Evasion of the insect immune response by Moniliformis dubius (Acanthocephala): further observations on the origin of the envelope

The envelope around larvae of Moniliformis dubius appears to protect the parasite against immune recognition and encapsulation by the insect host's haemocytes. The origin of this envelope has been the subject of controversy although most evidence suggests it is parasite-derived. If host-derived, the envelope would be expected to share surface properties with host tissue. Thus, experiments were undertaken, transplanting parasites and host tissue to other insects and using haemocytic encapsulation as an assay for immune recognition, in order to compare the response to host tissue and to the parasite's envelope. Parasites without their envelopes, and pieces of tissue (ventral nerve cord) from the experimental host (the locust Schistocerca gregaria) were recognized as foreign and encapsulated in the cockroach, Periplaneta americana. The majority of parasites with their envelopes were unencapsulated or only partially encapsulated on transfer to their normal host, P. americana, indicating that the envelope does not have surface similarity to locust tissue. Cockroach-derived parasites with or without envelopes were not encapsulated in S. gregaria, suggesting that the larva itself can evade or inhibit the locust's recognition mechanism. However, since larvae which develop in S. gregaria are enclosed in an envelope, the formation of the envelope would seem to be an inherent feature of the parasite's development.     

Heterotylenchus antumnalis. Hemocytic reactions and capsule formation in the host, Musca domestica

Failure of the nematode H. autumnalis to develop in M. domestica is attributed to the defense reaction of host larvae to the infective, gamogenetic stage of the parasite. The defense reaction involves melanization and encapsulation of the parasite, and is manifested as changes in the hemocyte picture of the host.     

Changes in differential haemocyte count and in vitro behaviour of plasmatocytes from host Heliothis virescens caused by Campoletis sonorensis polydnavirus

Campoletis sonorensis is a habitual parasitoid of 3rd-instar larvae of Heliothis virescens. C. sonorensis eggs and small glass rods were encapsulated in 5th-instar host larvae implanted in the absence of wasp calyx fluid; prior injection of calyx fluid into larvae suppressed the encapsulation response. Within 8 h of calyx fluid injection there was a removal of approx. 75% of the circulating capsule-forming haemocytes (plasmatocytes). The remaining subpopulation of plasmatocytes, in addition to being incapable of encapsulating targets in vivo, spread at a significantly reduced rate in vitro. Identical changes in plasmatocyte count and behaviour were observed after injection of virus purified from calyx fluid. Additionally, the activity of calyx fluid was abolished after ultraviolet irradiation. The onset of haemocytic abnormalities occurred more rapidly after natural parasitism of 3rd-instar host larvae. The cell-free haemolymph of calyx fluid-injected 5th-instar larvae also retarded the spreading of plasmatocytes from non-injected control larvae in vitro. We conclude that the abnormalities induced in H. virescens plasmatocytes by C. sonorensis virus contribute to the suppression of encapsulation.     

Effect of a nuclear polyhedrosis virus on the relationship between Trichoplusia ni (Lepidoptera: Noctuidae) and the parasite, Hyposoter exiguae (hymenoptera: Ichneumonidae)

