Manipulation of host behaviour by Toxoplasma gondii: what is the minimum a proposed proximate mechanism should explain?

Vyas, Ajai; Sapolsky, Robert M.

doi:10.14411/fp.2010.011

Cited by 56 publications

(49 citation statements)

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“…Thus, testosterone could reduce fear response either directly through its action in the brain or indirectly through its suppressive effects on the stress response (Mitra et al, 2012). The main challenge for these possibilities is the fact that behavioral effects of T. gondii are rather specific (Lamberton et al, 2008;Vyas et al, 2007a;Vyas and Sapolsky, 2010). For example, although it affects innate fear, the infection does not change unconditioned anxiety or conditioned fear, although reduced anxiety has also been reported in rats (Gonzalez et al, 2007;Webster et al, 1994).…”

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Parasite-augmented mate choice and reduction in innate fear in rats infected byToxoplasma gondii

Vyas

2013

Journal of Experimental Biology

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SummaryTypically, female rats demonstrate clear mate choice. Mate preference is driven by the evolutionary need to choose males with heritable parasite resistance and to prevent the transmission of contagious diseases during mating. Thus, females detect and avoid parasitized males. Over evolutionary time scales, parasite-free males plausibly evolve to advertise their status. This arrangement between males and females is obviously detrimental to parasites, especially for sexually transmitted parasites. Yet Toxoplasma gondii, a sexually transmitted parasite, gets around this obstacle by manipulating mate choice of uninfected females. Males infected with this parasite become more attractive to uninfected females. The ability of T. gondii to not only advantageously alter the behavior and physiology of its host but also secondarily alter the behavior of uninfected females presents a striking example of the ʻextended phenotypeʼ of parasites. Toxoplasma gondii also abolishes the innate fear response of rats to cat odor; this likely increases parasite transmission through the trophic route. It is plausible that these two manipulations are not two distinct phenotypes, but are rather part of a single pattern built around testosterone-mediated interplay between mate choice, parasitism and predation.Key words: anti-predator behavior, behavioral manipulation, major urinary proteins, parasitism, sexual selection, sexual transmission, trophic transmission, testosterone. In many species, females provide greater parental care and investment than males. This leads to a biased operational sex ratio, manifested as more sexually receptive males than females. As a direct result of such bias, males compete between themselves for access to females and females have the opportunity to choose from many suitors. This leads to sexual selection, resulting in evolution of male traits that are useful in fighting competitor males (intrasexual selection) and influencing mate choice of females (intersexual selection) (Andersson, 1994; Andersson and Simmons, 2006). The intra-sexual selection often results in evolution of conspicuous male phenotypes that aim to advertise and attract females (e.g. bright plumage in birds).From the perspective of this review, mechanisms driving mate choice in rats are of special interest. Several mechanisms have been proposed to explain preference of females for certain male traits.It is possible that females choose males that provide a direct and immediate benefit to the female and/or their progeny (Møller and Jennions, 2001). Relevant examples include parental care or nuptial gifts (food or material tokens transferred by male during courtship or mating). Male rats provide neither parental care nor nuptial gifts. However, it is possible that female rats choose males in order to reduce the chances of direct associative transmission of parasites or diseases (Able, 1996). That will constitute a mate choice driven by direct benefit.It is also possible that mate choice is based on indirect benefits that hinge on the gre...

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Parasite-augmented mate choice and reduction in innate fear in rats infected byToxoplasma gondii

Vyas

2013

Journal of Experimental Biology

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“…skallová et al , Henriquez et al 2009for review, Webster and Mcconkey 2010). Toxoplasma gondii with its complex life cycle and networking with the host's organism interferes with several neurotransmitter systems, such as the serotonin and dopamine systems (Hinze-selch et al 2007; for review, Vyas and sapolsky 2010). a very recent report even demonstrates that T. gondii by its own is able to synthesize dopamine (gaskell et al 2009).…”

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The diagnosis of a personality disorder increases the likelihood for seropositivity to Toxoplasma gondii in psychiatric patients

