Nematode endoparasites do not codiversify with their stick insect hosts

Host–parasite coevolution stems from reciprocal selection on host resistance and parasite infectivity, and can generate some of the strongest selective pressures known in nature. It is widely seen as a major driver of diversification, the most extreme case being parallel speciation in hosts and their associated parasites. Here, we report on endoparasitic nematodes, most likely members of the mermithid family, infecting different Timema stick insect species throughout California. The nematodes develop in the hemolymph of their insect host and kill it upon emergence, completely impeding host reproduction. Given the direct exposure of the endoparasites to the host's immune system in the hemolymph, and the consequences of infection on host fitness, we predicted that divergence among hosts may drive parallel divergence in the endoparasites. Our phylogenetic analyses suggested the presence of two differentiated endoparasite lineages. However, independently of whether the two lineages were considered separately or jointly, we found a complete lack of codivergence between the endoparasitic nematodes and their hosts in spite of extensive genetic variation among hosts and among parasites. Instead, there was strong isolation by distance among the endoparasitic nematodes, indicating that geography plays a more important role than host‐related adaptations in driving parasite diversification in this system. The accumulating evidence for lack of codiversification between parasites and their hosts at macroevolutionary scales contrasts with the overwhelming evidence for coevolution within populations, and calls for studies linking micro‐ versus macroevolutionary dynamics in host–parasite interactions.     

Virulence and competitive ability in an obligately killing parasite

Mixed infections are thought to have a major influence on the evolution of parasite virulence. During a mixed infection, higher within‐host parasite growth is favored under the assumption that it is critical to the competitive success of the parasite. As within‐host parasite growth may also increase damage to the host, a positive correlation is predicted between virulence and competitive success. However, when parasites must kill their hosts in order be transmitted, parasites may spend energy on directly attacking their host, even at the cost of their within‐host growth. In such systems, a negative correlation between virulence and competitive success may arise. We examined virulence and competitive ability in three sympatric species of obligately killing nematode parasites in the genus Steinernema. These nematodes exist in a mutualistic symbiosis with bacteria in the genus Xenorhabdus. Together the nematodes and their bacteria kill the insect host soon after infection, with reproduction of both species occurring mainly after host death. We found significant differences among the three nematode species in the speed of host killing. The nematode species with the lowest and highest levels of virulence were associated with the same species of Xenorhabdus, indicating that nematode traits, rather than the bacterial symbionts, may be responsible for the differences in virulence. In mixed infections, host mortality rate closely matched that associated with the more virulent species, and the more virulent species was found to be exclusively transmitted from the majority of coinfected hosts. Thus, despite the requirement of rapid host death, virulence appears to be positively correlated with competitive success in this system. These findings support a mechanistic link between parasite growth and both anti‐competitor and anti‐host factors.     

Extracellular vesicles released by anaerobic protozoan parasites: Current situation

Extracellular vesicles (EVs) have emerged as a ubiquitous mechanism for transferring information between cells and organisms across all three kingdoms of life. Parasitic unicellular eukaryotes use EVs as vehicles for intercellular communication and host manipulation. Pathogenic protozoans are able to modulate the immune system of the host and establish infection by transferring a wide range of molecules contained in different types of EVs. In addition to effects on the host, EVs are able to transfer virulence factors, drug‐resistance genes and differentiation factors between parasites. In this review we cover the current knowledge on EVs from anaerobic or microaerophilic extracellular protozoan parasites, including Trichomonas vaginalis, Tritrichomonas foetus, Giardia intestinalis and Entamoeba histolytica, with a focus on their potential role in the process of infection. The role of EVs in host: parasite communication adds a new level of complexity to our understanding of parasite biology, and may be a key to understand the complexity behind their mechanism of pathogenesis.     

