Review of microsporidia-mosquito relationships: from the simple to the complex

Microsporidia in mosquitoes can be divided into two categories based on their life cycles and host-parasite relationships. Some species of microsporidia exhibit simple life cycles with one spore type responsible for oral (horizontal) transmission. They affect only one generation of the mosquito and are not usually host or tissue specific. Brachiola algerae and Vavraia culicis are examples of species isolated from mosquitoes with relatively straightforward life cycles (one spore type) and simple host-parasite relationships. B. algerae and a close relative of V. culicis have also been isolated from a vertebrate (human) host but sources for these infections are unknown. In contrast to B. algerae and V. culicis, polymorphic (heterosporous) microsporidia in mosquitoes are characterized by complex life cycles involving multiple spore types responsible for horizontal and vertical transmission. They affect two generations of the mosquito and some involve an obligate intermediate host. These microsporidia are generally very host and tissue specific with complex developmental sequences comprised of unique stages and events. The microsporidium Edhazardia aedis is a pathogen of Aedes aegypti and does not require an intermediate host. The developmental cycle of E. aedis is characterized by four sporulation sequences, two in the parental host and two in the filial generation. Recent speculation relative to the source of B. algerae human infection have implicated infected mosquitoes and raised concerns about the safety of mosquito microsporidia in general. The subject of this review is to compare and contrast three species of microsporidia from mosquitoes, two with broad host ranges (B. algerae and V. culicis) and one specific to mosquitoes (E. aedis). This review describes features that distinguish mosquito-parasitic microsporidia with simple life cycles and broad host ranges from truly mosquito-specific microsporidian parasites with complex life cycles.     

Microsporidia in aquatic microcrustacea: the copepod microsporidium Marssoniella elegans Lemmermann, 1900 revisited

Marssoniella elegans Lemmermann, 1900, a parasite of ovarial tissues of the copepod Cyclops vicinus Uljanin, 1875, was studied as a representative of aquatic-clade microsporidia which form "heteroinfectious spores" (spores not infective to the original host as opposed to "homoinfectious spores" which are infective for the original host) and which thus should require an alternate host. Several structural characters of this microsporidian are similar to those of copepod morphs of microsporidia infecting mosquitoes. However, small subunit ribosomal DNA phylogeny indicates that caddis flies (Insecta, Trichoptera) might be the alternate hosts of Marssoniella. Ultrastructural data obtained are used to redefine the genus Marssoniella Lemmermann, 1900 and its type species Marssoniella elegans.     

流行性乙型脑炎与三带喙库蚊的防控

流行性乙型脑炎(乙脑)在我国广泛流行。三带喙库蚊是主要媒介,依据如下:(1)三带喙库蚊是乙脑流行区的优势蚊种;(2)该种蚊的季节消长与乙脑的季节分布相一致;(3)该种蚊有乙脑病毒的自然感染,带菌率高;(4)该种蚊能叮刺和经卵传递乙脑病毒。防控方法:(1)环境治理;(2)管理宿主动物(猪等);(3)灭蚊降低密度;(4)做好个人防护;(5)接种疫苗。     

莲缢管蚜生物学与种群消长规律的研究

莲缢管蚜是水生经济植物与核果类果树上的主要害虫,在江苏为全周期型。秋季,雌性蚜虫在冬寄主核果类果树上产卵。夏寄主有慈姑、莲藕、菱角、芡实、绿萍等水生经济植物。调查结果表明:北纬30°以南广大地区主要以胎生雌蚜过冬,营孤雌生殖,为不全周期型。莲缢管蚜全年可完成27—29代,无翅胎生雌蚜的寿命、产卵量与温湿度有关。23—27℃、相对湿度为81—92％时,有利于成蚜的生长和繁殖,每头成蚜平均产蚜67头,成蚜寿命9.7—10.4天。莲缢管蚜种群动态全年出现3个高峰,分别为4月下旬至5月初;6月下旬至7月上旬;8月下旬至9月中旬。主要天敌有:长突毛瓢虫、中华草蛉、食蚜肓蝽、黑带食蚜蝇等,对种群有一定的抑制作用。     

