Adaptive host manipulation by Toxoplasma gondii: fact or fiction?

Worth, Amanda R; Lymbery, Alan J.; Thompson, R.C.A.

doi:10.1016/j.pt.2013.01.004

Cited by 61 publications

(58 citation statements)

References 42 publications

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“…The parasite cannot achieve sexual reproduction in rodents and the described alterations increase the chances of transmission to its final, feline host. T. gondii can also infect other mammals (Poirotte et al, 2016) and is considered to be one of the most frequent infections in humans (Flegr, 2013b;Worth et al, 2013). Behavioral alterations that have been associated with latent toxoplasmosis include multiple forms of schizophrenia, personality disorder, Parkinson disease and Alzheimer disease, as well as increased aggressiveness, decreased willingness to follow social rules, and slower reaction times in men (Flegr, 2013a).…”

Section: Zombie Ants Fearless Rats and Other Prominent Cases Of Manmentioning

confidence: 99%

“…As a possible explanation, he suggested publication bias, that is, an initial euphoria concerning the intensity of manipulation effects became replaced by more realistic estimates over time (Poulin, 2000). More recently, other authors have stressed that alternative explanations need to be considered-and excluded-to provide conclusive empirical support for an assumed case of manipulation (Klein, 2005;Thomas et al, 2005;James, 2010;Cator et al, 2012Cator et al, , 2015Lafferty and Kuris, 2012;Worth et al, 2013). Alternatively, such alterations can: (1) represent mere side-effects of the pathology that is associated with infection; (2) form part of the successful immune response of the host to parasitization; or (3) represent traits that were inherited from ancestors but represent maladaptations in the present host-parasite combination (Klein, 2005;Thomas et al, 2005).…”

Section: Searching For General Patterns In Reports On Host Manipulationmentioning

confidence: 99%

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Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

Heil

2016

Front. Ecol. Evol.

109

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Parasites must overcome host immunity and change hosts for dispersal. Therefore, seemingly odd behaviors of parasitized animals, like those exhibited by "Zombie ants" or the "fatal attraction" of mammals to their predators, have been explained as the extended phenotype of parasites that manipulate their hosts for transmission enhancement. Manipulation has evolved in all major phylogenetic lineages of parasites but is not ubiquitous. In fact, the real frequency and relevance of manipulation is still matter of debate. Here, I highlight some of the most pertinent questions that arise if we aim at a broader understanding of the ecological relevance and evolutionary trajectory of manipulating parasites. Why are more parasites with a trophic mode of transmission manipulating their host than horizontally transmitted parasites? Why are the causal agents of sexually transmitted diseases (STDs) so rarely reported to manipulate their host? Why do parasites of animals usually manipulate their intermediate host, whereas many pathogens of plants manipulate their final host and then cause a "fatal attraction" of herbivores to the already infected plant? How can we distinguish manipulation effects from adaptive host responses to parasitization? Does manipulation cause a cost to certain parasites that can select against the evolution of manipulation? More emphasis should be put on direct comparisons among parasites of animals, plants, and humans. Manipulation for transmission enhancement should be studied in concert with manipulation for host immunity suppression, the molecular mechanisms that control the manipulation effect need to be deciphered, and we should test for alternative explanations for the observed phenotypic changes. Finally, we should quantify transmission rates and net fitness for manipulating and non-manipulating parasites, in ecologically realistic setups, to identify the forces that select against the evolution of manipulation. Ultimately, parasite net fitness represents the relevant outcome of any manipulation effect.Keywords: immunity, malaria, partner manipulation, pathogen, plant-enemy interaction, STDs, toxoplasmosis "FATAL ATTRACTION" AND MANIPULATING PARASITES Parasites represent a ubiquitous aspect in the life of multicellular organisms (Wood and Johnson, 2015) and most, if not all, of us have experienced how strongly an infection can interfere with our normal activities and well-being. Therefore, it might not appear to be too surprising when parasitized hosts exhibit behavioral alterations (see Glossary) as compared to healthy conspecifics.

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Section: Zombie Ants Fearless Rats and Other Prominent Cases Of Manmentioning

confidence: 99%

Section: Searching For General Patterns In Reports On Host Manipulationmentioning

confidence: 99%

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

Heil

2016

Front. Ecol. Evol.

