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How parasitoids deal with the immune system of their hostAn overview.

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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.
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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 [7] 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 [12] 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 [13]. In some cases these secretions are antimicrobial. For example, the imported fire ant, Solenopsis invictu, releases several antimicrobial
dialkylpiperidines [14].
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 [22].
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 [23].
The released hemolymph often contains compounds that also have repellent
properties [24], but in other cases the hemolymph works by rapidly coagulating, entanghng the predator [25] 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 [26], has been reported in a few lepidoptera [27] 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 [26]
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 [28]. 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 [29], 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
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Vinson
cuticular encystment. Metalnikov [30] 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 [30] 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 [31]. 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 [32]. 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 [33]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
[34] 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 [35],Brehelin [36]
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 [38] while the cellular coagulogen may involve a disulphide-linked
protein [39]. It has been suggested that hemocytes involved in coagulation and
wound repair respond to an injury factor [40]. The purification of an injury
factor has been reported [41], 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 [42] and Stephens [43], have been isolated
and characterized as a group of proteins, the cercopins (about 4,000 kD") and
the larger actins [44]. 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 [46]
*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 [49]. The peptidoglycan acts as an inducer of
the antibacterial protein [50].
The lectins (hemaglutinins) have long been known in both plants and animals and Bernheimer [51] demonstrated their presence in a number of lepidoptera. Most of the purified insect lecints have galactose specificity [5].
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 [54]. Lectins may play a role in hemocyte recognition
and removal of foreign material [55] 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 [57]. More
recently, Anderson and Chain [58] 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 [59] 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 [58].
The prophenoloxidase-phenoloxidasesystem in insects has been implicated
in humoral immunity [60], 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
[70] discuss the cuticular Po's, and the differences and similarities between
the two PO systems have also been critically reviewed [71]. Seybold et al. [72]
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 [72]. A prophenoloxidase-activating enzyme that appears to be a serine
proteinase has been isolated 173-751. A PPO-activating enzyme has also been
proposed [76], but the function of the resulting peptide [70] 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 [77], possibly through an intermediary such as a
serine protease [78]. Heat can also activate the PO cascade in a different manner and appears to operate at the latter step of the cascade [79]. 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 [4] 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 [83].
The importance of this system is due to its implicated role as an opsonin
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Vinson
[84], 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 [85] reported that granulocytes release a factor upon contact with
foreign material that attracts plasmatocytes entangling them at the localized
clot. Ratner and Vinson [86] reported that a encapsulation-promoting factor
is released from hemocytes of Heliothis, which is a small peptide [87]. Whether
this protein is part of one of the sticky proteins generated by PPO activation
[88]or comes from some other source is of interest because one factor released
upon PPO activation is a peptide [74].
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 [89]. 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 [90]
while the outer cells are more rounded and may reenter circulation [91]. Capsule thickness varies depending on the nature of the encapsulated surface [92].
The inner layers of the capsule around living organisms often melanize [4]
although this is not always the case [93], and melanization is less common
when inert materials are encapsulated [4].
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 [89], 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 [96] although others argue that the
foreign object is attractive [97]. 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 [96].
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.
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Vinson
The location of potential host insects by parasitoids involves odors, sight,
or sound [104], 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 [106]; 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 [109].
In the parasitic Hymenoptera the evolution of the sting not only may have
allowed the Hymenoptera to develop sociality [110], 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 [113]
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 [116] 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 [117], 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 [123]. 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 [124]. 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 [125].
Evidence was provided [126] 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 [93]. Davies
and Vinson [127], using an in vitro encapsulation system [86]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 [129].
The nature of the fibrous layer was examined [129] 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 [132] and the ichneumonid
Venturiu cunescens [133] 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 [129].
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 [112].
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 [134]. Roles for the chorion
of parasitoids include faciliation of oviposition [135] and attachment to host
tissues [132]. 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 [136]and Microplitis mediutor [137]and the ichneumonid Cumpoletis sonorensis [138] and V. canescens [139].
However, the chorion of the eggs of the egg parasitoids Telenomzis heliothidis
and Trichogrummu pretosum (Strand, unpublished) and the pupal parasitoid
Nusoniu vitripennis [135]lack a fibrous layer.