Studies on the development of the cestode Proteocephalus neglectus La Rue, 1911 (Cestoda: Proteocephalidae) under experimental conditions

A part of the life cycle of Proteocephalus neglectus La Rue, 1911, a parasite of trout, starting from release of eggs from mature parasites into water, to the early phase of development in the definitive host, was studied under experimental conditions. Special regard has been paid to development in the intermediate host, copepod Cyclops strenuus. Some oncospheres in eggs kept in water at 5 and 10 degrees C remained infective for 20-25 days. The percentage of infected copepods depended on the length of their contact with parasite eggs. Cestode larvae (cercoscoleces) were formed in the intermediate host on days 8-10 p.i. at the temperatures of 21-22 degrees C, on days 18-21 at 15 degrees C, on days 24-28 at 10 degrees C, and on days 59-65 at 6 degrees C. Most larvae, including infective cercoscoleces, were localized in the cephalothorax of the intermediate host, particularly in its first segment. This localization did not change during their development. The infectivity of cercoscoleces was verified by experimental infection of Salmo gairdneri fry. The development of the cestode in this definitive host was observed for 17 days after infection at 10 degrees C. The finding of P. neglectus cereoscoleces in fish of the families Cottidae and Cyprinidae on day 2 after experimental infection indicates that these larvae can survive for a short time in atypical fish hosts.     

Distribution of Hatschekia pagellibogneravei (Copepoda: Hatschekiidae) on the gills of Pagellus bogaraveo (Teleostei: Sparidae) from Madeira, Portugal

A population of the gill parasite Hatschekia pagellibogneravei (Hesse, 1878) was studied on one of its sparid fish hosts, the blackspot seabream, Pagellus bogaraveo (Brünnich), off the coast of Madeira Island, Portugal, northeast Atlantic. Very high infection levels of this copepod were detected, with no significant seasonal differences. Abundance was negatively correlated with fish size. There were significant differences in the distribution of this copepod among the gill arches of the host, which seem to be best explained by differences in water flow within the gill habitat.     

Microsporidian xenomas in fish seen in wider perspective

The history of understanding xenoparasitic complexes or xenomas provoked in the host cell by various protists and especially by microsporidia is outlined. Microsporidia have been known to produce xenomas in oligochaetes (e.g., genera Bacillidium, Burkea, Hrabyeia, Jirovecia, species of the collective group Microsporidium), crustaceans (e.g., Abelspora, Mrazekia), insects (e.g., Polydispyrenia, Thelohania) and poikilothermic vertebrates, mostly fish (Alloglugea, Amazonspora, Glugea, Ichthyosporidium, Loma, Microfilum, Microgemma, Neonosemoides, Pseudoloma, Spraguea, Tetramicra). An overview of characters of xenomas caused by species of these genera is presented. The study of microsporidia causing xenomas in fish offers an insight into cell pathology and is of interest since many of these species are important agents of diseases in commercial fish. Xenomas produced from a few types of target cell display a complete change of organisation of the host cell and differ, according to the agent, in their structure. Recent data show that proliferation of the parasite may have already started in the cells transporting the parasites to the final site of xenoma formation. However, these are preliminary revelations and most of the facets of the life cycle are still to be clarified. Curiously, xenoma-forming microsporidia do not seem to be strictly host specific. The salient features of fish microsporidian xenomas are discussed, such as role of the xenoma, whether its features are host- or microsporidium-dependent, development and demise of the xenoma in the course of time, and host reaction phenomena. The need of further research is emphasised.     

