The parasitic Nematomorph hairworm, Spinochordodes tellinii (Camerano) develops inside the terrestrial grasshopper, Meconema thalassinum (De Geer) (Orthoptera: Tettigoniidae), changing the insect's responses to water. The resulting aberrant behaviour makes infected insects more likely to jump into an aquatic environment where the adult parasite reproduces. We used proteomics tools (i.e. two-dimensional gel electrophoresis (2-DE), computer assisted comparative analysis of host and parasite protein spots and MALDI-TOF mass spectrometry) to identify these proteins and to explore the mechanisms underlying this subtle behavioural modification. We characterized simultaneously the host (brain) and the parasite proteomes at three stages of the manipulative process, i.e. before, during and after manipulation. For the host, there was a differential proteomic expression in relation to different effects such as the circadian cycle, the parasitic status, the manipulative period itself, and worm emergence. For the parasite, a differential proteomics expression allowed characterization of the parasitic and the free-living stages, the manipulative period and the emergence of the worm from the host. The findings suggest that the adult worm alters the normal functions of the grasshopper's central nervous system (CNS) by producing certain ‘effective’ molecules. In addition, in the brain of manipulated insects, there was found to be a differential expression of proteins specifically linked to neurotransmitter activities. The evidence obtained also suggested that the parasite produces molecules from the family Wnt acting directly on the development of the CNS. These proteins show important similarities with those known in other insects, suggesting a case of molecular mimicry. Finally, we found many proteins in the host's CNS as well as in the parasite for which the function(s) are still unknown in the published literature (www) protein databases. These results support the hypothesis that host behavioural changes are mediated by a mix of direct and indirect chemical manipulation.
extended phenotype; parasite–host systems; parasite manipulation; proteomics
Competition between parasites within a host can influence the evolution of parasite virulence and host resistance, but few studies examine the effects of unrelated parasites with conflicting transmission strategies infecting the same host. Vertically transmitted (VT) parasites, transmitted from mother to offspring, are in conflict with virulent, horizontally transmitted (HT) parasites, because healthy hosts are necessary to maximize VT parasite fitness. Resolution of the conflict between these parasites should lead to the evolution of one of two strategies: avoidance, or sabotage of HT parasite virulence by the VT parasite. We investigated two co-infecting parasites in the amphipod host, Gammarus roeseli: VT microsporidia have little effect on host fitness, but acanthocephala modify host behaviour, increasing the probability that the amphipod is predated by the acanthocephalan's definitive host. We found evidence for sabotage: the behavioural manipulation induced by the Acanthocephala Polymorphus minutus was weaker in hosts also infected by the microsporidia Dictyocoela sp. (roeselum) compared to hosts infected by P. minutus alone. Such conflicts may explain a significant portion of the variation generally observed in behavioural measures, and since VT parasites are ubiquitous in invertebrates, often passing undetected, conflict via transmission may be of great importance in the study of host–parasite relationships.
Acanthocephala; microsporidia; Gammarus roeseli; conflict; parasite transmission; behavioural manipulation
Parasite infections often induce a reduction in host immune response either because of a direct manipulation of the immune system by the parasite or because of energy depletion. Although infection-induced immunodepression can favour the establishment of the parasite within the host, a too severe immunodepression may increase the risk of infection with opportunistic pathogens, stopping the period over which the parasite can be transmitted to other hosts. Here, we explore how the risk of contracting opportunistic diseases affects the survival of the amphipod Gammarus pulex infected by the acanthocephalan Pomphorhynchus laevis. Previous work with this system has shown that upon infection, G. pulex has a substantially reduced immune response. Non-infected and P. laevis-infected hosts were maintained either in control or in micro-organism-enriched water, so as to vary the risk of encountering opportunistic pathogens. As predicted, we found that host mortality was exacerbated when infected gammarids were maintained in micro-organism-enriched water compared with clean, control water; whereas for non-infected gammarids, living in micro-organism-enriched water only moderately increased the risk of mortality. These results show that the virulence of parasites that reduce the host immune response is an environmentally sensitive trait that depends on the concomitant risk for the host of contracting opportunistic diseases. This extra source of host mortality probably represents a cost for P. laevis, and we tentatively predict that the optimal level of parasite exploitation should depend on environmental conditions.
