Fatal Attraction Phenomenon in Humans – Cat Odour Attractiveness Increased for Toxoplasma-Infected Men While Decreased for Infected Women

Abstract

BackgroundLatent toxoplasmosis, a lifelong infection with the protozoan Toxoplasma gondii, has cumulative effects on the behaviour of hosts, including humans. The most impressive effect of toxoplasmosis is the “fatal attraction phenomenon,” the conversion of innate fear of cat odour into attraction to cat odour in infected rodents. While most behavioural effects of toxoplasmosis were confirmed also in humans, neither the fatal attraction phenomenon nor any toxoplasmosis-associated changes in olfactory functions have been searched for in them.Principal FindingsThirty-four Toxoplasma-infected and 134 noninfected students rated the odour of urine samples from cat, horse, tiger, brown hyena and dog for intensity and pleasantness. The raters were blind to their infection status and identity of the samples. No signs of changed sensitivity of olfaction were observed. However, we found a strong, gender dependent effect of toxoplasmosis on the pleasantness attributed to cat urine odour (p = 0.0025). Infected men rated this odour as more pleasant than did the noninfected men, while infected women rated the same odour as less pleasant than did noninfected women. Toxoplasmosis did not affect how subjects rated the pleasantness of any other animal species' urine odour; however, a non-significant trend in the same directions was observed for hyena urine.ConclusionsThe absence of the effects of toxoplasmosis on the odour pleasantness score attributed to large cats would suggest that the amino acid felinine could be responsible for the fatal attraction phenomenon. Our results also raise the possibility that the odour-specific threshold deficits observed in schizophrenia patients could be caused by increased prevalence of Toxoplasma-infected subjects in this population rather than by schizophrenia itself. The trend observed with the hyena urine sample suggests that this carnivore, and other representatives of the Feliformia suborder, should be studied for their possible role as definitive hosts in the life cycle of Toxoplasma.

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

“…The commonly observed increase in testosterone levels in infected male rats involves an increase in the expression of those receptors in the testes that regulate the synthesis of testosterone (Lim et al, 2013). This finding might explain why enhanced levels of testosterone have been observed only in infected men (Flegr et al, 2008;Shirbazou et al, 2011), and for the multiple behavioral and psychological traits in which men and women with latent toxoplasmosis exhibit opposite trends (Flegr et al, 2011;Flegr, 2013b). Recently, T. gondii has been reported to hypomethylate the arginine vasopressin promoters in the medial amygdala of rats (Hari Dass and Vyas, 2014), an epigenetic manipulation that could cause a stronger activation of vasopressinergic neurons after exposure to cat odor (Flegr and Markos, 2014).…”

“…However, it remains an open question whether and to what degree these findings are also applicable to the brain of infected humans and, more importantly, the relevance of these effects in the interaction of the natural intermediate hosts with the natural final hosts of T. gondii has yet to be determined. 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).…”

The Relation ofToxoplasmaInfection and Sexual Attraction to Fear, Danger, Pain, and Submissiveness

“…We suppose that these personality traits could result in observed differences in reported sexual preferences and activities. It was observed that Toxoplasma-infected male subjects and male rats had higher level of testosterone (Flegr, Lindová, & Kodym, 2008;Vyas, 2013). Vyas and his group have shown that Toxoplasma upregulates the synthesis of this hormone by increasing the number of luteinizing hormone receptors on Leydig cells, that is, the receptors that regulate the synthesis of testosterone in testes (Lim, Kumar, Hari Dass, & Vyas, 2013).…”

“…The most remarkable toxoplasmosis-associated behavioral change is the so-called fatal attraction phenomenon-the switch from the mice's and rats' native fear of the smell of cats toward an attraction to this smell (Berdoy, Webster, & Macdonald, 2000). The existence of this phenomenon has been observed in mice and rats in about 20 studies performed in several laboratories worldwide and its analogy, higher ratings of attractiveness of smell of highly diluted cat (but not other species) urine was observed even in humans (Flegr, Lenochová, Hodný, & Vondrová, 2011). The neurological mechanism of this change in rats was revealed recently.…”

Toxoplasma gondiiinfection, from predation to schizophrenia: can animal behaviour help us understand human behaviour?

“…For instance, one may suspect that T. gondii-induced meningoencephalitis [including within immunocompetent adult hosts (Kaushik et al, 2005)] and brain cancer (Thomas et al, 2012) (Flegr, 2007;Flegr, 2013;Flegr et al, 2002;Flegr and Hrdy, 1994;Flegr et al, 2003;Webster, 2001). Even an equivalent of the fatal feline attraction phenomenon observed in infected rats (Berdoy et al, 2000) has been identified in humans, where T. gondii-positive humans showed altered questionnaire responses to the odours of the domestic cat (and of the brown hyena) (Flegr et al, 2011). Such subtle changes in human behaviour and personality in response to latent T. gondii infection at the individual level have even been proposed to alter the human aggregate personality at the population level (Lafferty, 2006).…”