New evidence on a cold case: trophic transmission, distribution and host-specificity in Hedruris spinigera (Nematoda: Hedruridae)

The life cycle of Hedruris spinigera Baylis, 1931 (Nematoda: Hedruridae) is determined here with the first formal identification of the parasite's intermediate host: the crustacean amphipod Paracorophium excavatum Thomson. Adult H. spinigera are redescribed from specimens collected from the stomach of fishes, Retropinna retropinna (Richardson) and Aldrichettaforsteri (Valenciennes), from Lake Waihola, New Zealand. Immature adults of the parasite collected from intermediate hosts (P. excavatum) are also described for the first time. The prevalence, abundance and intensity of infection of H. spinigera in several fish species are quantified along with the occurrence of P. excavatum, the parasite's intermediate host, in fish stomach contents. Although H. spinigera's transmission mode (trophic transmission) and fish diet potentially expose all fish species to infection, some level of host specificity must exist as parasite prevalence, abundance and intensity of infection vary greatly between potential definitive host species. We suggest here that the anatomy of the fish digestive tract and especially that of the stomach plays an important role in host suitability for H. spinigera. While P. excavatum is the only intermediate host in Lake Waihola, H. spinigera was found in six different fish species: Aldrichetta forsteri, Galaxias maculatus (Jenyns), Retropinna retropinna, Rhombosolea retiaria Hutton, Perca fluviatilis Linnaeus and Salmo trutta Linnaeus; although typical hedrurid attachment and mating positions were observed only in R. retropinna and A. forsteri. The limited distribution of H. spinigera is most likely due to that of its different host species (intermediate and definitive), all inhabitants of coastal fresh and brackish waters.     

Effects of host-immunity on the life cycle of Hyalomma rufipes Koch, 1844 (Ixodoidea: Ixodidae)

Studies of the effects of host-immunity on the life cycle of Hyalomma rufipes were carried out by allowing the ticks to feed on New Zealand white rabbits under laboratory conditions. The immunity of the rabbit host significantly affected the life cycle of this tick, reducing the percentage recovery of engorged females, their engorged weights and the total number of eggs laid by these females. The viability of the eggs laid by them was also considerably reduced compared to the eggs laid by females fed on naive rabbit hosts. The effects of host immunity were also revealed in the tendency towards three-host development of this species, which otherwise behaved as a two-host tick when fed on non-immune rabbit hosts.     

棉蚜生活史类型及其越冬寄主研究进展

棉蚜(Aphis gossypii)是一种生活史较复杂的杂食性农业害虫,由于以不同地域气象因素和植被的差异,限制了其生活史类型和越冬寄主种类。分析全球研究棉蚜生活史策略文献,以棉蚜能否以卵越冬为主线,分析世界不同区域棉蚜的2种生活史类型,对棉蚜异寄主全周期型这一生活史策略的原生寄主进行梳理。通过分析棉蚜在不同区域的生活史策略及其越冬寄主,有助于深入研究农作物保护策略,为棉蚜的系统化防治奠定理论基础。     

Importance of the life cycle in sympatric host race formation and speciation of pathogens

ABSTRACT Numerous morphological species of pathogenic fungi have been shown to actually encompass several genetically isolated lineages, often specialized on different hosts and, thus, constituting host races or sibling species. In this article, we explore theoretically the importance of some aspects of the life cycle on the conditions of sympatric divergence of host races, particularly in fungal plant pathogens. Because the life cycles classically modeled by theoreticians of sympatric speciation correspond to those of free-living animals, sympatric divergence of host races requires the evolution of active assortative mating or of active host preference if mating takes place on the hosts. With some particular life cycles with restricted dispersal between selection on the host and mating, we show that divergence can occur in sympatry and lead to host race formation, or even speciation, by a mere process of specialization, with strong divergent adaptive selection. Neither active assortative mating nor active habitat choice is required in these cases, and this may explain why the phylo-genetic species concept seems more appropriate than the biological species concept in these organisms.     

On the problem of retarding definitive host (s.l.)

The significance of the species and individual level in determining the hosts as a category of helminth life cycles is pointed out. From the viewpoint of species level, the categories of intermediate host and definitive host are ascribed to certain organisms as representatives of a certain species on the basis of the fact that a respective stage of helminth life cycle can take place inside them. From the viewpoint of individual level, these types of hosts are determined on the basis of associations between the helminth individual and host individual. In order to avoid discrepancies, which might occur in determining the host type in these ways, it is proposed that the organism, which was determined as intermediate or definitive host at the species level, should be regarded identically also at the individual level. In addition, the existence of retarding definitive host (s.l.) is substantiated on the example of helminths which survived the interorgan migrations and passed to the offsprings through the intrauterine or transmammary route.     