disease ecology; Pomphorhynchus laevis; immunodepression; opportunistic pathogens; virulence
For parasites with complex life cycles, size at transmission can impact performance in the next host, thereby coupling parasite phenotypes in the two consecutive hosts. However, a handful of studies with parasites, and numerous studies with free-living, complex-life-cycle animals, have found that larval size correlates poorly with fitness under particular conditions, implying that other traits, such as physiological or ontogenetic variation, may predict fitness more reliably. Using the tapeworm Schistocephalus solidus, we evaluated how parasite size, age, and ontogeny in the copepod first host interact to determine performance in the stickleback second host.
We raised infected copepods under two feeding treatments (to manipulate parasite growth), and then exposed fish to worms of two different ages (to manipulate parasite ontogeny). We assessed how growth and ontogeny in copepods affected three measures of fitness in fish: infection probability, growth rate, and energy storage.
Our main, novel finding is that the increase in fitness (infection probability and growth in fish) with larval size and age observed in previous studies on S. solidus seems to be largely mediated by ontogenetic variation. Worms that developed rapidly (had a cercomer after 9 days in copepods) were able to infect fish at an earlier age, and they grew to larger sizes with larger energy reserves in fish. Infection probability in fish increased with larval size chiefly in young worms, when size and ontogeny are positively correlated, but not in older worms that had essentially completed their larval development in copepods.
Transmission to sticklebacks as a small, not-yet-fully developed larva has clear costs for S. solidus, but it remains unclear what prevents the evolution of faster growth and development in this species.
Cercomer; Cestoda; Complex life cycle; Energy allocation; Glycogen; Life history tradeoff; Metamorphosis; Plerocercoid; Procercoid
Nematodes comprise a large phylum of both free-living and parasitic species that show remarkably diverse lifestyles, ecological niches, and behavioral repertoires. Parasitic species in particular often display highly specialized host-seeking behaviors that reflect their specific host preferences. Many host-seeking behaviors can be triggered by the presence of host odors, yet little is known about either the specific olfactory cues that trigger these behaviors or the neural circuits that underlie them. Heterorhabditis bacteriophora and Steinernema carpocapsae are phylogenetically distant insect-parasitic nematodes whose host-seeking and host-invasion behavior resembles that of some of the most devastating human- and plant-parasitic nematodes. Here we compare the olfactory responses of H. bacteriophora and S. carpocapsae infective juveniles (IJs) to those of Caenorhabditis elegans dauers, which are analogous life stages . We show that the broad host range of these parasites results from their ability to respond to the universally-produced signal carbon dioxide (CO2) as well as a wide array of odors, including host-specific odors that we identified using TD-GC-MS. We show that CO2 is attractive for the parasitic IJs and C. elegans dauers despite being repulsive for C. elegans adults [2–4], and we identify an ancient and conserved sensory neuron that mediates CO2 response in both parasitic and free-living species regardless of whether CO2 is an attractive or a repulsive cue. Finally, we show that the parasites’ odor response profiles are more similar to each other than to that of C. elegans despite their greater phylogenetic distance, likely reflecting evolutionary convergence to insect parasitism. Our results suggest that the olfactory responses of parasitic versus free-living nematodes are highly diverse and that this diversity is critical to the evolution of nematode behavior.
Pathogens and parasites can induce changes in host or vector behavior that enhance their transmission. In plant systems, such effects are largely restricted to vectors, because they are mobile and may exhibit preferences dependent upon plant host infection status. Here we report the first evidence that acquisition of a plant virus directly alters host selection behavior by its insect vector. We show that the aphid Rhopalosiphum padi, after acquiring Barley yellow dwarf virus (BYDV) during in vitro feeding, prefers noninfected wheat plants, while noninfective aphids also fed in vitro prefer BYDV-infected plants. This behavioral change should promote pathogen spread since noninfective vector preference for infected plants will promote acquisition, while infective vector preference for noninfected hosts will promote transmission. We propose the “Vector Manipulation Hypothesis” to explain the evolution of strategies in plant pathogens to enhance their spread to new hosts. Our findings have implications for disease and vector management.