The influence of a parasite community on the dynamics of a host population: a longitudinal study on willow ptarmigan and their parasites

Despite the fact that most host populations are infected by a community of different parasite species, the majority of empirical studies have focused on the interaction between the host and a single parasite species. Here, we explore the hypothesis that host population dynamics are affected both by single parasite species and by the whole parasite community. We monitored population density and breeding productivity of two populations of willow ptarmigan ( Lagopus lagopus ) in northern Norway for 8 and 11 years, respectively, and sampled eukaryotic endoparasites. We found that increasing abundances of the cestode Hymenolepis microps was associated with increased breeding mortality and reduced annual growth rate of the host population in both areas, and reduced host body mass and body condition in the area where such data were available. In one of the areas, the abundance of the nematode Trichostrongylus tenuis was associated with reductions in host body mass, body condition and breeding mortality and the filaroid nematode Splendidofilaria papillocerca was negatively related to host population growth rates. The parasite community was also negatively related to host fitness parameters, suggesting an additional community effect on host body mass and breeding mortality, although none of the parasites had a significant impact on their own. The prevalence of parasites with very different taxonomical origins tended to covary within years, suggesting that variability in the parasite community was not random, but governed by changes in host susceptibility or environmental conditions that affected exposure to parasites in general. Other variables including climate, plant production and rodent densities were not associated with the recorded demographic changes in the host population.     

Metabarcoding options to study eukaryotic endoparasites of birds

There is growing interest in the study of avian endoparasite communities, and metabarcoding is a promising approach to complement more conventional or targeted methods. In the case of eukaryotic endoparasites, phylogenetic diversity is extreme, with parasites from 4 kingdoms and 11 phyla documented in birds. We addressed this challenge by comparing different primer sets across 16 samples from 5 bird species. Samples consisted of blood, feces, and controlled mixes with known proportions of bird and nematode DNA. Illumina sequencing revealed that a 28S primer set used in combination with a custom blocking primer allowed detection of various plasmodiid parasites and filarioid nematodes in the blood, coccidia in the feces, as well as two potentially pathogenic fungal groups. When tested on the controlled DNA mixes, these primers also increased the proportion of nematode DNA by over an order of magnitude. An 18S primer set, originally designed to exclude metazoan sequences, was the most effective at reducing the relative number of avian DNA sequences and was the only one to detect Trypanosoma in the blood. Expectedly, however, it did not allow nematode detection and also failed to detect avian malaria parasites. This study shows that a 28S set including a blocking primer allows detection of several major and very diverse bird parasite clades, while reliable amplification of all major parasite groups may require a combination of markers. It helps clarify options for bird parasite metabarcoding, according to priorities in terms of the endoparasite clades and the ecological questions researchers wish to focus on.     

Effectively vertical transmission of a Drosophila‐parasitic nematode: mechanism and consequences

1. Long‐term control of insects by parasites is possible only if the parasite populations persist. Because parasite transmission rate depends on host density, parasite populations may go extinct during periods of low host density. Vertical transmission of parasites, however, is independent of host density and may therefore provide a demographic bridge through times when their insect hosts are rare. 2. The nematode Howardula aoronymphium, which parasitises mycophagous species of Drosophila, can experience both horizontal and effectively vertical transmission, relative rates of which depend, in theory at least, on the density of hosts at breeding sites. 3. A nine‐generation experiment was carried out in which nematodes were transmitted either exclusively vertically or primarily horizontally. This experiment revealed that these parasites can persist and exhibit positive population growth even when there is only vertical transmission. 4. Assays at the end of the experiment revealed that the vertically transmitted nematodes had suffered no inbreeding depression and that they were similar to the horizontally transmitted nematodes in terms of virulence, infectivity, within‐host growth rate, and fecundity. Thus, vertical transmission of H. aoronymphium did not appear to compromise the ability of these parasites to control Drosophila populations.     

The role of the European bitterling (<Emphasis Type="Italic">Rhodeus amarus,</Emphasis> Cyprinidae) in parasite accumulation and transmission in riverine ecosystems