109

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“…The effects of T. gondii infection on rodent behavior vary with the experimental design, including differences in rodent species, route of infection, parasite strain, dosage and stage of parasites, time postinfection, and type of behavior test (36,37). These differences make it difficult to clarify the characteristics of the brain pathology associated with behavioral changes following T. gondii infection.…”

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confidence: 99%

Toxoplasma gondii Infection in Mice Impairs Long-Term Fear Memory Consolidation through Dysfunction of the Cortex and Amygdala

et al. 2016

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cChronic infection with Toxoplasma gondii becomes established in tissues of the central nervous system, where parasites may directly or indirectly modulate neuronal function. Epidemiological studies have revealed that chronic infection in humans is a risk factor for developing mental diseases. However, the mechanisms underlying parasite-induced neuronal dysfunction in the brain remain unclear. Here, we examined memory associated with conditioned fear in mice and found that T. gondii infection impairs consolidation of conditioned fear memory. To examine the brain pathology induced by T. gondii infection, we analyzed the parasite load and histopathological changes. T. gondii infects all brain areas, yet the cortex exhibits more severe tissue damage than other regions. We measured neurotransmitter levels in the cortex and amygdala because these regions are involved in fear memory expression. The levels of dopamine metabolites but not those of dopamine were increased in the cortex of infected mice compared with those in the cortex of uninfected mice. In contrast, serotonin levels were decreased in the amygdala and norepinephrine levels were decreased in the cortex and amygdala of infected mice. The levels of cortical dopamine metabolites were associated with the time spent freezing in the fear-conditioning test. These results suggest that T. gondii infection affects fear memory through dysfunction of the cortex and amygdala. Our findings provide insight into the mechanisms underlying the neurological changes seen during T. gondii infection.T oxoplasma gondii is one of the most successful brain parasites, infecting approximately one-third of the human population (1). T. gondii can persist in brain and muscle throughout the host's life, and chronic infection is asymptomatic in immunocompetent humans (2). However, recent studies have suggested that T. gondii infection is a risk factor for developing mental diseases, such as schizophrenia and depression, as well as human behavior and personality changes and suicide (3, 4). Interestingly, T. gondii infection increases the risk of schizophrenia roughly 2.7 times, which is higher than that for genes associated with schizophrenia (5). Several studies have also suggested that rodents infected with T. gondii exhibit decreased avoidance behavior in response to cat odors, indicating manipulation of the host's behavior by T. gondii to facilitate the parasite's transmission and complete sexual replication in the definitive host (6-11).To date, research on the mechanism(s) underlying behavioral changes following T. gondii infection has been conducted primarily from two points of view. First, the relationship between parasite localization in the brain and behavioral changes has been investigated, with a previous study reporting that T. gondii has no obvious tropism in the brain (12-15). However, another study found that tissue cyst density in amygdalar areas (the medial and basolateral amygdala) is 2-fold higher than that in nonamygdalar areas (9), whereas the presence of tissue cy...

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“…As a consequence, behavioural manipulation in rodents could be expected to specifically increase predation of infected rodents by cats. However, Worth et al [27] highlighted inconsistencies between effects of T. gondii behavioural manipulation: while some studies reported behavioural modifications specific to cat stimuli [24][25][26], others showed unspecific modification in activity and anxiety levels [22,23], with sometimes conflicting results. Moreover, Kannan et al [28] showed differences in the duration of the behavioural modification in mice between two T. gondii strains.…”

Section: Introductionmentioning

confidence: 99%

When should a trophically and vertically transmitted parasite manipulate its intermediate host? The case ofToxoplasma gondii

et al. 2013

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Parasites with complex life cycles are expected to manipulate the behaviour of their intermediate hosts (IHs), which increase their predation rate and facilitate the transmission to definitive hosts (DHs). This ability, however, is a doubleedged sword when the parasite can also be transmitted vertically in the IH. In this situation, as the manipulation of the IH behaviour increases the IH death rate, it conflicts with vertical transmission, which requires healthy and reproducing IHs. The protozoan Toxoplasma gondii, a widespread pathogen, combines both trophic and vertical transmission strategies. Is parasite manipulation of host behaviour still adaptive in this situation? We model the evolution of the IH manipulation by T. gondii to study the conflict between these two routes of transmission under different epidemiological situations. Model outputs show that manipulation is particularly advantageous for virulent strains and in epidemic situations, and that different levels of manipulation may evolve depending on the sex of the IH and the transmission routes considered. These results may help to understand the variability of strain characteristics encountered for T. gondii and may extend to other trophically transmitted parasites.

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Adaptive host manipulation by Toxoplasma gondii: fact or fiction?

Cited by 61 publications

References 42 publications

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

Toxoplasma gondii Infection in Mice Impairs Long-Term Fear Memory Consolidation through Dysfunction of the Cortex and Amygdala

When should a trophically and vertically transmitted parasite manipulate its intermediate host? The case ofToxoplasma gondii

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