Abstract
The apicomplexan parasite Toxoplasma gondii, the causative agent of toxoplasmosis, can infect all warm-blooded animals. T. gondii can subtly alter host behaviors—either through manipulation to enhance transmission to the feline definitive host or as a side-effect, or “constraint,” of infection. In humans, T. gondii infection, either alone or in association with other co-infecting neurotropic agents, has been reliably associated with both subtle behavioral changes and, in some cases, severe neuropsychiatric disorders, including schizophrenia. Research on the potential impact of T. gondii on the behavior of other long-lived naturally infected hosts is lacking. Recent studies reported a large number of wild red foxes exhibiting a range of aberrant behavioral traits, subsequently classified as Dopey Fox Syndrome (DFS). Here we assessed the potential association between T. gondii and/or other neurotropic agents with DFS. Live, captive foxes within welfare centers were serologically tested for T. gondii and, if they died naturally, PCR-tested for vulpine circovirus (FoxCV). Post-mortem pseudo-control wild foxes, obtained from pest management companies, were PCR-tested for T. gondii, FoxCV, canine distemper virus (CDV), canine adenovirus type (CAV)-1 and CAV-2. We also assessed, using non-invasive assays, whether T. gondii–infected foxes showed subtle behavioral alterations as observed among infected rodent (and other) hosts, including altered activity, risk, and stress levels. All foxes tested negative for CAV, CDV, CHV, and DogCV. DFS was found to be associated with singular T. gondii infection (captives vs. pseudo-controls, 33.3% (3/9) vs. 6.8% (5/74)) and singular FoxCV infection (66.7% (6/9) vs. 11.1% (1/9)) and with T. gondii/FoxCV co-infection (33.3% (3/9) vs. 11.1% (1/9)). Overall, a higher proportion of captive foxes had signs of neuroinflammation compared to pseudo-controls (66.7% (4/6) vs. 11.1% (1/9)). Consistent with behavioral changes seen in infected rodents, T. gondii–infected foxes displayed increased attraction toward feline odor (n=6 foxes). These preliminary results suggest that wild foxes with DFS are infected with T. gondii and likely co-infected with FoxCV and/or another co-infecting neurotropic agent. Our findings using this novel system have important implications for our understanding of both the impact of parasites on mammalian host behavior in general and, potentially, of the infectious causation of certain neuropsychiatric disorders.
Highlights
The ability of parasites to alter the behavior of their hosts fascinates both scientists and non-scientists alike
(Co)-Infection With Other Neurotropic Agents To test the hypothesis that the aberrant behavior of foxes with Dopey Fox Syndrome (DFS) is associated with infection with a neurotropic agent other than T. gondii, either alone or in combination with T. gondii, we developed a multiplex assay which was performed on nucleic acid extracted from 18 fox brains
To test whether DFS was associated with T. gondii infection, we compared the prevalence of infection in captive to pseudocontrol populations
Summary
The ability of parasites to alter the behavior of their hosts fascinates both scientists and non-scientists alike. While there are numerous examples of parasite-altered behavior among invertebrate hosts [1], there remain few clear examples of vertebrate host-parasite systems, despite their potential profound theoretical and applied implications. Between 20% and 80% of the global human population are thought to be seropositive [2] Cats and their wild relatives (Felidae) are the only known definitive hosts of T. gondii. The localization of T. gondii in the brain may be predicted to alter the behavior of other infected secondary host species. In this case, behavioral alterations do not occur via selective manipulation to enhance transmission but do so as a “byproduct” of infection, even if of no current adaptive value to the parasite. From an evolutionary selection perspective, the latter can be referred to as “parasite constraint” rather than “parasite manipulation” [9]
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