Hinze-Selch

Däubener²,

Erdag³

et al. 2010

FOLIA PARASIT

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More than one decade ago Flegr and Hrdý (1994) reported that individuals with serologically proven infection with Toxoplasma gondii (tg) differ with respect to several personality traits compared to uninfected controls. recently, there is growing evidence that parasites such as T. gondii indeed can modify human and animal behaviour (e.g. skallová et al. 2006behaviour (e.g. skallová et al. , Henriquez et al. 2009 for review, Webster and Mcconkey 2010). Toxoplasma gondii with its complex life cycle and networking with the host's organism interferes with several neurotransmitter systems, such as the serotonin and dopamine systems (Hinze-selch et al. 2007; for review, Vyas and sapolsky 2010). a very recent report even demonstrates that T. gondii by its own is able to synthesize dopamine (gaskell et al. 2009). there are numerous reports on Toxoplasma serology and psychiatric diagnoses such as schizophrenia and major depression (for review see torrey et al. 2007). in our large epidemiologic study we found that tg infection by serology is not more frequent in individuals with schizophrenia or major depression compared to a group of psychiatrically not affected healthy individuals controlled for age and region of provenience but the serological response is more intense in the patients than the controls (Hinze-selch et al. 2007). so, rather than just having more infected individuals among psychiatric patients as suggested by several other studies (for review see torrey et al. 2007) the host response towards the parasite might differ between patients and controls and might make a difference in this ubiquitous infection. this view is supported by the more recent data that the interaction between the host immune system, the parasitic activity and neurotransmitter systems might be responsible for the behavioural changes that can be seen even experimentally (e.g. skallová et al. 2006(e.g. skallová et al. , Henriquez et al. 2009).Briefly, TG infection in humans takes place when infectious microcysts, typically in affected undercooked or raw meat, are ingested, or through contamination with infected cat faeces (tenter et al. 2000). since the infection is However, psychiatric patients with a personality disorder have not yet been investigated systematically. in our sample containing 896 psychiatric inpatients with the primary diagnoses of schizophrenia, major depression, schizoaffective or bipolar disorder and 214 psychiatrically unaffected controls (same geographic region, sampled during same time period) we analysed for effects of the additional diagnosis of a personality disorder in the patients. Psychiatrically, a patient can meet the criteria of a personality disorder additionally to any of the mentioned primary diagnoses. We applied logistic regression and cross-table statistics, separated groups by the presence/absence of a personality disorder (icD-10) and adjusted for age between groups. We found that among all patients the additional diagnosis of a personality disorder was significantly associated with TG infectio...

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“…Even though so far the pathology caused by parasites in the brain appears widely disseminated (see Adamo, 2012;Adamo, 2013;Gulinello et al, 2010;Lefèvre et al, 2009;Vyas and Sapolsky, 2010), the reversed responses to stimuli induced by helminths in arthropods and by T. gondii in mammals imply that firing patterns are disrupted in specific sensorimotor circuits (House et al, 2011). Thus, it is essential to continue exploring the altered behavior of hosts with methods providing information on the localization of parasites' neuronal and immune effects in the CNS of manipulated hosts.…”

Section: Discussionmentioning

confidence: 99%

“…Toxoplasma gondii-infected rodents exhibit a variety of sensorimotor deficits (Gulinello et al, 2010). In particular, infected rats are specifically attracted rather than repulsed by the odor of cat urine (Berdoy et al, 2000;House et al, 2011;Vyas and Sapolsky, 2010;Vyas et al, 2007). Remarkably, cat odor activates sexual arousal pathways (House et al, 2011) in T. gondii-infected rats.…”

Section: Cerebral Parasitesmentioning

confidence: 99%

Parasite-induced alterations of sensorimotor pathways in gammarids: collateral damage of neuroinflammation?

Helluy

2013

Journal of Experimental Biology

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Manipulation of host behaviour by Toxoplasma gondii: what is the minimum a proposed proximate mechanism should explain?

Cited by 56 publications

References 46 publications

Parasite-augmented mate choice and reduction in innate fear in rats infected byToxoplasma gondii

Parasite-augmented mate choice and reduction in innate fear in rats infected byToxoplasma gondii

The diagnosis of a personality disorder increases the likelihood for seropositivity to Toxoplasma gondii in psychiatric patients

Parasite-induced alterations of sensorimotor pathways in gammarids: collateral damage of neuroinflammation?

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