Parasitism of Molluscs by Nematodes: Types of Associations and Evolutionary Trends

Although there are no confirmed fossil records of mollusc parasitic nematodes, diverse associations of more than 108 described nematode species with slugs and snails provide a fertile ground for speculation of how mollusc parasitism evolved in nematodes. Current phylogenic resolution suggests that molluscs have been independently acquired as hosts on a number of occasions. However, molluscs are significant as hosts for only two major groups of nematodes: as intermediate hosts for metastrongyloids and as definitive hosts for a number of rhabditids. Of the 61 species of nematodes known to use molluscs as intermediate hosts, 49 belong to Metastrongyloidea (Order Strongylida); of the 47 species of nematodes that use molluscs as definitive hosts, 33 belong to the Order Rhabditida. Recent phylogenetic hypotheses have been unable to resolve whether metastrongyloids are sister taxa to those rhabditids that use molluscs as definitive hosts. Although most rhabditid nematodes have been reported not to kill their mollusc hosts prior to their reproduction, some species are pathogenic. In fact, infective juveniles of Phasmarhabditis hermaphrodita vector a lethal bacterium into the slug host in which they reproduce. This life cycle is remarkably similar to the entomopathogenic nematodes in the families Steinernematidae and Heterorhabditidae. Also, the discoveries of Alloionema and Pellioditis in slugs are interesting, as these species have been speculated to represent the ancestral forms of the entomopathogenic nematodes. Development of the infective stage appears to be an important step toward the acquisition of molluscs as definitive hosts, and the association with specific bacteria may have arisen in conjunction with the evolution of necromeny.     

Diverse Host-Seeking Behaviors of Skin-Penetrating Nematodes

Skin-penetrating parasitic nematodes infect approximately one billion people worldwide and are responsible for some of the most common neglected tropical diseases. The infective larvae of skin-penetrating nematodes are thought to search for hosts using sensory cues, yet their host-seeking behavior is poorly understood. We conducted an in-depth analysis of host seeking in the skin-penetrating human parasite Strongyloides stercoralis, and compared its behavior to that of other parasitic nematodes. We found that Str. stercoralis is highly mobile relative to other parasitic nematodes and uses a cruising strategy for finding hosts. Str. stercoralis shows robust attraction to a diverse array of human skin and sweat odorants, most of which are known mosquito attractants. Olfactory preferences of Str. stercoralis vary across life stages, suggesting a mechanism by which host seeking is limited to infective larvae. A comparison of odor-driven behavior in Str. stercoralis and six other nematode species revealed that parasite olfactory preferences reflect host specificity rather than phylogeny, suggesting an important role for olfaction in host selection. Our results may enable the development of new strategies for combating harmful nematode infections.     

Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown Clades

Inference of evolutionary relationships between nematodes is severely hampered by their conserved morphology, the high frequency of homoplasy, and the scarcity of phylum-wide molecular data. To study the origin of nematode radiation and to unravel the phylogenetic relationships between distantly related species, 339 nearly full-length small-subunit rDNA sequences were analyzed from a diverse range of nematodes. Bayesian inference revealed a backbone comprising 12 consecutive dichotomies that subdivided the phylum Nematoda into 12 clades. The most basal clade is dominated by the subclass Enoplia, and members of the order Triplonchida occupy positions most close to the common ancestor of the nematodes. Crown Clades 8-12, a group formerly indicated as "Secernentea" that includes Caenorhabditis elegans and virtually all major plant and animal parasites, show significantly higher nucleotide substitution rates than the more basal Clades 1-7. Accelerated substitution rates are associated with parasitic lifestyles (Clades 8 and 12) or short generation times (Clades 9-11). The relatively high substitution rates in the distal clades resulted in numerous autapomorphies that allow in most cases DNA barcode-based species identification. Teratocephalus, a genus comprising terrestrial bacterivores, was shown to be most close to the starting point of Secernentean radiation. Notably, fungal feeding nematodes were exclusively found basal to or as sister taxon next to the 3 groups of plant parasitic nematodes, namely, Trichodoridae, Longidoridae, and Tylenchomorpha. The exclusive common presence of fungivorous and plant parasitic nematodes supports a long-standing hypothesis that states that plant parasitic nematodes arose from fungivorous ancestors.     

