Borraz-León JI, Rantala MJ, Krams IA, Cerda-Molina AL, Contreras-Garduño J. 2022. Are Toxoplasma-infected subjects more attractive, symmetrical, or healthier than non-infected ones? Evidence from subjective and objective measurements. PeerJ 10:e13122. Mar 2022. https://doi.org/10.7717/peerj.13122
Abstract
Background: Parasites are among the main factors that negatively impact the health and reproductive success of organisms. However, if parasites diminish a host’s health and attractiveness to such an extent that finding a mate becomes almost impossible, the parasite would decrease its odds of reproducing and passing to the next generation. There is evidence that Toxoplasma gondii (T. gondii) manipulates phenotypic characteristics of its intermediate hosts to increase its spread. However, whether T. gondii manipulates phenotypic characteristics in humans remains poorly studied. Therefore, the present research had two main aims: (1) To compare traits associated with health and parasite resistance in Toxoplasma-infected and non-infected subjects. (2) To investigate whether other people perceive differences in attractiveness and health between Toxoplasma-infected and non-infected subjects of both sexes.
Methods: For the first aim, Toxoplasma-infected (n = 35) and non-infected subjects (n = 178) were compared for self-perceived attractiveness, number of sexual partners, number of minor ailments, body mass index, mate value, handgrip strength, facial fluctuating asymmetry, and facial width-to-height ratio. For the second aim, an independent group of 205 raters (59 men and 146 women) evaluated the attractiveness and perceived health of facial pictures of Toxoplasma-infected and non-infected subjects.
Results: First, we found that infected men had lower facial fluctuating asymmetry whereas infected women had lower body mass, lower body mass index, a tendency for lower facial fluctuating asymmetry, higher self-perceived attractiveness, and a higher number of sexual partners than non-infected ones. Then, we found that infected men and women were rated as more attractive and healthier than non-infected ones.
Conclusions: Our results suggest that some sexually transmitted parasites, such as T. gondii, may produce changes in the appearance and behavior of the human host, either as a by-product of the infection or as the result of the manipulation of the parasite to increase its spread to new hosts. Taken together, these results lay the foundation for future research on the manipulation of the human host by sexually transmitted pathogens and parasites.
Discussion
For the first hypothesis, we found that Toxoplasma-infected subjects had lower facial FA than non-infected ones. Broken out by sex, we found that Toxoplasma-infected men had lower facial FA than non-infected men, whereas Toxoplasma-infected women had lower body mass, lower BMI, and a tendency to lower facial FA, higher self-perceived attractiveness, and a higher number of sexual partners than non-infected ones. Previous studies have reported positive associations between symmetrical traits, health, good genes, attractiveness, and parasitic resistance both in humans and non-human animals (e.g., Møller, 1992; Gangestad, Thornhill & Yeo, 1994; Polak, 1997; Borráz-León et al., 2021b; Luoto et al., 2021). Thus, one possible explanation for our results is that highly symmetrical subjects can successfully afford the physiological costs related to parasitism, which supports the hypothesis that highly symmetrical features are honest signals of good health (Borráz-León, Cerda-Molina & Mayagoitia-Novales, 2017; Luoto et al., 2021, but see Pound et al., 2014). Another possibility is that T. gondii infection may produce changes in facial symmetry of its hosts through changes in endocrinological variables such as testosterone levels; this hypothesis is consistent with the finding that Toxoplasma-infected men have higher testosterone levels (Flegr, Lindová & Kodym, 2008; Borráz-León et al., 2021a) and Toxoplasma-infected women have lower testosterone levels than non-infected subjects (Flegr, Lindová & Kodym, 2008), as well as with some data showing that body symmetry can change due to hormonal fluctuations across the menstrual cycle (Scutt & Manning, 1996; but see Marcinkowska & Holzleitner, 2020). These changes, both in the endocrinology system and in facial symmetry, would ultimately benefit the spread of the parasite by increasing the attractiveness of its hosts through increasing their facial symmetry. This hypothesis is also consistent with previous results showing that Toxoplasma-infected male rats have higher testosterone levels and are preferred as sexual partners by non-infected females (Dass et al., 2011), and with positive relationships between high testosterone levels, attractiveness, and immune responses in men (Rantala et al., 2012; Luoto et al., 2021). However, this hypothesis must be empirically tested further since other studies have found no direct associations between testosterone levels and facial symmetry (e.g., Borráz-León et al., 2014).
