Abstract
SummaryIn rodents, the decrease of felid aversion induced by Toxoplasma gondii, a phenomenon termed fatal attraction, is interpreted as an adaptive manipulation by the neurotropic protozoan parasite. With the aim of understanding how the parasite induces such specific behavioral modifications, we performed a multiparametric analysis of T. gondii-induced changes on host behavior, physiology, and brain transcriptome as well as parasite cyst load and distribution. Using a set of complementary behavioral tests, we provide strong evidence that T. gondii lowers general anxiety in infected mice, increases explorative behaviors, and surprisingly alters predator aversion without selectivity toward felids. Furthermore, we show a positive correlation between the severity of the behavioral alterations and the cyst load, which indirectly reflects the level of inflammation during brain colonization. Taken together, these findings refute the myth of a selective loss of cat fear in T. gondii-infected mice and point toward widespread immune-related alterations of behaviors.
Highlights
Innate behaviors are determinant for the survival of animals
Toxoplasma gondii Chronic Infection Triggers a Decrease in Anxiety and Enhances Exploration To get a clear overview of how T. gondii affects host behavior in general, infected mice went through a series of behavioral tests (Figure S1A; Table S2)
For all experiments described in this study, male B6CBAF1/J mice were infected by intraperitoneal (i.p.) injection of the indicated parasite strain
Summary
Innate behaviors are determinant for the survival of animals. Among these critical predetermined reactions, prey have a vital necessity to display appropriate responses, like freezing or fleeing, the very first time they encounter a predator. The parasite undergoes gametogenesis in the felid intestine, and the infectious oocysts resulting from sexual reproduction are shed off by the feces into the environment These oocysts are taken up by warm-blooded animals, including mammals, marsupials, and birds, constituting a very large pool of intermediate hosts (Lindsay and Dubey, 2014). T. gondii is known to alter the innate aversion to felid odors (Berdoy et al, 2000; Hammoudi and Soldati-Favre, 2017; Vyas, 2015; Vyas et al, 2007) This latter aspect of T. gondii parasitism is referred to as the ‘‘fatal attraction phenomenon,’’ which refers to the ability of the parasite to manipulate its intermediate host that becomes attracted to felids, facilitating parasite spreading. The decreased aversion to felids is seemingly not resulting from an impairment of olfactory faculties (Berdoy et al, 1995; Torres et al, 2018) but appears to be a consequence of complex neuronal and physiological mechanisms altering the perception of the host when facing a predation
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