Parasite Manipulation Research Articles

Patterns and variation in the mammal parasite-glucocorticoid relationship.

Parasites are ubiquitous and can strongly affect their hosts through mechanisms such as behavioural changes, increased energetic costs and/or immunomodulation. When parasites are detrimental to their hosts, they should act as physiological stressors and elicit the release of glucocorticoids. Alternatively, previously elevated glucocorticoid levels could facilitate parasite infection due to neuroimmunomodulation. However, results are equivocal, with studies showing either positive, negative or no relationship between parasite infection and glucocorticoid levels. Since factors such as parasite type, infection severity or host age and sex can influence the parasite-glucocorticoid relationship, we review the main mechanisms driving this relationship. We then perform a phylogenetic meta-analysis of 110 records from 65 studies in mammalian hosts from experimental and observational studies to quantify the general direction of this relationship and to identify ecological and methodological drivers of the observed variability. Our review produced equivocal results concerning the direction of the relationship, but there was stronger support for a positive relationship, although causality remained unclear. Mechanisms such as host manipulation for parasite survival, host response to infection, cumulative effects of multiple stressors, and neuro-immunomodulatory effects of glucocorticoids could explain the positive relationship. Our meta-analysis results revealed an overall positive relationship between glucocorticoids and parasitism among both experimental and observational studies. Because all experimental studies included were parasite manipulations, we conclude that parasites caused in general an increase in glucocorticoid levels. To obtain a better understanding of the directionality of this link, experimental manipulation of glucocorticoid levels is now required to assess the causal effects of high glucocorticoid levels on parasite infection. Neither parasite type, the method used to assess parasite infection nor phylogeny influenced the relationship, and there was no evidence for publication bias. Future studies should attempt to be as comprehensive as possible, including moderators potentially influencing the parasite-glucocorticoid relationship. We particularly emphasise the importance of testing hosts of a broad age range, concomitantly measuring sex hormone levels or at least reproductive status, and for observational studies, also considering food availability, host body condition and social stressors to obtain a better understanding of the parasite-glucocorticoid relationship.

Zombie bugs? Manipulation of kissing bug behavior by the parasite Trypanosoma cruzi

The parasite manipulation hypothesis states that the parasite modifies host's behavior thereby increasing the probability that the parasite will pass from an intermediate host to its final host. We used the kissing bugs Triatoma pallidipennis and T. longipennis and two isolates of the Trypanosoma cruzi parasite (Chilpancingo and Morelos) to test these ideas. These insects are intermediate hosts of this parasite, which is the causal agent of Chagas disease. The Chilpancingo isolate is more pathogenic than the Morelos isolate, in the bugs. We expected that infected bugs would be more active and likely at detecting human-like odors. Given the differences in pathogenicity between isolates, we expected the Chilpancingo isolate to induce these effects more strongly and lead to higher parasite number than the Morelos isolate. Finally, infected bugs would gain less mass (a mechanism thought to increase bite rate, and thus transmission) than non-infected bugs. Having determined that both isolate haplotypes belong to the Tc1a group, we found that: (a) young instars of both species were more active and likely to detect human odor when they were infected, regardless of the isolate; (b) there was no difference in parasite abundance depending on isolate; and, (c) infected bugs did not end up with less weight than uninfected bugs. These results suggest that T. cruzi can manipulate the bugs, which implies a higher risk to contract Chagas disease than previously thought.

Tapeworm manipulation of copepod behaviour: parasite genotype has a larger effect than host genotype.

Compared with uninfected individuals, infected animals can exhibit altered phenotypes. The changes often appear beneficial to parasites, leading to the notion that modified host phenotypes are extended parasite phenotypes, shaped by parasite genes. However, the phenotype of a parasitized individual may reflect parasitic manipulation, host responses to infection or both, and disentangling the contribution of parasite genes versus host genes to these altered phenotypes is challenging. Using a tapeworm (Schistocephalus solidus) infecting its copepod first intermediate host, I performed a full-factorial, cross-infection experiment with five host and five parasite genotypes. I found that a behavioural trait modified by infection, copepod activity, was affected by both host and parasite genotype. There was no clear evidence for host genotype by parasite genotype interactions. Several observations indicated that host behaviour was chiefly determined by parasite genes: (i) all infected copepods, regardless of host or parasite genotype, exhibited behavioural changes, (ii) parasitism reduced the differences among copepod genotypes, and (iii) within infected copepods, parasite genotype had twice as large an effect on behaviour as host genotype. I conclude that the altered behaviour of infected copepods primarily represents an extended parasite phenotype, and I discuss how genetic variation in parasitic host manipulation could be maintained.