The effect of a nuclear polyhedrosis virus on the relationship between Trichoplusia ni and the parasite, Hyposoter exiguae, was investigated to determine if the virus could invade and multiply in the tissues of the parasites, if parasites which emerged from virus-infected T. ni larvae had normal emergence, fecundity, and longevity, and if the parasite could serve as a vector for the virus. Light microscopy revealed particles which appeared to be polyhedra within the lumen of the midgut of parasite larvae from virus-infected hosts. Transmission electron microscopy confirmed the presence of polyhedra and free virions within the midgut of the larvae. Polyhedra or free virions were never found within any parasite tissues. Parasite larvae within hosts exposed to virus before parasitization perished when their hosts died of virus infection. Parasite larvae in hosts exposed to virus after parasitization completed their development before their hosts died of virus infection. The proportion of parasites which survived increased as the time between host parasitization and host virus exposure increased. Parasite larvae which developed in hosts exposed to the virus soon after parasitization spent significantly less time in their hosts than did parasites which developed in noninfected hosts. There was no significant difference in time spent in the pupal stage, percent adult emergence, adult longevity with and without food and water, and fecundity of parasites which developed in virus-infected hosts and those which developed in noninfected hosts. Female parasites laid as many eggs in virus-infected hosts as they did in noninfected hosts. Sixty percent of the female parasites which oviposited in virus-infected hosts vectored infective doses of virus to an average of 6% of the healthy hosts subsequently exposed to them. None of the healthy host larvae exposed to male parasites which had been exposed to virus-infected host larvae became infected with the virus. Forty percent of the female parasites which developed in virus-infected hosts transmitted infective doses of the virus to an average of 65% of the healthy host larvae exposed to them. Ninety percent of the male parasites which developed in virus-infected hosts transferred infective doses of the virus to an average of 21% of the healthy host larvae exposed to them.     

Hemocytic changes associated with the encapsulation and melanization of some insect parasites

The hemocytic changes that attend parasite encapsulation and melanization in larvae of Drosophila, Musca domestica, and Orthellia caesarion are very similar to those changes occurring in noninfected individuals at metamporhosis. Some of the changes include the precocious differentiation and migration of hemocytes. Comparative and quantitative hemocytological data suggest that some stimulus in infected larvae, acting directly on the hemocytes or on the mechanism(s) controlling their activity, causes the cells to leave areas of the body where they are normally found and to encapsulate parasites. Questions concerning the origin and mode of action of the initial stimulus are raised, and as a basis for future experimentation it is proposed that the cellular immune reactions of these insects against internal metazoan parasites result from a hormonal imbalance.     

The effects of host age and superparasitism by the parasitoid, Microplitis rufiventris on the cellular and humoral immune response of Spodoptera littoralis larvae

To study the dynamics of stage-dependent immune responses in Spodoptera littoralis (Boisd.) larvae (Lepidoptera: Noctuidae), single and superparasitism experiments were carried out using the parasitoid Microplitis rufiventris Kok. (Braconidae: Hymenoptera). Compared to younger (preferred) host larvae, the older (non-preferred) host larvae displayed a vigorous humoral response that often damaged and destroyed the single wasp egg or larva. Superparasitism and host age altered both the cellular and humoral immune responses. Younger host larvae showed a stronger encapsulation response compared to older host larvae. Moreover encapsulation rates in younger hosts (e.g., second instar) decreased with increasing numbers of parasitoid eggs deposited/larvae. In older larvae, the encapsulation rate was low in fourth, less in fifth and absent in sixth instar hosts. Conversely, the order and magnitude of the cellular immune response in S. littoralis hosts were highest in second instar larvae with the first instar larvae being a little lower. The immune response steadily decreased from the third through to the fifth instar and was least obvious in the sixth instar. In contrast, the general humoral immune response was most pronounced in sixth instar larvae and diminished towards younger stages. The results suggest that both cellular and humoral responses are stage-dependent. Wasp offspring in younger superparasitized host larvae fought for host supremacy with only one wasp surviving, while supernumerary wasp larvae generally survived in older superparasitized larvae, but were unable to complete development. Older instars seem to have a method for immobilizing/killing wasp larvae that is not operating in the younger instars.     

Experimental investigation of the seasonal aspect of the relationship between blowflies and their parasites

It has been shown experimentally that the diapause in the life cycles of blowflies Parasarcophaga similis, P. argyrostoma, Bellieria melanura, Calliphora vicina and their parasites Aphaereta minuta and Alysia manducator is induced by the seasonal shortening of the daylength. The host species modifies the photoperiodic reaction of the A. minuta parasite. In A. manducator, there is intraspecific geographical variability of the photoperiodic reaction. In certain conditions, diapause induction in this parasite depends on the physiological state of the host. The parasite's influence on the host's development: parasitization by A. minuta terminates the diapause and induces the premature pupation of Lucilia illustris larvae.     