Success of trophically transmitted parasites depends to a great extent on their ability to manipulate their intermediate hosts in a way that makes them easier prey for target hosts. Parasite-induced behavioural changes are the most spectacular and diverse examples of manipulation. Most of the studies have been focused on individual behaviour of hosts including fish. We suggest that agonistic interactions and territoriality in fish hosts may affect their vulnerability to predators and thus the transmission efficiency of trophically transmitted parasites. The parasite Diplostomum spathaceum (Trematoda) and juvenile rainbow trout, Oncorhynchus mykiss, were used to study whether infection can alter aggression rates and territorial behaviour of intermediate fish hosts.
The changes in behaviour of rainbow trout, Oncorhynchus mykiss, infected with an eye fluke Diplostomum spathaceum (Trematoda), was monitored over the course of an experimental infection for 1.5 months. At the beginning of their development, not yet infective D. spathaceum metacercariae decreased the aggressiveness of rainbow trout. By the time that metacercariae were fully infective to their definitive hosts, the aggressiveness increased and exceeded that of control fish. Despite the increased aggressiveness, the experimentally infected fish lost contests for a territory (dark parts of the bottom) against the control fish.
The results obtained indicate that the parasitized fish pay the cost of aggressiveness without the benefit of acquiring a territory that would provide them with better protection against predators. This behaviour should increase transmission of the parasite as expected by the parasite manipulation hypothesis.
The highly prevalent parasite Toxoplasma gondii manipulates its host's behavior. In infected rodents, the behavioral changes increase the likelihood that the parasite will be transmitted back to its definitive cat host, an essential step in completion of the parasite's life cycle. The mechanism(s) responsible for behavioral changes in the host is unknown but two lines of published evidence suggest that the parasite alters neurotransmitter signal transduction: the disruption of the parasite-induced behavioral changes with medications used to treat psychiatric disease (specifically dopamine antagonists) and identification of a tyrosine hydroxylase encoded in the parasite genome. In this study, infection of mammalian dopaminergic cells with T. gondii enhanced the levels of K+-induced release of dopamine several-fold, with a direct correlation between the number of infected cells and the quantity of dopamine released. Immunostaining brain sections of infected mice with dopamine antibody showed intense staining of encysted parasites. Based on these analyses, T. gondii orchestrates a significant increase in dopamine metabolism in neural cells. Tyrosine hydroxylase, the rate-limiting enzyme for dopamine synthesis, was also found in intracellular tissue cysts in brain tissue with antibodies specific for the parasite-encoded tyrosine hydroxylase. These observations provide a mechanism for parasite-induced behavioral changes. The observed effects on dopamine metabolism could also be relevant in interpreting reports of psychobehavioral changes in toxoplasmosis-infected humans.
Parasite diversity is a constant challenge to host immune systems and has important clinical implications, but factors underpinning its emergence and maintenance are still poorly understood. Hosts typically harbour multiple parasite genotypes that share both host resources and immune responses. Parasite diversity is thus shaped not only by resource competition between co-infecting parasites but also by host-driven immune-mediated competition. We investigated these effects in an insect–trypanosome system, combining in vivo and in vitro single and double inoculations. In vivo, a non-pathogenic, general immune challenge was used to manipulate host immune condition and resulted in a reduced ability of hosts to defend against a subsequent exposure to the trypanosome parasites, illustrating the costs of immune activation. The associated increase in available host space benefited the weaker parasite strains of each pair as much as the otherwise more competitive strains, resulting in more frequent multiple infections in immune-challenged hosts. In vitro assays showed that in the absence of a host, overall parasite diversity was minimal because the outcome of competition was virtually fixed and resulted in strain extinction. Altogether, this shows that parasite competition is largely host-mediated and suggests a role for host immune condition in the maintenance of parasite diversity.