Malaria vector control in the third millennium: progress and perspectives of molecular approaches

Remarkable progress has been made towards a deeper understanding of mosquito biology since the completion of the Anopheles gambiae Giles genome project. Combined with the development of efficient transgenic technologies for genetic modification of major vector species and the availability of powerful molecular, genetic and bioinformatics tools, this is allowing the identification of genes involved in mosquito biological functions crucial to malaria transmission, ranging from host-seeking behaviour and innate immunity to insecticide resistance. Moreover, population genetic studies are beginning to elucidate the complex structure of vector populations. Finally, novel methods for malaria control are emerging that are based on the use of genetically modified mosquitoes either to interrupt the journey of the Plasmodium parasite within its insect host or to suppress those mosquito species that function as vectors for parasite transmission.     

Studies on transmission and life cycle of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus

In order to elucidate the transmission and dispersion routes used by the myxozoan parasite Enteromyxum scophthalmi Palenzuela, Redondo et Alvarez-Pellitero, 2002 within its host (Scophihalmus maximus L.), a detailed study of the course of natural and experimental infections was carried out. Purified stages obtained from infected fish were also used in in vitro assays with explants of uninfected intestinal epithelium. The parasites can contact and penetrate loci in the intestinal epithelium very quickly. From there, they proliferate and spread to the rest of the digestive system, generally in an antero-posterior pattern. The dispersion routes include both the detachment of epithelium containing proliferative stages to the intestinal lumen and the breaching of the subepithelial connective system and local capillary networks. The former mechanism is also responsible for the release of viable proliferative stages to the water, where they can reach new fish hosts. The finding of parasite stages in blood smears, haematopoietic organs, muscular tissue, heart and, less frequently, skin and gills, suggests the existence of additional infection routes in transmission, especially in spontaneous infections, and indicates the role of vascular system in parasite dispersion within the fish. The very high virulence of this species in turbot and the rare development of mature spores in this fish may suggest it is an accidental host for this parasite. This may also question the existence of a two-host life cycle involving an actinosporean stage in this species. Further studies are needed to clarify this open point of the life cycle.     

How do microsporidia invade cells?

Microsporidia are obligate intracellular eukaryotic parasites that utilize a unique mechanism to infect host cells. One of the main characteristics of all microsporidia is that they produce spores containing an extrusion apparatus that consists of a coiled polar tube ending in an anchoring disc at the apical part of the spore. With appropriate conditions inside a suitable host, the polar tube is discharged through the thin anterior end of the spore, thereby penetrating a new host cell for inoculating the infective sporoplasm into the new host cell. This method of invading new host cells is one of the most sophisticated infection mechanisms in biology and ensures that the microsporidia enter the host cell unrecognized and protected from the host defence reactions. Recent studies have shown that microsporidia gain access to host cells by phagocytosis as well. However, after phagocytosis, the special infection mechanism of the microsporidia is used to escape from the maturing phagosomes and to infect the cytoplasm of the cells. Gaining access to cells by endocytosis, and escaping destruction in the phago-/endo-/lysosome by egressing quickly from the phagocytic vacuole to multiply outside the lysosome, is a common phenomenon in biology that has been evolved several times during evolution. How this is put into execution by the microsporidia is an inimitable principle by which an obligate intracellular organism has managed this problem. The extrusion apparatus of the microsporidia has obviously ensured the success of this phylum during evolution, resulting in a group of obligate intracellular organisms, capable of infecting almost any type of host and cell.     