Imaging mosquito transmission of Plasmodium sporozoites into the mammalian host: Immunological implications

The malaria infection is initiated in mammals by injection of the sporozoite stage of the parasite through the bite of Plasmodium-infected, female Anopheles mosquitoes. Sporozoites are injected into extravascular portions of the skin while the mosquito is probing for a blood source. Sporozoite gliding motility allows them to locate and penetrate blood vessels of the dermis or subcutaneous tissues; once in the blood, they reach the liver, within which they continue their development. Some of the injected parasites invade dermal lymph vessels and travel to the proximal draining lymphatic node, where they interact with host immunocytes. The host responds to viable or attenuated sporozoites with antibodies directed against the immunodominant circumsporozoite protein (CSP), as well as against other sporozoite proteins. These CSP antibodies can inhibit the numbers of sporozoites injected by mosquitoes and the motility of those injected into the skin. This first phase of the immune response is followed by cell-mediated immunity involving CD8 T-cells directed against the developing liver stage of the parasite. This review discusses the early history of imaging studies, and focuses on the role that imaging has played in enabling a better understanding of both the induction and effector functions of the immune responses against sporozoites.     

Age and size at maturity of the mosquito Culex pipiens infected by the microsporidian parasite Vavraia culicis

The costs of parasitism to a host''s reproductive success (RS) often increase with time since infection. For hosts experiencing this type of infection, it is predicted that they will maximize their RS by bringing forward their schedule of reproduction. This is because the costs associated with such a response can be discounted against a reduced future RS due to parasitism. The microsporidian Vavraia culicis is a natural parasite of mosquitoes and one whose costs increase over time as its spores accumulate and damage host tissues. As larvae, male and female Culex pipiens mosquitoes behaved differently towards infection with V. culicis. Infected females pupated earlier than uninfected females and tended to emerge as smaller adults, indicating a cost to their fecundity. However, the age and size at maturity of infected male mosquitoes was no different from uninfected males. The results of this study support theoretical predictions and highlight the potential roles that host gender and density-dependent interactions may have in determining the response of host life-history traits to parasitism.     

Resistance of Apanteles eggs to the haemocytic encapsulation by their habitual host, Pieris

The calyx fluid in the lateral oviduct of a gregarious parasitoid, Apanteles glomeratus contained ellipsoid particles of ca. 130 × 200 nm. These calyx fluid particles did not appear to be embedded in a fibrous outer layer on the surface of eggs in the lateral oviduct. They were not observed on the surfaces of the eggs 3 to 4 hr after being deposited into the host haemocoele. Oviposition experiments indicated that the occurrence of haemocytic defence reactions of the late 2nd instar larvae of the Pieris rapae crucivora against 1 st instar larvae of the parasitoid increased with a decreasing number of the parasitoid eggs introduced into a host, and that more than 5 to 9 parasitoid eggs were needed for suppressing the ability of the host to encapsulate its parasitoid larvae immediately after hatching. When eggs with calyx fluid obtained from egg reservoir were injected into the host, they were found to be encapsulated 1 to 2 days after the injection. They could not start their embryonic development. When calyx fluid-free 3-hr-old eggs were injected in a number of more than 5 eggs into a 5th instar larva of Pieris, 58% of 31 eggs injected had normally hatched without evoking encapsulation reactions by the host. Both electron microscopic observations of parasitoid eggs in the host haemocoele and the experimental results suggested that calyx fluid or calyx fluid particles of the parasitoid might not be involved in the encapsulation-inhibiting activity of the parasitoid eggs. Rather it was anticipated that a substance (or substances) might be secreted by the parasitoid eggs into the haemocoele of the host, which suppressed defence reactions of the host.     

