Time Makes You Older, Parasites Make You Bolder — Toxoplasma Gondii Infections Predict Hyena Boldness toward Definitive Lion Hosts

There is growing interest in the alteration of host behaviors by parasites, yet crucial gaps remain in our understanding of its ecological and evolutionary significance. Here, we present the first evidence that the enhanced boldness of infected intermediate hosts of Toxoplasma gondii can increase their risk of mortality by the parasite’s definitive feline hosts. In a long-term study of hyenas in Kenya’s Masai Mara region, we found that 65% of hyenas were seropositive for T. gondii in ELISA IgG assays. Seropositive hyenas approached lions more closely than uninfected counterparts, and also showed longer latencies to approach a simulated conspecific territorial intruder. Lastly, although not significant, the ratio of mortalities caused by lions (vs. other sources) was higher for hyenas that were infected by T. gondii. These results accord with a long-standing hypothesis that the manipulation of host boldness and/or ailurophilia evolved to enhance disease transmission. Since hyenas are rarely consumed by lions, however, elevating their boldness toward lions may not be adaptive for T. gondii. Instead, it may reflect “collateral manipulation” that evolved to influence homologous mechanisms underlying behaviors of alternative hosts (e.g. rodents). This model is often invoked to explain T. gondii’s many effects in humans, but is virtually unexplored in natural settings. For T. gondii, these effects could feasibly impact both behavior and fitness in a vast array, and significant proportion, of earth’s mammals and birds. In addition to characterizing behavioral covariates of infection, we examined spatial and temporal patterns of T. gondii prevalence within the Mara landscape. Contrary to our predictions, disease prevalence did not differ 1) at a protected vs. disturbed locality, or 2) over three decades of increasing human activity within the disturbed locality.