parasite; diversity; co-infection; competition; trypanosome; immune challenge
The recent declines in managed honey bee populations are of scientific, ecological and economic concern, and are partially attributed to honey bee parasites and related disease. McDonnell et al. investigate behavioral, chemical and neurogenomic effects of parasitization by the ectoparasite Varroa destructor and the endoparasite Nosema ceranae. The study reveals important links between underlying mechanisms of immunity and parasitization in social insects by demonstrating that chemical signals and neurogenomic states are significantly different between parasitized and non-parasitized honey bees, and that neurogenomic states are partially conserved between bees infected with distinct parasites. However the study does not reveal whether differences measured are primarily the result of adaptive host responses or of manipulation of the honey bee host by the parasites and/or confounding viral loads of parasitized individuals. Questions answered and raised by McDonnell et al. will lead to an improved understanding of honey bee health and, more generally, host-parasite interactions.
Honey bee health; Host-parasite coevolution; Insect immunity
Syrian hamsters become anemic and exhibit delayed growth following oral infection with third-stage Ancylostoma ceylanicum hookworm larvae. Here we describe experiments designed to determine the feasibility of adult worm transfer (AWT) between hosts, a technique that would facilitate the specific study of bloodfeeding hookworms in vivo without prior exposure of the host to larva-specific antigens, permit the ex vivo manipulation of adult parasites prior to reimplantation, and also allow for cross-species transfer of worms. Weanling hamsters given an oral AWT of 40 or 60 mixed-sex A. ceylanicum worms rapidly developed anemia; in the higher-dose group, hemoglobin levels declined from prechallenge levels by 44% within 4 days following AWT. Long-term survival of transferred worms was demonstrated by recovery of parasites from the intestines 42 days after AWT. AWT hamsters acquired humoral immune responses against soluble adult hookworm extracts and excretory-secretory products that were comparable in magnitude to those of animals given a typical infection with larvae. In AWT experiments employing the nonpermissive murine model, C57BL/6 mice given adult worms rapidly became anemic and lost weight in a manner similar to AWT hamsters. Infection of additional mouse strains demonstrated that while C57BL/10 and CD-1 mice also developed anemia following AWT, BALB/c mice were resistant. The technique of AWT to mice may further our understanding of hookworm pathogenesis by allowing the study of adult hookworm infections in a species with well-characterized genetics and an abundance of available reagents.
Social insects dominate ecological communities because of their sophisticated group behaviors. However, the intricate behaviors of social insects may be exploited by social parasites, which manipulate insect societies for their own benefit. Interactions between social parasites and their hosts lead to unusual coevolutionary dynamics that ultimately affect the breeding systems and population structures of both species. This study represents one of the first attempts to understand the population and colony genetic structure of a parasite and its host in a social wasp system.
We used DNA microsatellite markers to investigate gene flow, genetic variation, and mating behavior of the facultative social parasite Vespula squamosa and its primary host, V. maculifrons. Our analyses of genetic variability uncovered that both species possessed similar amounts of genetic variation and failed to show genetic structure over the sampling area. Our analysis of mating system of V. maculifrons and V. squamosa revealed high levels of polyandry and no evidence for inbreeding in the two species. Moreover, we found no significant differences between estimates of worker relatedness in this study and a previous investigation conducted over two decades ago, suggesting that the selective pressures operating on queen mate number have remained constant. Finally, the distribution of queen mate number in both species deviated from simple expectations suggesting that mate number may be under stabilizing selection.
The general biology of V. squamosa has not changed substantially from that of a typical, nonparasitic Vespula wasp. For example, population sizes of the host and its parasite appear to be similar, in contrast to other social parasites, which often display lower population sizes than their hosts. In addition, parasitism has not caused the mating behavior of V. squamosa queens to deviate from the high levels of multiple mating that typify Vespula wasps. This stands in contrast to some socially parasitic ants, which revert to mating with few males. Overall, the general similarity of the genetic structure of V. maculifrons and V. squamosa presumably reflects the fact that V. squamosa is still capable of independent colony founding and thus reflects an intermediate stage in the evolution of social parasitism.