Thinking outside the blood: Perspectives on tissue-resident Trypanosoma brucei

Trypanosoma brucei is a protozoan parasite that causes human and animal African trypanosomiases (HAT and AAT). In the mammalian host, the parasite lives entirely extracellularly, in both the blood and interstitial spaces in tissues. Although most T. brucei research has focused on the biology of blood- and central nervous system (CNS)-resident parasites, a number of recent studies have highlighted parasite reservoirs in the dermis and adipose tissue, leading to a renewed interest in tissue-resident parasite populations. In light of this renewed interest, work describing tissue-resident parasites can serve as a valuable resource to inform future investigations of tissue-resident T. brucei. Here, we review this body of literature, which describes infections in humans, natural hosts, and experimental animal models, providing a wealth of information on the distribution and biology of extravascular parasites, the corresponding immune response in each tissue, and resulting host pathology. We discuss the implications of these studies and future questions in the study of extravascular T. brucei.     

Intermediate host specificity in Schistosoma mansoni

Miracidia of Schistosoma mansoni penetrate into many kinds of snails, but development of normal sporocysts takes place only in certain species of Biomphalaria. Different populations of this snail vary greatly in laboratory infection rates with S. mansoni originating from diverse geographic localities. Cross-exposure experiments show that compatibility factors exist in both snails and parasites. Susceptibility of stocks of Biomphalaria to particular strains of S. mansoni is genetically determined and may be modified by selection in the laboratory. In a compatible snail, the sporocyst develops without host tissue reaction; in incompatible snails the early larvae are rapidly surrounded by amebocytes and fibroblasts, and destroyed. This reaction resembles the generalized host cellular response elicited by any foreign body. An individual snail exposed to many miracidia may have both developing and encapsulated sporocysts side by side within its tissues. The weight of current evidence suggests that elicitation or absence of this cellular response resides in the recognition or nonrecognition of the sporocyst as a foreign body. The sporocyst tegument surface, which forms within a few hours after miracidial penetration, may have a molecular conformation identical with that of the snail, or may be able to bind specific host molecules, so that detection and subsequent encapsulation by host cells are averted. Presuming genetic determination of the sporocyst surface structure and of the host cell detection capability, differing infection rates would result from the particular frequencies of relevant genes in the populations concerned.     

Biochemical Aspects of Parasitism by the Angiosperm Parasites: Phenolics in Parasites and Hosts

the contents of total phenolics in three parasitic angiosperms, Cuscuta species, Orobanche aegyptiaca and Dendrophthoe falcata and their respective hosts, were colorimetrieally determined. A biochemical comparison was made of the phenolics on the basis of the ability of alcoholic extracts of the tissues to inhibit amylose phosphorylase in vitro. High concentration of phenolics seemed to be a general feature of parasitic angiosperms. An increase in the concentration of the phenolics occurred in the tissues of infected hosts, in comparison with controls. the phenolics of Orobanche and mistletoe had inhibitory activity against amylose phosphorylase, but those of Cuscuta developed the inhibitory ability only when growing on hosts which themselves possessed inhibitory phenolics. the inhibitory activity of host phenolics was sometimes altered as a result of infection by parasite. Although the hosts often exerted some influence on the concentration and the inhibitory activity of phenolics in the parasites, there was no direct relationship between host and parasite phenolics. the sum of the phenolics in the tissues of parasite and the infected bost generally exceeded the phenolics in the tissues of the control host. The content of phenolics and their inhibitory activity did not appear to be directly related to the resistance of a host or to the extent of its susceptibility to parasite infection.     