Life cycle and epizootiology of Amblyospora ferocis (Microspora: Amblyosporidae) in the mosquito Psorophora ferox (Diptera: Culicidae)

A natural population of Psorophora ferox (Humbold, 1820) infected with the microsporidium Amblyospora ferocis Garcia et Becnel, 1994 was sampled weekly during a seven-month survey in Punta Lara, Buenos Aires Province, Argentina. The sequence of development of A. ferocis in larvae of P. ferox leading to the formation of meiospores followed the developmental pathway previously reported for various species of Amblyospora. The natural prevalence of A. ferocis in the larval population of P. ferox ranged from 0.4% to 13.8%. Spores were detected in the ovaries of field-collected females of P. ferox and were shown to be responsible for transovarial transmission of A. ferocis to the next generation of mosquito larvae in laboratory tests. These spores were binucleate and slightly pyriform in shape. The prevalence of A. ferocis in the adult population ranged from 2.7% to 13.9%. Data on effects of the infection on female fecundity showed that infected field-collected adults of P. ferox laid an average of 47.6 +/- 6.5 eggs of which 35.8% +/- 4.1% hatched. Uninfected field-collected adults of P. ferox laid 82.8 +/- 6.8 eggs of which 64.1% +/- 5.5% hatched. Six species of copepods living together with P. ferox were fed meiospores from field-infected larvae but none became infected. Horizontal transmission of A. ferocis to P. ferox larvae remains unknown.     

The biology of nematodes of the family Capillariidae Neveu-Lemaire, 1936

The present knowledge of the life cycles of nematodes of the family Capillariidae is reviewed and these data are considered from the viewpoint of a new system of the classification of genera in this family (Moravec 1982). An analysis of the relevant literature as also own studies have shown that, in this nematode group, there occur both direct (homoxenous) life cycles without an intermediate host (Baruscapillaria, Pseudocapillaria, Calodium, Pseudocapillaroides, partly also Capillaria, Eucoleus and Aonchotheca) and heteroxenous cycles with participation of obligate intermediate hosts that are usually oligochaetes and rarely fishes (Schulmanela, Pearsonema, partly also Capillaria, Eucoleus and Aonchotheca). A remarkable case is the species Aonchotheca philippinensis, an intestinal parasite of man, with alternative life cycles, i.e. either with participation of the intermediate host or without it (autoinfection), this being dependent on whether eggs or larvae are produced by the female parasites. The transmission of some capillariid species with a direct life cycle may include paratenic hosts (oligochaetes, fishes). Capillariids undergo four moults during their ontogenetic development, the first of which taking place inside the body of the intermediate host in case of heteroxenous cycles. The present knowledge of the biology of nematodes of the Capillariidae is very incomplete; their life cycles have hitherto been studied (in a different extent) in members of only 9 out of 22 presently valid genera (approximately in 7% of recognized capillariid species).     

Experimental infection of Atlantic salmon (Salmo salar) with marine Eubothrium sp. (Cestoda: Pseudophyllidea): observations on the life cycle, aspects of development and growth of the parasite.

The life cycle of marine Eubothrium sp. (Cestoda: Pseudophyllidea), from Atlantic salmon (Salmo salar L.) was experimentally completed in one year and included only one intermediate host (Acartia tonsa Dana) (Copepoda: Calanoida). Adult cestodes were collected from farmed salmon, and ripe eggs released by the cestodes were fed to Acartia tonsa. Ingested eggs hatched in the gut and the larvae developed in the haemocoel of the copepod for 15 days at 16 degrees C. A total of 170 seawater-reared salmon were exposed to infected copepods and the total prevalence of Eubothrium sp. in the salmon after infection was 95.3%, with a mean intensity of 15.0 (range 1-87). The infected salmon were kept in the laboratory where the growth of the cestodes was studied for eleven months. Mean length of the cestodes increased with time, but a large variation among the cestodes was observed. Growth and maturation of the cestodes were dependent on host size and the number of worms present in the intestine. No evidence of mortality of Eubothrium sp. was observed during the experimental period.     

On the problem of variable numbers of hosts in the life-cycles of helminths.

The authors analyze the phenomena underlying the variation of host numbers in the life-cycle of several helminth species. Variation of host number in the cycle is effected by alternative shortening of the cycle (with this the cycle turns out either without or with a polyvalent obligatory host or, in rarer cases, without or with appearing of neogeny) or by facultative widening of the cycle (without or with participation of additional hosts, namely para-paratenic, paradefinitive, metaparatenic, or euparatenic hosts). The term of metaparatenic host is made precise by limitation to a "hemistadiogenous" additional host (sensu Barus and Rysavy 1977).