The trade-off hypothesis for the evolution of virulence predicts that parasite transmission stage production and host exploitation are balanced such that lifetime transmission success (LTS) is maximised. However, the experimental evidence for this prediction is weak, mainly because LTS, which indicates parasite fitness, has been difficult to measure. For castrating parasites, this simple model has been modified to take into account that parasites convert host reproductive resources into transmission stages. Parasites that kill the host too early will hardly benefit from these resources, while postponing the killing of the host results in diminished returns. As predicted from optimality models, a parasite inducing castration should therefore castrate early, but show intermediate levels of virulence, where virulence is measured as time to host killing. We studied virulence in an experimental system where a bacterial parasite castrates its host and produces spores that are not released until after host death. This permits estimating the LTS of the parasite, which can then be related to its virulence. We exposed replicate individual
Daphnia magna (Crustacea) of one host clone to the same amount of bacterial spores and followed individuals until their death. We found that the parasite shows strong variation in the time to kill its host and that transmission stage production peaks at an intermediate level of virulence. A further experiment tested for the genetic basis of variation in virulence by comparing survival curves of daphniids infected with parasite spores obtained from early killing versus late killing infections. Hosts infected with early killer spores had a significantly higher death rate as compared to those infected with late killers, indicating that variation in time to death was at least in part caused by genetic differences among parasites. We speculate that the clear peak in lifetime reproductive success at intermediate killing times may be caused by the exceptionally strong physiological trade-off between host and parasite reproduction. This is the first experimental study to demonstrate that the production of propagules is highest at intermediate levels of virulence and that parasite genetic variability is available to drive the evolution of virulence in this system.
Daphnia hosts to the same amount of bacterial spores from the castrating bacterium
Pasteuria ramose provides experimental evidence that parasite fitness is maximized at intermediate levels of virulence.
Phylogenetically unrelated parasites often increase the chances of their transmission by inducing similar phenotypic changes in their hosts. However, it is not known whether these convergent strategies rely on the same biochemical precursors. In this paper, we explored such aspects by studying two gammarid species (Gammarus insensibilis and Gammarus pulex; Crustacea: Amphipoda: Gammaridae) serving as intermediate hosts in the life cycle of two distantly related parasites: the trematode, Microphallus papillorobustus and the acanthocephalan, Polymorphus minutus. Both these parasite species are known to manipulate the behaviour of their amphipod hosts, bringing them towards the water surface, where they are preferentially eaten by aquatic birds (definitive hosts). By studying and comparing the brains of infected G. insensibilis and G. pulex with proteomics tools, we have elucidated some of the proximate causes involved in the parasite-induced alterations of host behaviour for each system. Protein identifications suggest that altered physiological compartments in hosts can be similar (e.g. immunoneural connexions) or different (e.g. vision process), and hence specific to the host–parasite association considered. Moreover, proteins required to alter the same physiological compartment can be specific or conversely common in both systems, illustrating in the latter case a molecular convergence in the proximate mechanisms of manipulation.
acanthocephalan; gammarid; manipulative parasite; molecular convergence; proteomics; trematode
Cricket Paralysis virus (CrPV) is a member of the Dicistroviridae family of RNA viruses, which infect a broad range of insect hosts, including the fruit fly Drosophila melanogaster. Drosophila has emerged as an effective system for studying innate immunity because of its powerful genetic techniques and the high degree of gene and pathway conservation. Intra-abdominal injection of CrPV into adult flies causes a lethal infection that provides a robust assay for the identification of mutants with altered sensitivity to viral infection. To gain insight into the interactions between viruses and the innate immune system, we injected wild type flies with CrPV and observed that antimicrobial peptides (AMPs) were not induced and hemocytes were depleted in the course of infection. To investigate the contribution of conserved immune signaling pathways to antiviral innate immune responses, CrPV was injected into isogenic mutants of the Immune Deficiency (Imd) pathway, which resembles the mammalian Tumor Necrosis Factor Receptor (TNFR) pathway. Loss-of-function mutations in several Imd pathway genes displayed increased sensitivity to CrPV infection and higher CrPV loads. Our data show that antiviral innate immune responses in flies infected with CrPV depend upon hemocytes and signaling through the Imd pathway.