In aquatic ecosystems, fish play a key role in parasite accumulation and transmission to predacious animals. In the present study, realized on seven populations of a small cyprinid fish species, the European bitterling Rhodeus amarus, we investigated (1) the role of the European bitterling as a potential intermediate or paratenic host, (2) the ability of the fish to accumulate parasites with similar final host group, and (3) its significance as a potential source of parasite infection in the ecosystem in respect to habitat characteristics. A total of 36 parasite species were recorded; 31 species (90% of all parasite specimens) were classified as endoparasites. Most of the endoparasites were found in the larval life stage, using bitterling as an intermediate or paratenic host. In particular, parasite community structure showed significantly higher proportions of allogenic parasites in comparison with autogenic. The supposed co-occurrence of parasite species with identical final host groups showed only a weak association. The adjacent reservoir areas were a significant determinant of both the total and infracommunity parasite species richness and for the mean parasite abundance. No relationship between the distance of sampling site from the adjacent reservoir and parasite community characteristics was found. As a small-sized fish with a wide distribution range and high local abundances, the European bitterling can represent a natural prey for a wide range of piscivorous predators. Due to its susceptibility to the number of larval endoparasites, this fish species may therefore fulfill the role as important transmitter of parasites to their final hosts.     

Ecological implications of parasites in natural <Emphasis Type="Italic">Daphnia</Emphasis> populations

In natural host populations, parasitism is considered to be omnipresent and to play an important role in shaping host life history and population dynamics. Here, we study parasitism in natural populations of the zooplankton host Daphnia magna investigating their individual and population level effects during a 2-year field study. Our results revealed a rich and highly prevalent community of parasites, with eight endoparasite species (four microsporidia, one amoeba, two bacteria and one nematode) and six epibionts (belonging to five different taxa: Chlorophyta, Bacillariophyceae, Ciliata, Fungi and Rotifera). Several of the endoparasites were associated with a severe overall fecundity reduction of the hosts, while such effects were not seen for epibionts. In particular, infections by Pasteuria ramosa, White Fat Cell Disease and Flabelliforma magnivora were strongly associated with a reduction in overall D. magna fecundity. Across the sampling period, average population fecundity of D. magna was negatively associated with overall infection intensity and total endoparasite richness. Population density of D. magna was negatively correlated to overall endoparasite prevalence and positively correlated with epibiont richness. Finally, the reduction in host fecundity caused by different parasite species was negatively correlated to both parasite prevalence and the length of the time period during which the parasite persisted in the host population. Consistent with epidemiological models, these results indicate that parasite mediated host damages influence the population dynamics of both hosts and parasites.     

The role of programmed cell death in Plasmodium–mosquito interactions

Many host–parasite interactions are regulated in part by the programmed cell death of host cells or the parasite. Here we review evidence suggesting that programmed cell death occurs during the early stages of the development of the malaria parasite in its vector. Zygotes and ookinetes of Plasmodium berghei have been shown to die by programmed cell death (apoptosis) in the midgut lumen of the vector Anopheles stephensi, or whilst developing in vitro. Several morphological markers, indicative of apoptosis, are described and evidence for the involvement of a biochemical pathway involving cysteine proteases discussed in relationship to other protozoan parasites. Malaria infection induces apoptosis in the cells of two mosquito tissues, the midgut and the follicular epithelium. Observations on cell death in both these tissues are reviewed including the role of caspases as effector molecules and the rescue of resorbing follicles resulting from inhibition of caspases. Putative signal molecules that might induce parasite and vector apoptosis are suggested including nitric oxide, reactive nitrogen intermediates, oxygen radicals and endocrine balances. Finally, we suggest that programmed cell death may play a critical role in regulation of infection by the parasite and the host, and contribute to the success or not of parasite establishment and host survival.     

Host–parasite interactions and vectors in the barn swallow in relation to climate change

Recent climate change has affected the phenology of numerous species, and such differential changes may affect host–parasite interactions. Using information on vectors (louseflies, mosquitoes, blackflies) and parasites (tropical fowl mite Ornithonyssus bursa, the lousefly Ornithomyia avicularia, a chewing louse Brueelia sp., two species of feather mites Trouessartia crucifera and Trouessartia appendiculata, and two species of blood parasites Leucozytozoon whitworthi and Haemoproteus prognei) of the barn swallow Hirundo rustica collected during 1971–2008, I analyzed temporal changes in emergence and abundance, relationships with climatic conditions, and changes in the fitness impact of parasites on their hosts. Temperature and rainfall during the summer breeding season of the host increased during the study. The intensity of infestation by mites decreased, but increased for the lousefly during 1982–2008. The prevalence of two species of blood parasites increased during 1988–2008. The timing of first mass emergence of mosquitoes and blackflies advanced. These temporal changes in phenology and abundance of parasites and vectors could be linked to changes in temperature, but less so to changes in precipitation. Parasites had fitness consequences for hosts because intensity of the mite and the chewing louse was significantly associated with delayed breeding of the host, while a greater abundance of feather mites was associated with earlier breeding. Reproductive success of the host decreased with increasing abundance of the chewing louse. The temporal decrease in mite abundance was associated with advanced breeding of the host, while the increase in abundance of the lousefly was associated with earlier breeding. Virulence by the tropical fowl mite decreased with increasing temperature, independent of confounding factors. These findings suggest that climate change affects parasite species differently, hence altering the composition of the parasite community, and that climate change causes changes in the virulence of parasites. Because the changing phenology of different species of parasites had both positive and negative effects on their hosts, and because the abundance of some parasites increased, while that of other decreased, there was no consistent temporal change in host fitness during 1971–2008.     