Invisible Designers: Brain Evolution Through the Lens of Parasite Manipulation

AbstractThe ability of parasites to manipulate host behavior to their advantage has been studied extensively, but the impact of parasite manipulation on the evolution of neural and endocrine mechan...

No impact of a presumed manipulative parasite on the responses and susceptibility of fish to simulated predation

AbstractParasites manipulating their host to facilitate trophic transmission is a widespread and diverse phenomenon. Trematode eye‐flukes in the family Diplostomidae infect a variety of fish species as metacercariae, many residing in the eyes. A recently described diplostomid, Tylodelphys darbyi, from the South Island of New Zealand has been found to infect common bully Gobiomorphus cotidianus, an endemic freshwater fish. Within the fish, the metacercariae move about freely in the liquid parts of the eye and are quite large. We hypothesized that increasing intensity of T. darbyi infection will result in increasing visual impairment, thus reducing the ability of G. cotidianus to identify and react to a predatory threat. To test this hypothesis, we performed experiments to (a) examine the fish's reaction to a purely visual predator cue and (b) test their ability to avoid simulated predation under natural levels of infection. Among the 64 fish used in our experiments, T. darbyi had a prevalence of 98.7% with an average of 17.6 worms per fish. However, there was no relationship between T. darbyi intensity and either the fish's reaction to a visual predator stimulus or their ability to escape a simulated predator. Our findings indicate that despite being present in large numbers in the eyes of its fish host, the parasite appears incapable of improving its chances of trophic transmission to its avian definitive host. The results also suggest that the fish G. cotidianus could be using other senses (e.g., olfaction and lateral line) to compensate for visual impairment, and detect and respond to predators.

Inter-population variation in the intensity of host manipulation by the fish acanthocephalan Pomphorhynchus tereticollis: are differences driven by predation risk?

Many trophically-transmitted parasites induce behavioural alteration in their intermediate hosts that tend to increase host vulnerability to predation. Inter-population variability in parasite-induced alterations is expected to arise from variable local opportunities for trophic transmission. Yet, this hypothesis has not been investigated so far. We addressed the issue in four populations of the fish parasite Pomphorhynchus tereticollis (Acanthocephala), using variable fish biomass density as a proxy for transmission opportunities. We found variation in the intensity of parasite-induced changes in phototaxis and refuge use among populations. Two of the populations with the lowest predator biomass exhibited the highest levels of behavioural manipulation and prevalence, as expected at low transmission opportunities. They also exhibited micro-habitat segregation between infected and uninfected gammarids in the field. In addition, infection had variable effects on two physiological defence systems, immunity and antioxidant capacity, and on total protein content. Overall, our study brings partial support to the prediction that host manipulation and prevalence should be higher at low predator biomass. Although stronger evidence should be sought by increasing population replicates, our study points to the importance of the ecological context, specifically transmission opportunities brought about by predation pressure, for the evolution of parasite manipulation in trophically-transmitted parasites.

Secreted parasite Pin1 isomerase stabilizes host PKM2 to reprogram host cell metabolism

Metabolic reprogramming is an important feature of host–pathogen interactions and a hallmark of tumorigenesis. The intracellular apicomplexa parasite Theileria induces a Warburg-like effect in host leukocytes by hijacking signaling machineries, epigenetic regulators and transcriptional programs to create a transformed cell state. The molecular mechanisms underlying host cell transformation are unclear. Here we show that a parasite-encoded prolyl-isomerase, TaPin1, stabilizes host pyruvate kinase isoform M2 (PKM2) leading to HIF-1α-dependent regulation of metabolic enzymes, glucose uptake and transformed phenotypes in parasite-infected cells. Our results provide a direct molecular link between the secreted parasite TaPin1 protein and host gene expression programs. This study demonstrates the importance of prolyl isomerization in the parasite manipulation of host metabolism.

Host manipulation by parasites as a cryptic driver of energy flow through food webs.