Seasonal dynamics of Skrjabinoptera phrynosoma (Nematoda) infection in horned lizards from the Alvord Basin: temporal components of a unique life cycle

The nematode Skrjabinoptera phrynosoma is a stomach parasite of horned lizards in the genus Phrynosoma. This nematode demonstrates a distinctive life cycle wherein entire gravid females harboring infective eggs exit with lizard feces. Pogonomyrmex spp. harvester ants collect these females and feed them to their larvae, which are the only stages of the intermediate host that can become infected. We hypothesized that the seasonal dynamics of nematode abundance within lizard hosts would be correlated with the seasonal availability of suitable intermediate hosts. To describe seasonal variation of nematode population variables and elucidate the timing of critical events in the parasite life cycle, nematodes were collected from both hosts across three collection periods in the ant-and-lizard activity season of 2008 in the Alvord Basin of southeastern Oregon. Among 3 collection periods, and across the activity season, nematodes were harvested from individual Phrynosoma platyrhinos , and the distribution of developmental categories and body lengths of nematodes was analyzed to determine the seasonal change in nematode population composition. Pogonomyrmex spp. ants were collected in pit-fall traps and dissected to determine infection prevalence. The abundance of non-gravid female and juvenile nematodes collected from lizards' stomachs decreased significantly between the early and late collection period, which was likely a consequence of the sequential conversion of these developmental categories to gravid females. The presence of gravid female nematodes peaked in cloacal and fecal collections during mid-season. The body lengths of male nematodes increased as the activity season progressed, perhaps due to growth, but their abundance remained the same. Smaller juvenile nematodes were present in late-season collections from lizards, possibly indicating new acquisitions from infected ants. We propose that once a set population of male nematodes establishes in lizards' stomachs, newly acquired juvenile nematodes develop into non-gravid females that mate, become gravid females, and exit the lizard mid-season. We additionally suggest that the exit of females may be timed with the peak foraging activity of ant intermediate hosts and access to larval ants in the nests. Infection prevalence in the intermediate host was low, with only 1 of 6,000 dissected harvester ants containing a single larval nematode. The temporal dynamics of S. phrynosoma populations within P. platyrhinos at this northern locale is most likely driven by the seasonal availability of harvester ant intermediate hosts.     

TGF-beta and the evolution of nematode parasitism

The many similarities between arrested dauer larvae of free-living nematodes and infective L3 of parasitic nematodes has led to suggestions that they are analogous lifecycle stages. The control of the formation of dauer larvae in Caenorhabditis elegans is well understood, with a TGF-β-superfamily growth factor playing a central role. Recent analyses of the expression of homologous TGF-β genes in parasitic nematodes has allowed this analogy to be tested; but the results so far do not support it. Rather, the results imply that in the evolution of animal parasitism, parasitic nematodes have taken signalling pathways and molecules from their free-living ancestors and used them in different ways in the evolution of their parasitic lifestyles.     

Comparative and experimental embryogenesis of Plectidae (Nematoda)

Comparative analysis of early embryogenesis indicates that considerable differences exist among nematode species. To better understand to what extent the well-studied development of Caenorhabditis elegans is representative for nematodes in general, we extended our earlier studies to other families of this phylum. Here we report our findings on seven species of Plectidae. We found that Plectidae embryos share a number of developmental similarities with one branch of nematodes (Secernentea), including C. elegans, but not with the other branch (Adenophorea), and thus support conclusions concerning their phylogenetic position drawn from molecular data. However, Plectidae also show developmental differences to other Secernentea, suggesting an early separation from them. Prominent characteristics of Plectidae are (1) strict left-right divisions of somatic founder cells generating a prominent early bilateral symmetry and (2) a very early start of gastrulation with immigration of a single gut precursor cell. To determine whether gastrulation with two gut precursors is crucial for C. elegans embryos, we induced it to gastrulate with a single blastomere like in Plectidae. As this alteration is compatible with an essentially normal subsequent embryogenesis, cleavage of the gut precursor before gastrulation is obviously not required. As major differences exist among nematodes concerning the potential to compensate for eliminated early blastomeres, we tested this feature in one Plectus species. We found that Plectus does not replace a lost cell but behaves like C. elegansin this respect, in contrast to our previous findings in Acrobeloides nanus, another member of the Secernentea.     