Differential impacts of shared parasites on fitness components among competing hosts

Effects of parasites on individual hosts can eventually translate to impacts on host communities. In particular, parasitism can differentially affect host fitness among sympatric and interacting host species. We examined whether the impact of shared parasites varied among host species within the same community. Specifically, we looked at the impacts of the acanthocephalan Acanthocephalus galaxii, the trematodes Coitocaecum parvum and Maritrema poulini, and the nematode Hedruris spinigera, on three host species: the amphipods, Paracalliope fluviatilis and Paracorophium excavatum, and the isopod, Austridotea annectens. We assessed parasite infection levels in the three host species and tested for effects on host survival, behavior, probability of pairing, and fecundity. Maritrema poulini and C. parvum were most abundant in P. excavatum but had no effect on its survival, whereas they negatively affected the survival of P. fluviatilis, the other amphipod. Female amphipods carrying young had higher M. poulini and C. parvum abundance than those without, yet the number of young carried was not linked to parasite abundance. Behavior of the isopod A. annectens was affected by M. poulini infection; more heavily infected individuals were more active. Paracorophium excavatum moved longer distances when abundance of C. parvum was lower, yet no relationship existed with respect to infection by both M. poulini and C. parvum. The differential effects of parasites on amphipods and isopods may lead to community‐wide effects. Understanding the consequences of parasitic infection and differences among host species is key to gaining greater insight into the role of parasite mediation in ecosystem dynamics.     

HOST GROWTH CONDITIONS INFLUENCE EXPERIMENTAL EVOLUTION OF LIFE HISTORY AND VIRULENCE OF A PARASITE WITH VERTICAL AND HORIZONTAL TRANSMISSION

In parasites with mixed modes of transmission, ecological conditions may determine the relative importance of vertical and horizontal transmission for parasite fitness. This may lead to differential selection pressure on the efficiency of the two modes of transmission and on parasite virulence. In populations with high birth rates, increased opportunities for vertical transmission may select for higher vertical transmissibility and possibly lower virulence. We tested this idea in experimental populations of the protozoan Paramecium caudatum and its bacterial parasite Holospora undulata. Serial dilution produced constant host population growth and frequent vertical transmission. Consistent with predictions, evolved parasites from this “high‐growth” treatment had higher fidelity of vertical transmission and lower virulence than parasites from host populations constantly kept near their carrying capacity (“low‐growth treatment”). High‐growth parasites also produced fewer, but more infectious horizontal transmission stages, suggesting the compensation of trade‐offs between vertical and horizontal transmission components in this treatment. These results illustrate how environmentally driven changes in host demography can promote evolutionary divergence of parasite life history and transmission strategies.     

Intestinal Parasites of Free-ranging,Semicaptive,and Captive <Emphasis Type="Italic">Pongo abelii</Emphasis> in Sumatra,Indonesia

We collected fecal samples from 32 free-ranging, 19 semicaptive, and 54 captive Sumatran orangutans on Sumatra from 1998 until 2004 and screened them for gastrointestinal parasites. Our objectives were to compare the intestinal parasites of free-ranging, semicaptive, and captive orangutans and to evaluate the risk of parasite transmission in orangutan reintroduction programs. We identified 4 genera of Protozoa, 7 genera of nematodes, 1 trematode sp., and 1 cestode sp. The prevalence of Balantidium coli in free-ranging orangutans was significantly higher than in captive individuals. However, the prevalence of Strongyloides sp. was higher in captive than in free-ranging orangutans. Free-ranging female orangutans had a significantly higher total prevalence of intestinal parasites than that of males. We found no significant difference between parasite prevalences in different age groups. Compared to gorillas and chimpanzees, orangutans carry a smaller variety of protozoan and nematode species. Strongyloides sp. infections form the highest risk in reintroduction programs as crowding, ground-dwelling, and poor hygiene in captive and semicaptive orangutans may cause a constant reinfection.     

