reduced the ability of hemocytes to form pseudopodia . Osman  found that when the secretions were applied to nylon thread, the threads were not encapsulated, and that the three secretions together were most effective. The Pimpla secretions did not affect the hemocytes of Gelpinia hercyniae , a Diprionidae (Hymenoptera). It is somewhat distressing that all three Pimpla glands, each containing different compounds, inhibit hemocytes because the results suggest hemocytes are sensitive to a wide range of compounds, making the job of determining the significant ones more difficult. The last two systems include parasitoid species that harbor DNA-containing Parasitoid Host Immune Resistance 17 polydnaviruses  which were first discoverd in Curdiochiles nigriceps . These viruses were first referred to as “viral-like particles” and appeared similar to particles from the oviducts of an ichneumonid V. canescens (described earlier) that are involved in the evasion of encapsulation [141,142]. Particles were also reported from parasitoid reproductive systems and host tissues of other species [145,210-2121. Since that time many functionshave been described forpolydnavimses [145,213,214].Here I will concentrate on the immune system. The calyx fluid (fluid in the calyx or lateral oviducts) had been shown by Salt  and Vinson  to be involved in the parasitoid‘s defense against the immune system. Working with an ichneumonid, Campoletis sonorensis, Edson et al.  demonstrated that the activity was due to a virus (polydnavirus) which was capable of protecting the eggs of C. sonorensis from encapsulation. In several braconids a similar situation exists except that both venom and polydnavirus are necessary to inhibit encapsulation [216-2181, the venom appearing to be necessary for the virus to enter host cells . The calyx fluid or viruses appear to have the ability to cross-protect [220-2221. How these polydnaviruses suppress the host’s immune system is not yet understood. The polydnaviruses of both the ichneumonids and braconids enter various host cells [145,223]where they are expressed [224,225] but do to replicate . In each case studied the polydnavirus presence in the host results in abnormalities (reduced spreading) in the plasmatocytes [227-2301 resembling similar abnormalities reported by Osman  and Rizki and Rizki  for parasitoids that do not appear to have polydnaviruses. Davies and Vinson  determined that a factor in the hemolymph, rather than direct viral infection, appeared to be responsible for the reduced spreading of plasmatocytes although Guzo and Stoltz  reported that the polydnavirus of Cotesia rnelanoscela induces morphological changes in a polydnavirus-exposed insect tissue culture line. In the tussock moth, Orgziu Iencostigma, the prohemocytes were considered the target of the polydnavirus from the braconid Cotesia melanoscelu . As with other braconids, both virus and venom glands were necessary to obtain the effect and while both encapsulations and nodule formation were suppressed, phagocytosis was not . In Heliothis virescens the polydnavirus of C. sonorensis does not alter the prohemocytes but reduces the number of plasmatocytes and inhibits the spreading ability of those remaining . In Spodoptera frugipeidu the CsV is less effective in reducing plasmatocyte spreading so that 32% of the eggs of C. sonorensis are encapsulated . In hosts where the eggs hatch, and the parasitoid develops, the spreading ability of the plasmatocytes was inhibited 12321. There are other differences yet to be understood concerning the immune response of species having the polydnavirus. For example, Tanaka  reported that both calyx fluid and teratocytes are necessary to protect the eggs and larvae of Microplites mediator from encapsulation, and Apanteles kariyai utilize the calyx fluid, venom, and teratocytes . Further, Kitano  reports that the action of the venom is on the egg surface. It may well be that several processes are involved. With C. nigriceps the egg appears to be protected by a fibrous layer that does not evoke an immune response [127,129]. The fibrous layer appears to be slowly destroyed, and if 18 Vinson lost, the egg’s protection is lost [93,125-127,1291. However, in persistent hosts, such as H. zirescens, the polydnavirus with venom suppresses the plasmatocytes ability to attack and spread (Tanaka and Vinson, unpublished data), thus providing protection to eggs where the other fibrous layer has begun to disappear and to the larvae as they hatch. However, how long the polydnavirus is able to persist and exert an effect is not known. Since the virus does not appear to replicate  and we may speculate that the polydnaviruses influence may weaken with time, although some polydnavirus effects may be dose independent . If the influence of the virus decreases with time, it would be advantageous for the developing parasitoid (or teratocytes) to release factors that insure the continued suppression of the immune response [170,171,175,187]. In addition, it may be advantageous for larvae (directly or via teratocytes) to release substances that reduce the activity of phathogens [161,162,168,177] to which the immune-impaired hosts may be more susceptible . SUBVERSION Many parastioid Diptera, particularly the Tachinidae, enter the host hemocoel but either maintain or develop an association with the outside by a perforation of the integument of the host. This association is maintained by a respiratory funnel and sheath which develops around the parasitoid larvae. Unfortunately studies of the origin of the components of the respiratory funnel and sheath have not been undertaken and the older literature summarized by Salt  has not dramatically changed. 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