A second form of evasion appears to be a form of molecular mimicry, the
study of which began with Salt [140] 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
[141], which was shown [142] to contain oblong membrane bound particles
about 1,300 A across. These particles provide a particulate coat over the eggs
[133], which led Salt [143] to suggest that the particles either blocked host recognition or suppressed the response.
The particles were reported to consist of a mucoprotein [144].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 [147], these results have not
been confirmed [148]. Because of the similarity of the occurrence and assembly in the nuclei of calyx epithelial cells [149], 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
[150]. The P-42 protein occurs in the basal lamina of fat-body cells and in hemocytes of the host [150], suggesting that the parasitoid may evade recognition
through molecular mimicry. However Berg et al. [151] 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 [153]. 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 [154] 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
[159]. The injection of aggregates of material such as India ink or fungal spores
[160] 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 [15]. 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 [163]. Teratocytes are cells of the embryonic membrane of certain endoparasitoid hymenopteran eggs [103], 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 [163].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 [158], and when a number of solitary endoparasitoids occur in a host all but one are killed and encapsulated [159].
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 [168] and others [lll].One suggestion
includes evidence that the teratocytes secrete a fungicide [169]. However, most
authors have suggested that teratocytes interfere with the immune response.
For example, the encapsulation of first-instar C. nigriceps larvae [170] was
reduced by injections of either calyx fluid or teratocytes. Tanaka and Wag0
[171] 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 [172]. Kitano [173] and Wag0 and Kitano [174] 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 [175] and these authors suggest older teratocytes may be
involved. Both Kitano et al. [175] and Tanaka and Wag0 [171] 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 [94]). 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 [180] 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 [181] 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
[182], 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 [185].
If the prophenoloxidase cascade is involved in the immune response then
successful parasitoids might be expected to suppress this system. Brewer and
Vinson [63], using the PO inhibitor PTU, reported reduced encapsulation of
Curdiockiles nigriceps eggs. Both Salt [186] and Nappi [64] reported more surviving parasitoids emerging from PTU-contaminated hosts. These studies have
been further supported by Stoltz and Cook [187], 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 [188] 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 [171] and Kitano et al. [175] 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 [192] 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 [200].
These studies provide a background for interpreting the results of studies
with the successful parasitoid Leptaphilina heterotoma = Pusedocoila bochei), a
cynipid. Walker [201]reported fewer lamellocytes in parasitized Drosophila larvae and she suggested that the wasp egg interfered with lamellocyte differentiation. Cross-protection studies [202] 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 [201]were confirmed and extended to include several other; Drosophila species [203].
The Rizkis [204]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" [204]. Rizki and Rizki [190]speculate that lamellolysin may
affectmicrotubule formation.
A second system involves the ichneumonid Pimpla turionellae L., a pupal
parasitoid attacking a variety of lepidoptera [205]. 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 [206] 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 [206].All three glands reduced
the ability of hemocytes to form pseudopodia [207]. Osman [208] 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 [208], 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 [209] which were first discoverd in Curdiochiles nigriceps [146].
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 [143] and Vinson [170] to be involved in the parasitoid‘s defense against
the immune system. Working with an ichneumonid, Campoletis sonorensis, Edson
et al. [215] 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 [219]. 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 [226]. 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 [207] and Rizki and Rizki [204]
for parasitoids that do not appear to have polydnaviruses. Davies and Vinson
[228] 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 [231] 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 [231]. 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 [231]. 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 [228]. In
Spodoptera frugipeidu the CsV is less effective in reducing plasmatocyte spreading so that 32% of the eggs of C. sonorensis are encapsulated [232]. 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 [233] 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 [171]. Further, Kitano [234] 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 [226] and we may speculate that the polydnaviruses influence may
weaken with time, although some polydnavirus effects may be dose independent [235]. 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 [15].
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 [236]
has not dramatically changed. The respiratory sheath appears to arise from
the hemocytes in a process similar to wound healing [237-2391. This concept
was supported by Beard [240], who reported that a respiratory sheath did not
form around the maggots of the tachinid genuss Trichupuda when developing
in the bug Anasa tristis, a host species which fails to encapsulate foreign objects
inserted into its hemocoel. Also as noted by Strichland [241], a parasitoid may
be overcome in the respiratory sheath if for some reason the parasitoid is killed
or fails to feed and keep active. The available data indicates that the encapsulation process proceeds but the parasitoid’s connection to an oxygen source
prevents its death and the parasitoid is able, with its mandibular hooks, to
keep one end open to feed.
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