Change in Human Social Behavior in Response to a Common Vaccine
Introduction
Animals infected with pathogens rarely behave like uninfected animals. In some cases, the behavior of infected individuals is self-protective (e.g., behavioral fever, sickness behavior), and in other cases, it benefits the parasite (e.g., increases transmission or parasite survival). Klein (1) reviews the extensive evidence for parasitic influence on proximate mechanisms that mediate host social behavior.
From an evolutionary point of view, infection can be seen as a dynamic battle between a parasite/pathogen and host. Features characteristic of infection are similar to the tools of war; they are the products of evolved strategies that benefitted one side or the other. Whereas behavioral changes in response to infection are almost ubiquitous among vertebrates, the adaptive significance of such behavioral change is often difficult to ascertain—that is, it remains unclear whether the effect benefits the parasite or the host, and if there is a benefit, how it is achieved. What is clear is that the behavior of infected animals does not resemble that of uninfected conspecifics, and the difference has implications for both the individual host and the movement of the pathogen through the host population (2).
The gold standard for demonstrating parasite-induced behavioral change is experimental infection, and reasonably, such studies are not often carried out on humans. Thus, despite abundant examples of behavioral change in nonhuman animals infected with parasites, evidence for parasite-induced behavioral change in humans is virtually nonexistent, except for diseases that directly involve the nervous system or musculature (e.g., rabies; see also Moore (2)). Of course, Toxoplasma gondii is well known for its association with certain personality traits (3), but again, infection was neither experimental nor randomly distributed over the study population; we cannot rule out the possibility that certain personality types are more prone to be exposed or susceptible to Toxoplasma. Despite these difficulties in the study of human disease and behavior, we nonetheless expect to see behavioral changes in infected humans, given the ubiquity of such changes in other taxa.
With that expectation, we asked if exposure to a directly transmitted pathogen—flu virus—would affect the behavior of humans. We focused on social behavior because enhanced social behavior could potentially benefit either (or both) the parasite or the host. Parasites that manipulate hosts to increase social behavior may benefit through increased transmission; hosts that increase their social contacts might benefit through increased care from conspecifics. Thus, we hypothesized that on encountering flu virus, humans would increase their social behavior.
Seasonal influenza is a representative, common, directly-transmitted human infection. According to the United States Center for Disease Control (4), the average time between exposure to seasonal influenza and symptom onset is 2 days (range: 1–4 days), and infected individuals are contagious a day before symptom onset and for several days thereafter (Fig. 1). Shedding of the virus peaks 2 days after exposure, and symptom scores peak on Day 3 (5). Once symptoms appear, transmission via social interactions may be reduced by the onset of sickness behavior. However, no sickness behavior is evident presymptomatically, making the social behavior of infected individuals at this time particularly important.
Section snippets
Methods
Because of the inherent complications of experimental infection studies with humans, we sought an alternative method of identifying exposure to influenza. Many humans are exposed to a modified form of influenza virus every autumn in the form of flu vaccines. Although the immunization rarely produces full-fledged sickness behavior or illness, its very success depends on the recipient’s body recognizing the antigenic threat and mounting an appropriate immune response. We therefore used influenza
Results
Compared to the 2 days pre-immunization, the 2 days post-immunization were characterized by increased social behavior. Whereas the total number of social events per participant did not change significantly from pre- to post-immunization (19.5 vs. 22.0 events; ranges 218 and 79, respectively; z = 1.02, n = 35, p = 0.31), the total number of individuals with whom each participant interacted increased dramatically from 54 to 101 people (ranges 235 and 2078, respectively; z = 3.08, n = 35, p =
Discussion
In the 2 days immediately after influenza immunization, study participants socially encountered almost twice as many other humans as they did in the 2 days before immunization. Participants were not consciously aware of any changes in their levels of sociability, nor could the changes in their social behavior be accounted for by differences in social patterns associated with particular days of the week. Human social behavior changed on the introduction of viral antigens.
There are some
Conclusions
To our knowledge, this is the strongest indicator yet discovered of pathogen-mediated behavioral change in otherwise asymptomatic humans. Our results unambiguously point to increased social interaction after exposure. Much remains to be investigated regarding this interaction, and future directions include planned placebo-controlled trials, investigations of the effect of unattenuated virus on human social behavior, and investigations of other directly transmitted human pathogens. If this
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