Effects of resource availability and social aggregation on the species richness of raccoon endoparasite infracommunities

Within populations the contact rate of hosts and infectious parasites is mediated by the interactions of resource availability, host density, and host behavior. Fluctuations in host density can result in the loss or extinction of a parasite population as contact rates between parasites and susceptible individuals drop below thresholds of parasite population persistence. Less understood is how changes in resources and the behavioral ecology of host populations affect parasites. We used food provisioning to experimentally assess the effects of resource availability and of inducing host aggregation on the endoparasite community of free‐ranging raccoons. Twelve independent raccoon populations were subjected to differential resource provisioning for two years: a clumped food distribution to aggregate hosts (n = 5 populations), a dispersed food distribution to add food without aggregating hosts (n = 3), and a no food treatment (n = 4). Remote cameras indicated that aggregation sizes were three to four times greater in aggregated versus non‐aggregated populations. We considered endoparasites with direct and indirect life cycles separately and determined the best‐fit models of parasite species richness in relation to host aggregation, food supplements, and host age and sex. Social aggregation had a negligible impact on the species richness of directly or indirectly transmitted parasites. However, food additions decreased the number of indirectly transmitted parasite species by 35% in the oldest age classes. These results suggest that while resource availability can influence the transmission of indirectly transmitted parasites, an examination of additional factors will be necessary to understand the role of host contact and factors that shape the community structure of endoparasites in natural environments.     

Temperature and multiple parasites combine to alter host community structure

Predicting the effects of climate change requires understanding complex interactions among multiple abiotic and biotic factors. By influencing key interactions among host species, parasites can affect community and ecosystem structuring. Yet, our understanding of how multiple parasites and abiotic factors interact to alter ecosystem structure remains limited. To empirically test the role of temperature variation and parasites in shaping communities, we used a multigenerational mesocosm experiment composed of four sympatric freshwater crustacean species (isopods and amphipods) that share up to four parasite species. Mesocosms were assigned to one of four different treatments with contrasting seasonal temperatures (normal and elevated) and parasite exposure levels (continuous and arrested (presence or absence of parasite larvae in mesocosm)). We found that parasite exposure and water temperature had interactive effects on the host community. Continuous exposure to parasites altered the community structure and differences in water temperature altered species abundance. The abundance of the amphipod Paracalliope fluviatilis decreased substantially when experiencing continuous parasite exposure and elevated water temperatures. Elevated temperatures also led to parasite-induced mortality in another amphipod host, Paracorophium excavatum. Contrastingly, isopod hosts were affected much less, suggesting increasing temperatures in conjunction with higher parasite exposure might increase their relative abundance in the community. Changes in invertebrate host populations have implications for other species such as fish and birds that consume crustaceans as well as having impacts on ecosystem processes, such as aquatic primary production and nutrient cycling. In light of climate change predictions, parasite exposure and rise in average temperatures may have substantial impacts on communities and ecosystems, altering ecosystem structure and dynamics.     