Absence of Wolbachia in Nonfilariid Nematodes

Intracellular bacteria of the genus Wolbachia are among the most abundant endosymbionts on the planet, occurring in at least two major phyla-the Arthropoda and Nematoda. Current surveys of Wolbachia distribution have found contrasting patterns within these groups. Whereas Wolbachia are widespread and occur in all three major subphyla of arthropods, with estimates placing them in at least several million arthropod species, the presence of nematodes carrying Wolbachia is currently confined to the filariids, in which they occur at appreciable frequencies. It has been hypothesized that Wolbachia entered the ancestor of modern-day filariids in a single acquisition event, and subsequently cospeciated with their filariid hosts. To further investigate this hypothesis, we examined the broader distribution of Wolbachia in nematodes using a polymerase chain reaction (PCR) assay in a diverse set of nonfilariid species. The assay consisted of three different types of PCR screens on adults of 20 secernentean nematode species (14 rhabditids, 2 strongylid parasites of vertebrates; 1 diplogasterid; 3 cephalobid relatives, 1 myolaim, and 1 filariid) and two adenophorean species (plectids). Two PCR screens were specific to the 16S rDNA and ftsZ protein coding gene of Wolbachia; and the third screen was specific to the 18S rDNA of the nematodes. Based upon our results, we conclude that Wolbachia are absent in all 21 non-filariid species encompassing all the major groups of the Secernentea and two species of Adenophorea, from which the Secernentea derived. The absence of Wolbachia in these non-filariids is consistent with the hypothesis that Wolbachia entered the nematode phylum once, in an ancestral lineage of extant filariids.     

Information about transmission opportunities triggers a life-history switch in a parasite

Many microbial pathogens can switch to new hosts or adopt alternative transmission routes as environmental conditions change, displaying unexpected flexibility in their infection pathways and often causing emerging diseases. In contrast, parasitic worms that must develop through a fixed series of host species appear less likely to show phenotypic plasticity in their transmission pathways. Here, I demonstrate experimentally that a trematode parasite, Coitocaecum parvum, can accelerate its development and rapidly reach precocious maturity in its crustacean intermediate host in the absence of chemical cues emanating from its fish definitive host. Juvenile trematodes can also mature precociously when the mortality rate of their intermediate hosts is increased. Eggs produced by precocious adults hatch into viable larvae, capable of pursuing the parasite's life cycle. In the absence of chemical cues from fish hosts, the size of eggs released by precocious trematodes in their intermediate hosts becomes more variable, possibly indicating a bet-hedging strategy. These results illustrate that parasitic worms with complex life cycles have development and transmission strategies that are more plastic than commonly believed, allowing them to skip one host in their cycle when they perceive limited opportunities for transmission.     

Correlated evolution between host immunity and parasite life histories in primates and oxyurid parasites

Maturation time is a pivotal life-history trait of parasitic nematodes, determining adult body size, as well as daily and total fecundity. Recent theoretical work has emphasized the influence of prematurational mortality on the optimal values of age and size at maturity in nematodes. Eosinophils are a family of white blood cells often associated with infections by parasitic nematodes. Although the role of eosinophils in nematode resistance is controversial, recent work has suggested that the action of these immune effectors might be limited to the larval stages of the parasite. If eosinophils act on larval survival, one might predict, in line with theoretical models, that nematode species living in hosts with large eosinophil numbers should show reduced age and size at maturity. We tested this prediction using the association between the pinworms (Oxyuridae, Nematoda) and their primate hosts. Pinworms are highly host specific and are expected to be involved in a coevolutionary process with their hosts. We found that the body size of female parasites was negatively correlated with eosinophil concentration, whereas the concentration of two other leucocyte families-neutrophils and lymphocytes-was unrelated to female body size. Egg size of parasites also decreased with host eosinophil concentration, independently of female size. Male body size was unrelated to host immune parameters. Primates with the highest immune defence, therefore, harbour small female pinworms laying small eggs. These results are in agreement with theoretical expectations and suggest that life histories of oxyurid parasites covary with the immune defence of their hosts. Our findings illustrate the potential for host immune defence as a factor driving parasite life-history evolution.     

