Why such a contrast between the low prevalence of zoonotic pathogens in questing ticks and the high prevalence in their vertebrate reservoir hosts?

International audienceIn a context of emerging or re‐emerging tick‐borne diseases, many studies have measured the prevalence of zoonotic agents in hosts and vectors, using cross‐sectional protocols at different spatial scales. Surprisingly, a frequent contrast occurs between a high prevalence in the vertebrate hosts and a low prevalence in questing ticks. Furthermore, investigations on the species of the genera Anaplasma, Babesia and Borrelia have shown that several taxa co‐circulate and are maintained in vertebrate host populations. Indeed, the co‐infection of the individual vertebrate host by several taxa and genetic variants is the rule, rather than the exception. Based on a review of recent papers on ticks and tick‐borne diseases, we hypothesize that high and repeated exposure to ticks under natural conditions causes the frequent re‐infection of vertebrates with a diversity of tick‐transmitted taxa, leading to a high overall prevalence of infections and co‐infections. However, the immunity induced by this frequent exposure could keep the intensity of co‐infections by different strains of the same taxa at a low level within individual hosts, which in turn could lead to a low frequency of acquisition by the ticks during bloodmeals. Furthermore, in order to complete their life‐cycle, the tick‐transmitted organisms need also to resist the tick innate immunity, to compete with its microbiote and to be able to colonize the salivary glands of the vector. Facing these successive selective pressures, the maintenance of the infections in the host populations can be achieved only if ticks are abundant, to compensate for a low prevalence in tick populations. We argue that a meta‐community approach taking into account the functional traits of the different pathogen taxa and their intra‐taxa diversity is required to fully understand the dynamic interplay between the actors of the pathosystem and the potential emergence of pathogenic strain