Morbid attraction to leopard urine in Toxoplasma-infected chimpanzees

Abstract

Parasites are sometimes capable of inducing phenotypic changes in their hosts to improve transmission [1]. Toxoplasma gondii, a protozoan that infects a broad range of warm-blooded species, is one example that supports the so-called 'parasite manipulation hypothesis': it induces modifications in rodents' olfactory preferences, converting an innate aversion for cat odor into attraction and probably favoring trophic transmission to feline species, its only definitive hosts [2]. In humans, T. gondii induces behavioral modifications such as personality changes, prolonged reaction times and decreased long-term concentration [3]. However, modern humans are not suitable intermediate hosts because they are no longer preyed upon by felines. Consequently, behavioral modifications in infected people are generally assumed to be side effects of toxoplasmosis or residual manipulation traits that evolved in appropriate intermediate hosts. An alternative hypothesis, however, states that these changes result from parasite manipulative abilities that evolved when human ancestors were still under significant feline predation [3,4]. As such, T. gondii also alters olfactory preferences in humans; infected men rate cat urine, but not tiger urine, as pleasant while non-infected men do not [5]. To unravel the origin of Toxoplasma-induced modifications in humans, we performed olfactory tests on a living primate still predated by a feline species. We found in our closest relative, the chimpanzee (Pan troglodytes troglodytes), that Toxoplasma-infected (TI) animals lost their innate aversion towards the urine of leopards (Panthera pardus), their only natural predator. By contrast, we observed no clear difference in the response of TI and Toxoplasma-non-infected (TN) animals towards urine collected from other definitive feline hosts that chimpanzees do not encounter in nature. Although the adaptive value of parasitically induced behavior should be assessed carefully, we suggest that the behavioral modification we report could increase the probability of chimpanzee predation by leopards for the parasite's own benefit. This possible parasite adaptation would hence suggest that Toxoplasma-induced modifications in modern humans are an ancestral legacy of our evolutionary past.

Effects of latent toxoplasmosis on olfactory functions of men and women

“…Toxoplasma-infected subjects rate the pleasantness of smell of highly diluted urine of the definitive host of Toxoplasma, the cat, but not the pleasantness of smell of urine of other four species, differently than the non-infected controls (Flegr et al, 2011). Namely, the Toxoplasma infected men rated this smell as more pleasant, which recalls the well-known "fatal attraction phenomenon" observed in infected rodents (Berdoy et al, 2000;Vyas et al, 2007a) and chimpanzee (Poirotte et al, 2016), while the Toxoplasma-infected women rate the smell of the diluted cat urine as less pleasant. The change of the natural fear of the smell of cat predators of animals towards an attraction to this smell after the Toxoplasma infection is considered to be the product of manipulation activity of the Toxoplasma aimed to increase the chance of its transmission from the intermediate to definitive host by predation.…”

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

“…Does, for example, the changed response of infected men to cat odor (Flegr et al, 2011) mean that the parasite elicits the correct behavior in the wrong host, or does it mean that humans and their feline predators were important hosts during the evolution of T. gondii? The last interpretation gains some support from the observation that Toxoplasma-infected chimpanzees exhibit fatal attraction to leopard urine (Poirotte et al, 2016).…”

“…"Fatal attraction" has been observed for mammalian hosts that carry the protozoon Toxoplasma gondii: infected mammals enhance their exposure to feline predators, infected males become sexually more attractive to healthy females, and men with latent toxoplasmosis become more risk-taking and aggressive (Poulin, 2010;Hari Dass et al, 2011;Adamo, 2013;Flegr, 2013a;Weinersmith and Faulkes, 2014;Poirotte et al, 2016).…”

“…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).…”

Behavioral Changes Induced by Toxoplasmosis in Animals and Humans.

“…The findings in these primates support the theory that the parasite also modulates the behavior of humans, especially when they are encased in the amygdala of the 2011 limbic system, a region of the encephalon that is fundamental to self-preservation because it is the center of danger. (POIROTTE et al, 2016).…”