Ephemera strigata (Insecta: Ephemeroptera: Ephemeridae) is the intermediate host of the nematodes Rhabdochona denudata honshuensis and Rhabdochona coronacauda in Japan

Juvenile freshwater parasitic nematodes Rhabdochona denudata honshuensis Moravec and Nagasawa, 1989 and Rhabdochona coronacauda Belouss, 1965 (Spirurida: Thelazioidea: Rhabdochonidae) were found in mayfly nymphs collected in a mountain stream in Japan. Considering the relative density of mayfly nymphs, nematode prevalence, and intensity of parasitism, Ephemera strigata Eaton and Potamanthus formosus Ulmer (Ephemeroptera: Ephemeridae) are frequent natural intermediate hosts for R. d. honshuensis in this locality. The intermediate host of R. coronacauda also is the E. strigata nymph.     

Biological Control Potential of Neoaplectanid Nematodes

The neoaplectanids are among the most studied of all entomogenous nematodes. Because these nematodes kill their insect hosts, they are regarded as having excellent potential as biological control agents. While the host specificity of most entontogenous nematodes tends to limit their potential usefulness, the broad host range and high virulence of neoaplectanids make them attractive candidates for industrial development. Also, recent development of economical mass rearing procedures appears to make production on a commercial basis feasible. Infective stages may be stored for years trader various laboratory conditions. Although entomogenous nematodes, as parasites, are exempt from govermnent registration requirements, the mutualistic association of neoaplectanid nematodes with a bacterium will likely necessitate a detailed safety evaluation. Studies conducted to date indicate a lack of pathogenicity to mammals. Field trial success has been limited by the intolerance of infective stages to mffavorable environmental conditions, particularly low moisture. Applications against pests on exposed plant foliage have been especially disappointing. More encouraging anti consistent results have been obtained in more favorable environments, including soil and aquatic habitats, but the most promising treatment sites ntay be cryptic habitats where infective stages are shehered from environmental extremes. Cryptic habitats also exploit the ability of neoaplectanids to actively seek out hosts in recessed places where conventional insecticide applications are intpractical.     

A novel ascaroside controls the parasitic life cycle of the entomopathogenic nematode Heterorhabditis bacteriophora

Entomopathogenic nematodes survive in the soil as stress-resistant infective juveniles that seek out and infect insect hosts. Upon sensing internal host cues, the infective juveniles regurgitate bacterial pathogens from their gut that ultimately kill the host. Inside the host, the nematode develops into a reproductive adult and multiplies until unknown cues trigger the accumulation of infective juveniles. Here, we show that the entomopathogenic nematode Heterorhabditis bacteriophora uses a small-molecule pheromone to control infective juvenile development. The pheromone is structurally related to the dauer pheromone ascarosides that the free-living nematode Caenorhabditis elegans uses to control its development. However, none of the C. elegans ascarosides are effective in H. bacteriophora, suggesting that there is a high degree of species specificity. Our report is the first to show that ascarosides are important regulators of development in a parasitic nematode species. An understanding of chemical signaling in parasitic nematodes may enable the development of chemical tools to control these species.     