The Truman Show for protozoan parasites: A review of in vitro cultivation platforms

Protozoan parasites are responsible for severe disease and suffering in humans worldwide. Apart from disease transmission via insect vectors and contaminated soil, food, or water, transmission may occur congenitally or by way of blood transfusion and organ transplantation. Several recent outbreaks associated with fresh produce and potable water emphasize the need for vigilance and monitoring of protozoan parasites that cause severe disease in humans globally. Apart from the tropical parasite Plasmodium spp., other protozoa causing debilitating and fatal diseases such as Trypanosoma spp. and Naegleria fowleri need to be studied in more detail. Climate change and socioeconomic issues such as migration continue to be major drivers for the spread of these neglected tropical diseases beyond endemic zones. Due to the complex life cycles of protozoa involving multiple hosts, vectors, and stringent growth conditions, studying these parasites has been challenging. While in vivo models may provide insights into host–parasite interaction, the ethical aspects of laboratory animal use and the challenge of ready availability of parasite life stages underline the need for in vitro models as valid alternatives for culturing and maintaining protozoan parasites. To our knowledge, this review is the first of its kind to highlight available in vitro models for protozoa causing highly infectious diseases. In recent years, several research efforts using new technologies such as 3D organoid and spheroid systems for protozoan parasites have been introduced that provide valuable tools to advance complex culturing models and offer new opportunities toward the advancement of parasite in vitro studies. In vitro models aid scientists and healthcare providers in gaining insights into parasite infection biology, ultimately enabling the use of novel strategies for preventing and treating these diseases.     

Effect of juvenile hormone analog in a natural host-parasite system

Hormones mediate the physiological responses of animals to environmental changes. Consequently, hormones can be responsible of trade offs between different life history traits. Juvenile hormone (JH) is thought to mediate resource allocation in insects: specifically, it is thought to enhance the expression of condition-related traits like sexual signals, whilst reducing immune responsiveness. Here, we experimentally test whether a JH analog (JHa) had an effect on immunity of male dragonflies Celithemis eponina, and if such effects are translated into faster growth or development of a natural parasite (water mite). We also tested the effects of JHa on host condition (muscular mass and fat reserves) of mature male dragonflies. Mites from JHa treated dragonflies grew faster than mites from control dragonflies receiving just an acetone carrier. However, there was no effect of JHa on measures of host immune response (melanization of a nylon implant) or condition of mature males. We suggest that better parasite growth in JHa treated males does not result from the JH immunosuppressive function, but instead it appears that parasites receive hormone signals from the host and alter their development without affecting host condition measurably. Our work highlights the importance of measuring both immune parameters and response to real parasites when studying evolutionary trade offs.     

Predators and trematode parasites jointly affect larval anuran functional traits and corticosterone levels

Non‐consumptive predator effects may have dramatic consequences for host–parasite interactions by influencing the ability of prey items to avoid, resist, or tolerate infection. Both predators and parasites can affect host traits, such as growth rates and behavior, and these effects may in part be mediated through shared physiological pathways (e.g. the glucocorticoid stress hormone, corticosterone [CORT]). Here, we examined the effects of trematode parasites (Digena: Echinostomatidae) and predator (larval odonate) exposure on larvae of two amphibian species (Rana sylvatica and R. clamitans) in laboratory experiments. First, we measured behavior and CORT responses of tadpoles exposed to predator chemical cue in combination with parasite cue or under direct exposure to parasites. We then measured the combined effects of predator cue and parasite infection on survival and traits. Evidence for effects of parasite cue in our study was equivocal, but we found novel interactive effects of parasites and predators on larval frogs. Parasites and predators had antagonistic effects on CORT, behavior, and morphology, and negative synergistic effects on development. In addition, parasite infection and predator cues additively reduced activity levels of both species and growth in wood frogs. Negative effects of parasite infection on survival and traits were dose‐dependent for both species, although wood frogs generally experienced stronger effects of infection than green frogs. Our results emphasize the importance of considering effects of parasites as well as predators, since both can have strong effects on survival and the combination can have both additive and non‐additive effects on key traits. These effects likely have important implications for amphibian population dynamics, community structure, and conservation.     

Heydenius araneus n.sp. (Nematoda: Mermithidae), a parasite of a fossil spider, with an examination of helminths from extant spiders (Arachnida: Araneae)

Abstract. A mermithid, a parasite of a spider (Araneae: Thomisidae) in Baltic amber (40 mya), is described as Heydenius araneus n.sp. (Nematoda: Mermithidae) and represents the first fossil record of a nematode parasite of an arachnid. After a critical examination of reports of naturally occurring helminths of extant spiders, I conclude that although mermithid parasitism is well established in this host group, previous reports of hairworm parasites of spiders are "nomina dubia," putative records, or refer to mermithid nematodes.