Larvae of the tachinid fly,Drino inconspicuoides (Diptera: Tachinidae), suppress melanization in host lepidopteran insects

The ovoviviparous parasitoid, Drino inconspicuoides (Diptera: Tachinidae) parasitizes a wide range of lepidopteran insects; larval period progresses in the host hemocoel. Here, we examined how D. inconspicuoides responds to melanization, which involves the activation of prophenoloxidases and is the first immune reaction induced by the host against invading organisms. We found that the larvae of D. inconspicuoides suppressed the activation of prophenoloxidases in its natural hosts, Mythimna separata (Lepidoptera: Noctuidae) and Bombyx mori (Lepidoptera: Bombycidae). The suppression of melanization starts immediately after invasion and is maintained for at least 24 h. We did not detect a drastic degradation of prophenoloxidases, suggesting that the presence of other molecules targeted by D. inconspicuoides suppresses melanization. D. inconspicuoides does not inhibit a cellular immune reaction, encapsulation, and thus, it is likely that the tachinids survive secondary infections of the host by partially retaining the host immune function.     

A hyperparasite of coccids develops as a primary parasite of fly puparia

Species ofPachyneuron (Hym.: Pteromalidae) have been recorded as either primary parasites or hyperparasites.P. concolor (Foerster) is a polyphagous secondary parasite, attacking encyrtid primary parasites in soft scales, mealy bugs and coccinellid larvae. It also develops as a tertiary parasite. We now report thatP. concolor may also develop as a primary parasite of aphidophagous fly puparia. Host selection in this species appears to be based on locating a soft-bodied host within a hard, dry shell, independent of whether the host is a dipterous pupa in its puparium or a primary parasite in its mummified host. The overall effect ofP. concolor is detrimental. Its introduction into new areas should definitely be avoided.     

Cellular immune competence of a Drosophila mutant with neoplastic hematopoietic organs

In the Tum^l mutant of Drosophila melanogaster, the larval hematopoietic organs undergo neoplastic changes and release into circulation large numbers of blood cells. The lamellocytes, and to a lesser extent the plasmatocytes from which they are derived, are the cells that encapsulate various endogenous tissues and form melanotic tumors. The mutation is temperature sensitive, with maximum gene expression manifested at 29°C. The ability of Tum^l larvae to encapsulate eggs of the wasp parasite Leptopilina heterotoma is dependent not only on temperature, with host larvae much more immune reactive at 29°C than at lower temperatures (15° or 21°C), but also on the interval of time following infection when temperature shift experiments are performed. When the shift of parasitized larvae from 21° to 29°C is delayed by 18 hr the hosts are not as immune reactive as those shifted immediately after infection. Since Tum^l larvae are potentially highly immune reactive at the time of infection (with sufficient numbers of lamellocytes in circulation to encapsulate parasites), the low degree of immune competence in hosts shifted to 29°C after 18 hr or maintained at lower temperatures suggests that the increased capacity of blood cells to react against foreign surfaces is dependent on the cells acquiring new or altered recognition and adherence properties at 29°C. The 18-hr delay may provide the parasite with an opportunity to interfere with the acquisition of these specific cellular alterations. Differential hemocyte counts from parasitized larvae show abnormally low lamellocyte counts in susceptible hosts, indicating that successfully developing parasites interfere with the differentiation of hemocytes.     

An ultrastructural study on ventricular encapsulation reactions in Biomphalaria glabrata exposed to irradiated echinostome parasites

Jeong K. H., Lie K. J. and Heyneman D. 1984. An ultrastructural study on ventricular encapsulation reactions in Biomphalaria glabrata exposed to irradiated echinostome parasites. International Journal for Parasitology14: 127–133. Encapsulation reactions around sporocysts of Echinostoma lindoense and E. paraensei have been studied in the ventricle of Biomphalaria glabrata using ultrastructural procedures. Amebocytes and ameboblasts migrate from the amebocyte-producing organ to the ventricle and there surround irradiated echinostome larvae. Specialized junction sites were found that linked amebocytes in the three phases of capsule formation, migratory, flattening and phagocytic. Active engulfing of portions of the tegument by amebocytes was followed by phagocytosis of parasite internal cells and formation in amebocytes of residual bodies of indigestible material. Regression of encapsulation reactions in the ventricle was frequently associated with formation of sear tissue. Comparisons made between types of encapsulation reactions observed around echinostomes and schistosomes in B. glabrata reveal differences in speed of response, number of cells involved and size of amebocyte pseudopodia.     