Pterygodermatites nycticebi infections in golden lion tamarins (Leontopithecus rosalia rosalia) and aye‐ayes (Daubentonia madagascariensis) from a German zoo

In a golden lion tamarin (Leontopithecus rosalia rosalia) colony kept indoors in a German zoo, two animals presented a sudden onset of reduced general condition, lethargy, and diarrhea. At animal capture for clinical examination, adult nematode stages were observed after stress‐induced defecation. Despite treatment, two golden lion tamarins died in the following 2 days. At necropsy, spirurid stages were found in the lungs and intestine. Additionally, adult Pterygodermatites spp. were identified in histopathological samples of intestine and pancreas, confirming the previous diagnosis. Upon diagnosis, all animals were treated with ivermectin (0.2 mg/kg; SC). Thereafter, the general condition of the golden lion tamarins improved, whereby some of them excreted spirurid nematodes over 3 days. Four weeks after treatment, 20 fecal samples from the colony were examined and proved negative for parasitic stages. Given that common German cockroaches (Blattella germanica) are suitable intermediate hosts of Pterygodermatites nycticebi, 30 specimens were collected from seven different locations around the golden lion tamarins housing. Third‐stage larvae of Pterygodermatites spp. were recovered from those cockroaches. Regular anthelmintic treatments, coprological screenings, and controls for intermediate hosts were recommended. More than 2 years later, P. nycticebi infection was diagnosed again histopathologically in an aye‐aye (Daubentonia madagascariensis) which suddenly died. Coprological analysis confirmed the presence of spirurid eggs. Due to prosimian primates' cockroach‐eating habits and given that total cockroach eradication proved impossible, continuous cockroach control strategies and regular treatments of primates are currently performed to prevent further P. nycticebi infections.     

Brief Review of the Associations of Xylobiont Nematodes with Bark Beetles (Coleoptera,Curculionidae: Scolytinae)

Nematode pathogens cause wilt diseases in conifers and deciduous trees. The longhorn beetles (Coleoptera: Cerambycidae) and bark beetles (Coleoptera: Curculionidae: Scolytinae) act as nematode vectors spreading the invasive juvenile stages during their maturation feeding or during oviposition on the plant hosts. There are numerous reviews of nematodes associated with bark beetles on conifers, while little attention has been paid to the nematodes of deciduous trees. The development of Dutch elm disease and ash dieback is mainly caused by fungal pathogens transmitted by bark beetles; the latter act as vectors of not only fungi but also nematodes enclosed in nematangia under their elytra, and also in the tracheae and Malpighian canals. Apart from phytopathogenic nematodes, bark beetles transmit mycophagous and bacterivorous nematodes and own parasites of bark beetles. The ecological groups of nematodes associated with Scolytinae are reviewed; the known records of associations of nematodes with bark beetles are listed for coniferous host plants of Russia and neighboring countries; the world-wide list of these associations for deciduous plant hosts is given.

     

Relationship between intermediate host taxon and infection by nematodes of the genus Rhabdochona

We describe the intermediate and definitive hosts of the fish nematodes Rhabdochona coronacauda and R. denudata honshuensis and discuss the relationships between parasitism and the feeding habitats of their intermediate hosts. We found that the principal intermediate hosts of the two nematodes were filter-feeding mayflies of the genera Ephemera, Photamanthus and Isonychia. Ephemera strigata seemed to be the most important intermediate host of these nematodes. Adult R. coronacauda were found mainly in Hemibarbus longirostris and Rhinogobius flumineus, which are benthic fishes that feed on benthic aquatic insects, including E. strigata. For R. coronacauda, therefore, the feeding habits of the definitive hosts facilitate host alternation by this species. However, adult R. denudata honshuensis were found in cyprinids. In particular, Zacco temmincki was the principal natural definitive host in our study area. Since Z. temmincki is a swimming predator, E. strigata nymphs that burrow in the substrate are not the main prey of this species. This indicates that the transmission of R. denudata honshuensis hardly occurs from E. strigata nymph to Z. temmincki, suggesting another, unknown transmission route.     