PCD in protozoan parasites has emerged as a fascinating field of parasite biology. This not only relates to the underlying mechanisms and their evolutionary implications but also to the impact on the parasite-host interactions within mammalian hosts and arthropod vectors. During recent years, common functions of apoptosis and autophagy in protozoa and during parasitic infections have emerged. Here, we review how distinct cell death pathways in Trypanosoma, Leishmania, Plasmodium or Toxoplasma may contribute to regulation of parasite cell densities in vectors and mammalian hosts, to differentiation of parasites, to stress responses, and to modulation of the host immunity. The examples provided indicate crucial roles of PCD in parasite biology. The existence of PCD pathways in these organisms and the identification as being critical for parasite biology and parasite-host interactions could serve as a basis for developing new anti-parasitic drugs that take advantage of these pathways.
Trophically transmitted parasites often alter their intermediate host's phenotype, thereby predisposing hosts to increased predation. This is generally considered to be a parasite strategy evolved to enhance transmission to the next host. However, the adaptive value of host manipulation is not clear, as it may be associated with costs, such as increased susceptibility to predator species that are unsuitable next hosts for the parasites. Thus, it has been proposed that, to be adaptive, manipulation should be specific by predisposing hosts more strongly to predation by target hosts (next host in the life cycle) than to non-hosts. Here we formally evaluate this prediction, and show that manipulation does not have to be specific to be adaptive. However, when manipulation is nonspecific, it needs to effectively increase the overall predation risk of infected hosts if it is to increase the parasite transmission probability. Thus, when initial predation risk is low, even highly nonspecific manipulation strategies can be adaptive. However, when initial predation risk is high, manipulation needs to be more specific to increase parasite transmission success. Therefore, nonspecific host manipulation may evolve in nature, but the adaptive value of a certain manipulation strategy can vary among different parasite populations depending on the variation in initial predation risk.
parasite–host interactions; host phenotype; host behaviour; non-host predation
Background and Aims
While invasive species may escape from natural enemies in the new range, the establishment of novel biotic interactions with species native to the invaded range can determine their success. Biological control of plant populations can be achieved by manipulation of a species' enemies in the invaded range. Interactions were therefore investigated between a native parasitic plant and an invasive legume in Mediterranean-type woodlands of South Australia.
The effects of the native stem parasite, Cassytha pubescens, on the introduced host, Cytisus scoparius, and a co-occurring native host, Leptospermum myrsinoides, were compared. The hypothesis that the parasitic plant would have a greater impact on the introduced host than the native host was tested. In a field study, photosynthesis, growth and survival of hosts and parasite were examined.
As predicted, Cassytha had greater impacts on the introduced host than the native host. Dead Cytisus were associated with dense Cassytha infections but mortality of Leptospermum was not correlated with parasite infection. Cassytha infection reduced the photosynthetic rates of both hosts. Infected Cytisus showed slower recovery of photosystem II efficiency, lower transpiration rates and reduced photosynthetic biomass in comparison with uninfected plants. Parasite photosynthetic rates and growth rates were higher when growing on the introduced host Cytisus, than on Leptospermum.
Infection by a native parasitic plant had strong negative effects on the physiology and above-ground biomass allocation of an introduced species and was correlated with increased plant mortality. The greater impact of the parasite on the introduced host may be due to either the greater resources that this host provides or increased resistance to infection by the native host. This disparity of effects between introduced host and native host indicates the potential for Cassytha to be exploited as a control tool.