Regarding the lower body mass and the lower BMI of Toxoplasma-infected women, it is important to highlight that the values of both physical measurements are within what is considered “normal” and healthy (Brown et al., 2016). These results support the view that T. gondii might also increase the metabolic rate of its hosts which would influence their health and attractiveness perceptions. The tendency for reporting higher self-perceptions of attractiveness and a higher number of sexual partners among Toxoplasma-infected women is consistent with this explanation since the acquisition of sexual partners through more active mate-seeking, short-term sociosexual orientation, and higher attractiveness would facilitate the spread of T. gondii to new hosts. Another possibility is that Toxoplasma-infected subjects from both sexes are showing more attractive characteristics as a terminal investment strategy (e.g., Fessler et al., 2005). Nevertheless, this hypothesis is less plausible since there were no significant age differences between Toxoplasma-infected and non-infected subjects.
Regarding the second hypothesis, we found that other-perceptions of attractiveness and health are higher for Toxoplasma-infected subjects than for non-infected ones, independent of their sex. Moreover, the BMI and pathogen disgust of raters modulated the attractiveness and health perceptions of infected and non-infected subjects indistinctly. Interestingly, there also was a tendency for raters who had lower pathogen disgust and higher self-rated health to evaluate the faces of Toxoplasma-infected subjects as healthier than the faces of non-infected ones. Likewise, those raters with lower sexual disgust also tended to evaluate Toxoplasma-infected subjects as more attractive than non-infected ones. These results support and extend previous literature showing that, for example, Toxoplasma-infected male rats are preferred as sexual partners by females (Dass et al., 2011). Thus, it is possible that the same effect reported for Toxoplasma-infected male rats is present in Toxoplasma-infected humans. This effect may be modulated by phenotypic characteristics of potential mates such as disgust sensitivity and self-perceived health (e.g., Park, van Leeuwen & Stephen, 2012).
At this point, it is important to highlight that even though between 30% and 80% of the global population may be infected with T. gondii (e.g., Flegr, 2007; Johnson & Johnson, 2020), with transmission routes including contact with cat feces, contaminated food or water, or sexual intercourse with an infected person (Flegr, 2007; Flegr & Horáček, 2019; Tong et al., 2021), only a meager percentage of subjects (mainly those who are immunosuppressed) may develop severe complications associated with the infection (Johnson & Johnson, 2020). Likewise, a low percentage of infected subjects may develop mental disorders such as schizophrenia, obsessive-compulsive disorder, or suicidal tendencies (Flegr & Horáček, 2019; Torrey & Yolken, 2019; Nayeri, Sarvi & Daryani, 2022). However, it seems that exposure to previous traumatic experiences, chronic stress, genetic predisposition, drugs abuse, as well as Toxoplasma and other pathogen infections (e.g., Cytomegalovirus, herpes, Clamydia spitacci, Treponema pallidum) are all involved in the development of these mental disorders (MJ Rantala et al., 2021, unpublished data). In immunocompetent subjects, Toxoplasma infection may cause mild disease and usually turns into life-long latent toxoplasmosis being clinically asymptomatic (Roberts et al., 2001). Therefore, it is possible that the apparently non-pathological and potentially beneficial interactions between T. gondii and some of its intermediate hosts, such as rats and humans are the result of co-evolutionary strategies that benefit, or at least do not harm, the fitness of both the parasite and the host.