The host plant and the nematodes

Parasite selection by the host would be expected and is frequently found amongst the specialized plant parasitic nematodes and on perennial plants. Hijink & Oostenbrink (1968) showed that annual cropping could establish distinct nematode communities and such communities can become quickly established (Green, 1975). In carrot crops Aphelenchoides and Rotylenchus species became a larger proportion of the community very early in the growth of the crop (Green, 1976). Stabilization of communities in this way indicates a very close relationship between the nematodes and the host plants even when specialized feeding is not apparent. Cropping alters the plant community so that even these nematodes with a wide host range become dependant on the one host, provided weed control is efficient. Spacing of the crop further restricts the nematodes so they become more dependant on individual plants. Nematode attacks on crops are notable for two features. The hosts appear under-exploited, that is there are few individual hosts with many parasites but many with few and, the hosts are rarely killed.     

Metazoan parasites of African annual killifish (Nothobranchiidae): abundance,diversity, and their environmental correlates

Estimates of biodiversity and its global patterns are affected by parasite richness and specificity. Despite this, parasite communities are largely neglected in biodiversity estimates, especially in the tropics. We studied the parasites of annual killifish of the genus Nothobranchius that inhabit annually desiccating pools across the African savannah and survive the dry period as developmentally arrested embryos. Their discontinuous, non‐overlapping generations make them a unique organism in which to study natural parasite fauna. We investigated the relationship between global (climate and altitude) and local (pool size, vegetation, host density and diversity, and diversity of potential intermediate hosts) environmental factors and the community structure of killifish parasites. We examined metazoan parasites from 21 populations of four host species (Nothobranchius orthonotus, N. furzeri, N. kadleci, and N. pienaari) across a gradient of aridity in Mozambique. Seventeen parasite taxa were recorded, with trematode larval stages (metacercariae) being the most abundant taxa. The parasites recorded were both allogenic (life cycle includes non‐aquatic host; predominantly trematodes) and autogenic (cycling only in aquatic hosts; nematodes). The parasite abundance was highest in climatic regions with intermediate aridity, while parasite diversity was associated with local environmental characteristics and positively correlated with fish species diversity and the amount of aquatic vegetation. Our results suggest that parasite communities of sympatric Nothobranchius species are similar and dominated by the larval stages of generalist parasites. Therefore, Nothobranchius serve as important intermediate or paratenic hosts of parasites, with piscivorous birds and predatory fish being their most likely definitive hosts.     

食线虫真菌资源研究概况

食线虫真菌是指寄生、捕捉、定殖和毒害线虫的一类真菌,这类真菌是自然界中线虫种群控制的重要因子,也是动植物病害生物防治的重要研究材料,具有特殊的研究意义和经济价值。目前全世界共报道700余种食线虫真菌,包括捕食线虫真菌380余种,线虫内寄生真菌120余种,产毒真菌270余种和大量机会真菌。针对丰富的食线虫真菌资源,近年来世界各国尤其是中国科学家对其进行了广泛研究,在捕食线虫真菌资源的分类、系统进化、生态分布、有性无性联系等方面的研究取得了重要进展,在线虫内寄生真菌侵染宿主的方式及产毒真菌的次生代谢产物挖掘等方面也进行了广泛研究,文章综述了以上研究进展并简述了食线虫真菌资源的生物防治应用概况。     

Wolbachia filarial interactions

Wolbachia pipientis is a widespread intracellular bacterial symbiont of arthropods and is common in insects. One of their more exotic and unexpected hosts is the filarial nematodes, notable for the parasites responsible for onchocerciasis (river blindness), lymphatic filariasis (elephantiasis) and dirofilariasis (heartworm). Wolbachia are only present in a subgroup of the filarial nematodes and do not extend to other groups of nematodes either parasitic or free‐living. In the medically and veterinary important species that host Wolbachia, the symbiont has become an essential partner to key biological processes in the life of the nematode to the point where antibiotic elimination of the bacteria leads to a potent and effective anti‐filarial drug treatment. We review the cellular and molecular basis of Wolbachia filarial interactions and highlight the key processes provided by the endosymbiont upon which the nematodes have become entirely dependent. This dependency is primarily restricted to periods of the lifecycle with heavy metabolic demands including growth and development of larval stages and embryogenesis in the adult female. Also, the longevity of filarial parasites is compromised following depletion of the symbiont, which for the first time has delivered a safe and effective treatment to kill adult parasites with antibiotics.