Manipulative parasites alter predator-prey interactions, and thus may facilitate, shift or create energy flow pathways through food webs (referred to hereafter as manipulation-mediated energy flow, MMEF). The ecological significance of MMEF would be determined not only by the strength of host manipulation, but also ecological and epidemiological factors, including host biomass, parasite incidence, and trophic position of the host-parasite association in their food webs. While previous theory has predicted that strong manipulation will destabilize host-parasite dynamics, a recently proposed theoretical framework claims that a switching strategy (sequential manipulation from predation suppression to enhancement) should allow parasites to induce strong predation enhancement and thus large MMEF. We formally outline the current and future directions to better understand the causes and consequences of MMEF across biological hierarchies.

Adaptive suicide: is a kin-selected driver of fatal behaviours likely?

While several manipulated host behaviours are accepted as extended phenotypes of parasites, there remains debate over whether other altered behaviours in hosts following parasitic invasion represent cases of parasite manipulation, host defence or the pathology of infection. One particularly controversial subject is 'suicidal behaviour' in infected hosts. The host-suicide hypothesis proposes that host death benefits hosts doomed to reduced direct fitness by protecting kin from parasitism and therefore increasing inclusive fitness. However, adaptive suicide has been difficult to demonstrate conclusively as a host adaptation in studies on social or clonal insects, for whom high relatedness should enable greater inclusive fitness benefits. Following discussion of empirical and theoretical works from a behavioural ecology perspective, this review finds that the most persuasive evidence for selection of adaptive suicide comes from bacteria. Despite a focus on parasites, driven by the existing literature, the potential for the evolution of adaptive suicidal behaviour in hosts is also considered to apply to cases of infection by pathogens, provided that the disease has a severe effect on direct fitness and that suicidal behaviour can affect pathogen transmission dynamics. Suggestions are made for future research and a broadening of the possible implications for coevolution between parasites and hosts.

Experimental evolution of parasitic host manipulation.

Host manipulation is a parasite-induced alteration of a host's phenotype that increases parasite fitness. However, if genetically encoded in the parasite, it should be under selection in the parasite. Such host manipulation has often been assumed to be energetically costly, which should restrict its evolution. Evidence of such costs, however, remains elusive. The trophically transmitted cestode Schistocephalus solidus manipulates the activity of its first intermediate copepod host to reduce its predation susceptibility before the parasite is ready for transmission. Thereafter, S. solidus increases host activity to facilitate transmission to its subsequent fish host. I selected S. solidus for or against host manipulation over three generations to investigate the evolvability of manipulation and identify potential trade-offs. Host manipulation responded to selection, confirming that this trait is heritable in the parasite and hence can present an extended phenotype. Changes in host manipulation were not restrained by any obvious costs.

Virus effects on plant quality and vector behavior are species specific and do not depend on host physiological phenotype

There is growing evidence that plant viruses manipulate host plants to increase transmission-conducive behaviors by vectors. Reports of this phenomenon frequently include only highly susceptible, domesticated annual plants as hosts, which constrains our ability to determine whether virus effects are a component of an adaptive strategy on the part of the pathogen or simply by-products of pathology. Here, we tested the hypothesis that transmission-conducive effects of a virus (Turnip yellows virus [TuYV]) on host palatability and vector behavior (Myzus persicae) are linked with host plant tolerance and physiological phenotype. Our study system consisted of a cultivated crop, false flax (Camelina sativa) (Brassicales: Brassicaceae), a wild congener (C. microcarpa), and a viable F1 hybrid of these two species. We found that the most tolerant host (C. microcarpa) exhibited the most transmission-conducive changes in phenotype relative to mock-inoculated healthy plants: Aphids preferred to settle and feed on TuYV-infected C. microcarpa and did not experience fitness changes due to infection—both of which will increase viruliferous aphid numbers. In contrast, TuYV induced transmission-limiting phenotypes in the least tolerant host (C. sativa) and to a greater degree in the F1 hybrid, which exhibited intermediate tolerance to infection. Our results provide no evidence that virus effects track with infection tolerance or physiological phenotype. Instead, vector preferences and performance are driven by host-specific changes in carbohydrates under TuYV infection. These results provide evidence that induction of transmission-enhancing phenotypes by plant viruses is not simply a by-product of general pathology, as has been proposed as an explanation for putative instances of parasite manipulation by viruses and many other taxa.

Ophiocordyceps-ant interactions as an integrative model to understand the molecular basis of parasitic behavioral manipulation.