Gimme shelter – the relative sensitivity of parasitic nematodes with direct and indirect life cycles to climate change

Climate change is expected to alter the dynamics of host–parasite systems globally. One key element in developing predictive models for these impacts is the life cycle of the parasite. It is, for example, commonly assumed that parasites with an indirect life cycle would be more sensitive to changing environmental conditions than parasites with a direct life cycle due to the greater chance that at least one of their obligate host species will go extinct. Here, we challenge this notion by contrasting parasitic nematodes with a direct life cycle against those with an indirect life cycle. Specifically, we suggest that behavioral thermoregulation by the intermediate host may buffer the larvae of indirectly transmitted parasites against temperature extremes, and hence climate warming. We term this the ‘shelter effect’. Formalizing each life cycle in a comprehensive model reveals a fitness advantage for the direct life cycle over the indirect life cycle at low temperatures, but the shelter effect reverses this advantage at high temperatures. When examined for seasonal environments, the models suggest that climate warming may in some regions create a temporal niche in mid‐summer that excludes parasites with a direct life cycle, but allows parasites with an indirect life cycle to persist. These patterns are amplified if parasite larvae are able to manipulate their intermediate host to increase ingestion probability by definite hosts. Furthermore, our results suggest that exploiting the benefits of host sheltering may have aided the evolution of indirect life cycles. Our modeling framework utilizes the Metabolic Theory of Ecology to synthesize the complexities of host behavioral thermoregulation and its impacts on various temperature‐dependent parasite life history components in a single measure of fitness, R₀. It allows quantitative predictions of climate change impacts, and is easily generalized to many host–parasite systems.     

Predictors of Parasitism in Wild White-Faced Capuchins (Cebus capucinus)

Parasite infections in wildlife are influenced by many factors including host demography, behavior and physiology, climate, habitat characteristics, and parasite biology and ecology. White-faced capuchins (Cebus capucinus) host a suite of gastrointestinal and pulmonary parasites, yet the mechanisms affecting host susceptibility and parasite transmissibility have not been examined in this host species. We used the information-theoretic approach (Akaike’s information criterion) and traditional null-hypothesis testing to determine which host characteristics, behaviors, or environmental factors affected the presence of two prevalent capuchin parasites (Filariopsis barretoi and Strongyloides sp.) as well as parasite species richness in four groups of wild capuchins from September 2007 to January 2008 and January to August 2009. Older capuchins were more likely to be infected with Filariopsis barretoi and had higher parasite species richness. Age-biased nematode infections may stem from age differences in capuchin behavior and physiology while high species richness likely results from long- term exposure to numerous parasite species. Infections with Strongyloides sp. were more likely to occur in the dry season when capuchins often descend to the forest floor to drink from terrestrial water sources, potentially increasing their risk of infection from soil-borne larvae. Capuchin behaviors were poor predictors of parasitism, as were female rank, host sex, home range size, and habitat quality. Many of our results were atypical for primate parasitology, suggesting that host–parasite interactions, and subsequently infection risk, may differ in highly seasonal habitats such as tropical dry forests where these monkeys occur.     

Genome-wide gene expression in response to parasitoid attack in <Emphasis Type="Italic">Drosophila</Emphasis>

Background  

Parasitoids are insect parasites whose larvae develop in the bodies of other insects. The main immune defense against parasitoids is encapsulation of the foreign body by blood cells, which subsequently often melanize. The capsule sequesters and kills the parasite. The molecular processes involved are still poorly understood, especially compared with insect humoral immunity.