Exploring the dynamic adult hard ticks-camel-pathogens interaction.

Abstract

The ability of ticks to interact and adapt to different ecologies and hosts determines their vectorial competence for various pathogens; however, ticks-livestock-pathogens interaction studies are limited. With our ticks-hosts-pathogens interface studies, we found 14 species of hard ticks feeding on various livestock. Ticks showed a strong preference for one-humped camels (Camelus dromedarius). The camel nostril was the most preferred predilection site. The most prevalent tick species on camels was Hyalomma rufipes. We found two novel Amblyomma gemma variants which are distinct both morphologically and genetically from previously described Amblyomma gemma. The signature odors from camel breath and body were attractive to adult H. rufipes, demonstrating ticks utilize camel-derived metabolites to find their host. Our research shows that H. rufipes and camel hosts have unique and shared pathogens showing H. rufipes' vector and dromedary camel's reservoir host qualities. Our study unravels the dynamic interactions between hard ticks, pathogens, and host camels that all influence the likelihood of pathogen adaptation and transmission dynamics.

Importance: Ticks are obligatory hematophagous arachnids, serving as vectors for a wide array of pathogens that can be transmitted to animals and humans. The ability of ticks to acquire and transmit various pathogens depends on their attraction to quality reservoir hosts and the survival of the pathogens in ticks' gut and other tissues. However, the complex dynamics of tick-pathogen interaction and host-seeking behavior remain understudied. This investigation revealed notable variation in tick preference for domestic animals, with camel being the most preferred host. Moreover, our spatial analysis of tick attachment sites showed nostrils are the most preferred sites by various tick species. Our epidemiology data showed variation in the pathogens harbored by camel (host) and vector (Hyalomma rufipes), demonstrating the camel's efficiency as reservoir host and ticks' vector competence for various pathogens. With our behavioral experiment using H. rufipes and its preferred host's (camel) breath and body signature odors, we identified novel attractants for H. rufipes, thus offering new avenues for combating tick-borne diseases. Overall, our study presents novel insights into how multiple factors shape tick-host-pathogen interaction.