Ophiocordyceps-infected ants display a substrate biting behavior that aids parasite transmission. World-wide research into this behavioral manipulation has led to new fungal species descriptions, annotated genomes, and detailed field observations. Experimentally tractable modified ant behaviors and the development of infection techniques have enabled the quest for the molecular basis of this phenomenon. Behavioral studies followed by transcriptomics, metabolomics and three-dimensional electron microscopy have led to novel mechanistic hypotheses. This multidisciplinary work represents a big leap forward. However, definitive answers have yet to be obtained. A comprehensive understanding hinges on continued integrative efforts that reveal the precise natural history, behavioral ecology and evolutionary relationships between Ophiocordyceps-ant systems, and the true functions and involvement of genes and metabolites in behavioral manipulation.

Turning your victim into a collaborator: exploitation of insect behavioral control systems by parasitic manipulators.

Some parasites manipulate host behavior by exploiting the host's behavioral control networks. This review explores two examples of this approach using parasites from opposite ends of the size spectrum, that is, viruses and parasitic insects. The first example explores the use of the gene (egt) by some baculoviruses to deactivate the hormone 20-hydroxyecdysone. Suppressing this chemical signal prevents the expression of behaviors that could reduce viral transmission. The second example explores how a parasitic wasp uses the host's immune/neural communication system to control host behavior. When a host's manipulated behavior requires complex neural coordination, exploitation of host behavioral control systems is likely to be involved. Simpler host behaviors can be induced by damage to host tissues.

Parasitic Manipulations of the Host Phenotype: Effects in Internal and External Environments

Parasites can influence their hosts in various ways. When a parasite changes the phenotype of its host to increase its own fitness, it is called parasitic manipulation of host phenotype. Perhaps, not all parasites are manipulators, but manipulations are undoubtedly a widespread natural phenomenon and well-established scientific concept. Parasites can manipulate the host phenotype to ensure their additional safety within the host body, create optimal conditions for their growth and development, and promote transmission from one host to another. Parasitic manipulative strategies are highly diverse and tightly connected with the parasite’s life cycle. The review gives insight into the most common types of manipulative strategies and discusses (i) the evolutionary advantages of these strategies, (ii) why some strategies are more common than others, and (iii) how manipulative strategies change in the course of parasite growth and development. Recently, it has become clear that parasitic manipulations can be an important factor influencing the relationships in both the parasitic infracommunity within the host and the ecosystem in general. The last two sections of the review describe the conflicts and cooperation within the parasitic infrapopulation and the role of parasitic manipulations in ecosystems. The review concludes with a short, imaginary journey into the future that discusses how climate change may influence the role of parasites and their manipulations in the ever-changing environment.

Parasite-induced colour alteration of intermediate hosts increases ingestion by suitable final host species

Abstract Parasites with complex life cycles often alter the phenotypic appearance of their intermediate hosts in order to facilitate ingestion by the final host. However, such manipulation can be costly as it might increase ingestion by less suitable or dead-end hosts as well. Species-specific parasitic manipulation is a way to enhance the transmission to suitable final hosts. Here, we experimentally show that the altered body colouration of the intermediate host Gammarus pulex caused by its acanthocephalan parasite Pomphorhynchus laevis differently affects predation by different fish species (barbel, perch, ruffe, brown trout and two populations of three-spined stickleback) depending on their suitability to act as final host. Species that were responsive to colour manipulation in a predation experiment were more susceptible to infection with P. laevis than unresponsive species. Furthermore, three-spined stickleback from different populations responded to parasite manipulation in opposite directions. Such increased ingestion of the intermediate host by preferred and suitable hosts suggests fine-tuned adaptive parasitic manipulation and sheds light on the ongoing evolutionary arms race between hosts and manipulative parasites.

Parasite manipulation of host behavior

Some parasites have evolved the ability to precisely control the behavior of animals in ways that enhance the transmission of parasite genes into the next generation. This is the concept of the 'extended phenotype' first conceived by Richard Dawkins in 1982. It states that the behavior we observe in animals is due not only to the expression of their genes, but also to the genes of parasites infecting them. In such cases, the behavior is an extended phenotype of the parasite.

Self-medication in insects: when altered behaviors of infected insects are a defense instead of a parasite manipulation.

Studies have demonstrated that medication behaviors by insects are much more common than previously thought. Bees, ants, flies, and butterflies can use a wide range of toxic and nutritional compounds to medicate themselves or their genetic kin. Medication occurs either in response to active infection (therapy) or high infection risk (prophylaxis), and can be used to increase resistance or tolerance to infection. While much progress has been made over the last few years, there are also key areas that require in-depth investigation. These include quantifying the costs of medication, especially at the colony level of social insects, and formulating theoretical models that can predict the role of infection risk in driving micro-evolutionary and macro-evolutionary patterns of animal medication behaviors.