Some examples of parasites that manipulate the appearance and behavior of their hosts to increases their attractiveness have been previously described in nature. For example, female moths of Helicoverpa zea infected with gonad-specific virus (GSV) or Hz-2V virus produce three to seven times more sex pheromone than non-infected females which could increase their sexual attractiveness (Burand et al., 2005). Likewise, water snails (Potamopyrugus antipodarum) infected with a trematode (Microphallus sp.) enhance their sexual attractiveness measured by an increase in the number of mating events and the total number of different mating partners (Soper et al., 2014). Even though reports about host manipulation by sexually transmitted pathogens and the potential benefits these pathogens could gain remain scarce in humans (e.g., Heil, 2016). The present study offers novel evidence supporting the idea that some sexually transmitted parasites such as T. gondii (e.g., Hlaváčová et al., 2020; Tong et al., 2021), may produce changes in the appearance and behavior of the human host, either as a by-product of the infection or as the result of the manipulation of the parasite to increase its spread to new hosts.
Limitations and future directions
The small sample size of the present study may have been an important limiting factor for finding statistical differences in the other studied phenotypic traits. Therefore, further studies with larger sample sizes must be carried out to confirm or reject the hypotheses tested in this study. Another limitation is that in the present study, physiological, immunological, and/or genetic markers associated with health were not directly measured. Although previous research has shown the advantages of using phenotypic over genotypic measurements of immune function and health (e.g., Luoto et al., 2021), future research must take the present limitations into account to offer a more complete explanation about how T. gondii may manipulate hosts’ behavior, morphology, and/or physiology.
Since reports that T. gondii can be a sexually transmitted parasite in humans are relatively recent (e.g., Flegr, Klapilová & Kaňková, 2014; Hlaváčová et al., 2020; Kaňková, Hlaváčová & Flegr, 2020; Tong et al., 2021), many questions and hypotheses still need to be properly formulated and tested in further studies. In this study, we provided the first evidence that Toxoplasma-infected individuals are more symmetrical and are perceived as more attractive and healthier than non-infected ones. Thus, further research can investigate, for example, the effect of Toxoplasma-status of raters on sociosexual orientation characteristics. It is possible that Toxoplasma-infected individuals may rate more positively the faces of potential mates which would benefit the spread of T. gondii by making them less choosy and probably exhibiting a short-term over a long-term sociosexual orientation. The effect of the menstrual cycle phase is another variable that have to be further studied. It could be possible that Toxoplasma-infected women who are in the fertile phase of the menstrual cycle, rate even more positively the faces of potential mates than Toxoplasma-infected women who are in other phase of the menstrual cycle, since changes in attractiveness perceptions during the menstrual cycle have been previously reported (e.g., Gangestad et al., 2007; Jones et al., 2008). Other future studies can look for differences in ejaculate quality between Toxoplasma-infected and non-infected men. Since T. gondii infection produces changes in testosterone levels, it is feasible that these changes may also affect some ejaculate parameters such as motility, sperm velocity, or ejaculate volume. In general, if the premises of the manipulation hypothesis by T. gondii are correct, such effects would increase its transmission rate to new hosts. Further research is also needed to study potential metabolic and physiological costs associated with Toxoplasma infection. For example, it is likely that the phenotypic changes of Toxoplasma-infected subjects such as lower facial FA, higher testosterone levels, and high-risk behaviors reported in this and other studies (Flegr, 2007; Johnson et al., 2018; Borráz-León et al., 2021a), may impose physiological costs to the host such as shortened life, reduced life quality during late adulthood, or increased predisposition to develop organic (e.g., hearth and pulmonary diseases) and mental diseases (e.g., depression, schizophrenia, bipolar disorder). Therefore, covariation between attractiveness, facial symmetry, changes in sex hormones and neurotransmitters, and the expression of physical and psychopathological symptoms, might be expected in genetically predisposed individuals. In the aggregate these research suggestions can shed light on the effects of Toxoplasma infection in human sociosexual and health domains.