Biological control; Cassytha pubescens; Cytisus scoparius; Leptospermum myrsinoides; parasitic plant; plant interactions; plant invasion; Scotch broom
Most inbred strains of mouse infected with the intestinal nematode Trichuris muris are resistant to infection expelling the parasite before adult worms establish. However, a few susceptible strains exist that are incapable of worm expulsion and harbor chronic infections of mature adult worms. Analyses of in vitro cytokine production by cells from the draining lymph node (mesenteric lymph node) have indicated that expulsion phenotype is tightly correlated with the selective expansion of helper T cells (Th) of the Th1 or Th2 cell subset within the mesenteric lymph node, resulting in susceptibility and resistance to T. muris, respectively. We have now confirmed and extended our in vitro observations in a series of experiments involving the in vivo manipulation of host cytokine levels. Depletion of interferon (IFN)- gamma in normally susceptible mice resulted in expulsion of the parasite, representing the first evidence for a role for IFN-gamma in the establishment of chronic helminth infection. Blocking interleukin (IL)-4 function in normally resistant animals prevented the generation of a protective immune response allowing adult stages of the parasite to develop. Conversely the administration of IL-4 to a normally susceptible host facilitated expulsion and indeed enabled established adult worms to be expelled when administered late in infection. In all cases assessment of a variety of in vivo parameters indicative of a Th1- or Th2-type response (parasite-specific immunoglobulin (Ig) G2a and the parasite-specific IgG1, total IgE levels and intestinal mastocytosis, respectively) demonstrated that the in vivo modulation of a Th1- or Th2- specific cytokine allowed the reciprocal Th cell subset to expand and become dominant with dramatic consequences for worm expulsion.
Mosquito-borne viruses are transmitted to human hosts via blood-feeding behavior of female mosquitoes. Female mosquitoes seek a host to take blood meals (host-seeking behavior). In order to prevent virus infections, it is important to understand how they modulate host-seeking behavior. Dopamine (DA) in the central nervous system acts as a neuromediator that regulates a variety of behaviors in insects. In female mosquitoes, host-seeking behavior increases when DA levels in the head decline after emergence. However, it remains unclear whether DA directly modulates host-seeking behavior in female mosquitoes. The aim of this study was to examine whether changes in DA levels in the head affects host-seeking activity in the adult female mosquito Aedes albopictus (Ae. albopictus).
We compared host-seeking behavior in one group of emerging female adults treated with l-β-3,4-dihydroxyphenylalanine (l-DOPA), the precursor of DA, (l-DOPA group), with that in an untreated control (control group) after confirming elevation of head DA in l-DOPA group by using high-performance liquid chromatography. The content of head DA in l-DOPA group significantly remained higher than that in controls on all days examined. The host-seeking activity in the control group showed a gradual increase over the 6-day experimental period. In contrast, there was no such increase in the host-seeking activity in the l-DOPA group. Therefore, the host-seeking activity of l-DOPA group was significantly lower than that of the controls between day 3 and 6 post-emergence.
Our results indicate that elevation of DA level reduces host-seeking activity in adult female mosquito Ae. albopictus.
Host-seeking behavior; Dopamine; Aedes albopictus
Chemical contamination and disease outbreaks have increased in many ecosystems. However, connecting pollution to disease spread remains difficult, in part, because contaminants can simultaneously exert direct and multi-generational effects on several host and parasite traits. To address these challenges, we parametrized a model using a zooplankton–fungus–copper system. In individual-level assays, we considered three sublethal contamination scenarios: no contamination, single-generation contamination (hosts and parasites exposed only during the assays) and multi-generational contamination (hosts and parasites exposed for several generations prior to and during the assays). Contamination boosted transmission by increasing contact of hosts with parasites. However, it diminished parasite reproduction by reducing the size and lifespan of infected hosts. Multi-generational contamination further reduced parasite reproduction. The parametrized model predicted that a single generation of contamination would enhance disease spread (via enhanced transmission), whereas multi-generational contamination would inhibit epidemics relative to unpolluted conditions (through greatly depressed parasite reproduction). In a population-level experiment, multi-generational contamination reduced the size of experimental epidemics but did not affect Daphnia populations without disease. This result highlights the importance of multi-generational effects for disease dynamics. Such integration of models with experiments can provide predictive power for disease problems in contaminated environments.