Parasite transmission between trophic levels stabilizes predator\u2013prey interaction

Manipulative parasites that promote their transmission by altering their host’s phenotype are widespread in nature, which suggests that host manipulation allows the permanent coexistence of the host with the parasite. However, the underlying mechanism by which host manipulation affects community stability remains unelucidated. Here, using a mathematical model, we show that host manipulation can stabilise community dynamics. We consider systems wherein parasites are transmitted between different trophic levels: intermediate host prey and final host predator. Without host manipulation, the non-manipulative parasite can destabilise an otherwise globally stable prey–predator system, causing population cycles. However, host manipulation can dampen such population cycles, particularly when the manipulation is strong. This finding suggests that host manipulation is a consequence of self-organized behavior of the parasite populations that allows permanent coexistence with the hosts and plays a key role in community stability.

Winning the arms race: host-parasite shared evolutionary history reduces infection risks in fish final hosts.

Parasite manipulation of intermediate hosts evolves to increase parasite trophic transmission to final hosts, yet counter selection should act on the final host to reduce infection risk and costs. However, determining who wins this arms race and to what extent is challenging. Here, for the first time, comparative functional response analysis quantified final host consumption patterns with respect to intermediate host parasite status. Experiments used two evolutionarily experienced fish hosts and two naive hosts, and their amphipod intermediate hosts of the acanthocephalan parasite Pomphorhynchus tereticollis. The two experienced fish consumed significantly fewer infected than non-infected prey, with lower attack rates and higher handling times towards the former. Conversely, the two naive fish consumed similar numbers of infected and non-infected prey at most densities, with similar attack rates and handling times towards both. Thus, evolutionarily experienced final hosts can reduce their infection risks and costs via reduced intermediate host consumption, with this not apparent in naive hosts.

Some like it hot: factors impacting thermal preferences of two Ponto-Caspian amphipods Dikerogammarus villosus (Sovinsky, 1894) and Dikerogammarus haemobaphes (Eichwald, 1841).

Temperature is a crucial factor determining biology and ecology of poikilothermic animals. It often constitutes an important barrier for invasive species originating from different climate zones but, on the other hand, may facilitate the invasion process of animals with wide thermal preferences and high resistance to extreme temperatures. In our experimental study, we investigated the thermal behaviour of two Ponto-Caspian amphipod crustaceans—Dikerogammarus villosus and Dikerogammarus haemobaphes. Both species are known to live under a wide range of thermal conditions which may promote their invasion. Moreover, both these amphipods are hosts for microsporidian parasites which co-evolved with them within the Ponto-Caspian region and spread in European waters. As the presence of a parasite may influence the thermal preferences of its host, we expected to observe behavioural changes in infected individuals of the studied amphipods leading to (1) behavioural fever (selecting a warmer habitat) or (2) anapyrexia (selecting a colder habitat). The experiment (N = 20) was carried out for 30 min in a 100 cm. 20 cm from boths sides were not avaliable for amphipods long thermal gradient (0–40 °C), using 30 randomly selected adult amphipod individuals of one species. At the end of each trial, we checked the position of amphipods along the gradient and determined their sex and infection status (uninfected or infected by one of microsporidium species). D. villosus was infected with Cucumispora dikerogammari whereas D. haemobaphes was a host for C. dikerogammari, Dictyocoela muelleri or D. berillonum. Thermal preferences of amphipods depended on their species and sex. Females of D. villosus preferred warmer microhabitats (often much above 30 °C) than conspecific males and females of D. haemobaphes, whereas no significant differences were found among males of both species and both sexes of D. haemobaphes. Moreover, infected males of D. villosus stayed in warmer water more often than uninfected males of this species, selecting temperatures higher than 30 °C, which may be explained either as a behavioural fever constituting a defence mechanism of a host against the infection, or as a parasite manipulation of the host behaviour increasing the parasite fitness. On the other hand, none of the parasite species affected the thermal preferences of D. haemobaphes, including also C. dikerogammari, changing the behaviour of D. villosus. Our research presents the complexity of the thermal behaviour of studied amphipods and the evidence that microsporidia may trigger a change in temperature preferendum of their host species and those observations may be the result of different host-parasite coevolution time which may vary for the two host species (Poulin, 2010).