contamination; disease; multi-generational effects; Daphnia; transmission; parasite reproduction
The utility of using evolutionary and ecological frameworks to understand the dynamics of infectious diseases is gaining increasing recognition. However, integrating evolutionary ecology and infectious disease epidemiology is challenging because within-host dynamics can have counterintuitive consequences for between-host transmission, especially for vector-borne parasites. A major obstacle to linking within- and between-host processes is that the drivers of the relationships between the density, virulence, and fitness of parasites are poorly understood. By experimentally manipulating the intensity of rodent malaria (Plasmodium berghei) infections in Anopheles stephensi mosquitoes under different environmental conditions, we show that parasites experience substantial density-dependent fitness costs because crowding reduces both parasite proliferation and vector survival. We then use our data to predict how interactions between parasite density and vector environmental conditions shape within-vector processes and onward disease transmission. Our model predicts that density-dependent processes can have substantial and unexpected effects on the transmission potential of vector-borne disease, which should be considered in the development and evaluation of transmission-blocking interventions.
Anopheles stephensi; density dependence; disease transmission; fitness costs; life-history strategies; Plasmodium berghei; programmed cell death; vector-borne disease
Host populations with high genetic diversity are predicted to have lower levels of infection prevalence. This theory assumes that host genetic diversity results in variation in susceptibility and that parasites exhibit variation in infectivity. Empirical studies on the effects of host heterogeneity typically neglect the role of parasite diversity. We conducted three laboratory experiments designed to test if genetic variation in Daphnia magna populations and genetic variation in its parasites together influence the course of parasite spread after introduction. We found that a natural D. magna population exhibited variation in susceptibility to infection by three parasite species and had strong host clone–parasite species interactions. There was no effect of host heterogeneity in experimental host populations (polycultures and monocultures) separately exposed to single strains of three parasite species. When we manipulated the genetic diversity of a single parasite species and exposed them to host monocultures and polycultures, we found that parasite prevalence increased with the number of parasite strains. Host monocultures exposed to several parasite strains had higher mean parasite prevalence and higher variance than polycultures. These results indicate that effect of host genetic diversity on the spread of infection depends on the level of genetic diversity in the parasite population.
Daphnia magna; genetic diversity; Glugoides intestinalis; heterogeneity; host-parasite; infection; microsporidia; monoculture; Ordospora colligata; prevalence
Parasites often manipulate host immunity for their own benefit, either by exacerbating or suppressing the immune response and this may directly affect the expression of parasite virulence. However, genetic variation in immunodepression, which is a prerequisite to its evolution, and the relationship between immunodepression and virulence, have rarely been studied. Here, we investigated the variation among sibships of the acanthocephalan parasite, Pomphorhynchus laevis, in infecting and in immunodepressing its amphipod host, Gammarus pulex. We also assessed the covariation between infectivity, parasite-induced immune depression and host mortality (parasite virulence). We found that infectivity, the intensity of immunodepression and virulence were variable among parasite sibships. Infectivity and the level of immunodepression were not correlated across parasite sibships. Whereas infectivity was unrelated to host mortality, we found that gammarids that were exposed to the parasite sibships that immunodepressed their hosts the most survived better. This positive covariation between host survival and immunodepression suggests that gammarids exposed to the less immunodepressive parasites could suffer from damage imposed by a higher activity of the phenoloxidase.
acanthocephalan; covariation; immune defences; parasite-induced immunodepression; phenoloxidase; virulence
Cat odors induce rapid, innate and stereotyped defensive behaviors in rats at first exposure, a presumed response to the evolutionary pressures of predation. Bizarrely, rats infected with the brain parasite Toxoplasma gondii approach the cat odors they typically avoid. Since the protozoan Toxoplasma requires the cat to sexually reproduce, this change in host behavior is thought to be a remarkable example of a parasite manipulating a mammalian host for its own benefit. Toxoplasma does not influence host response to non-feline predator odor nor does it alter behavior on olfactory, social, fear or anxiety tests, arguing for specific manipulation in the processing of cat odor. We report that Toxoplasma infection alters neural activity in limbic brain areas necessary for innate defensive behavior in response to cat odor. Moreover, Toxoplasma increases activity in nearby limbic regions of sexual attraction when the rat is exposed to cat urine, compelling evidence that Toxoplasma overwhelms the innate fear response by causing, in its stead, a type of sexual attraction to the normally aversive cat odor.