Q fever is a highly infectious disease with a worldwide distribution. Its causative agent, the intracellular bacterium Coxiella burnetii, infects a variety of vertebrate species, including humans. Its evolutionary origin remains almost entirely unknown and uncertainty persists regarding the identity and lifestyle of its ancestors. A few tick species were recently found to harbor maternally-inherited Coxiella-like organisms engaged in symbiotic interactions, but their relationships to the Q fever pathogen remain unclear. Here, we extensively sampled ticks, identifying new and atypical Coxiella strains from 40 of 58 examined species, and used this data to infer the evolutionary processes leading to the emergence of C. burnetii. Phylogenetic analyses of multi-locus typing and whole-genome sequencing data revealed that Coxiella-like organisms represent an ancient and monophyletic group allied to ticks. Remarkably, all known C. burnetii strains originate within this group and are the descendants of a Coxiella-like progenitor hosted by ticks. Using both colony-reared and field-collected gravid females, we further establish the presence of highly efficient maternal transmission of these Coxiella-like organisms in four examined tick species, a pattern coherent with an endosymbiotic lifestyle. Our laboratory culture assays also showed that these Coxiella-like organisms were not amenable to culture in the vertebrate cell environment, suggesting different metabolic requirements compared to C. burnetii. Altogether, this corpus of data demonstrates that C. burnetii recently evolved from an inherited symbiont of ticks which succeeded in infecting vertebrate cells, likely by the acquisition of novel virulence factors. How virulent infectious diseases emerge from non-pathogenic organisms is a challenging question. Here, we address this evolutionary issue in the case of Q fever. Its causative agent, the intracellular bacterium Coxiella burnetii, is extremely infectious to humans and a variety of animals. However, uncertainty persists regarding its evolutionary origin, including the identity and lifestyle of its ancestors. In this article, we show that C. burnetii arose from a rare evolutionary transformation of a maternally-inherited endosymbiont of ticks into a specialized and virulent pathogen of vertebrates. While arthropod symbionts are typically transmitted maternally and thought not to be infectious to vertebrates, we establish here that one Coxiella symbiont has evolved the necessary adaptations to exploit the vertebrate cell, leading to the emergence of Q fever.

Determining patterns of host use, and the frequency at which these patterns change, are of key importance if we are to understand tick population dynamics, the evolution of tick biodiversity, and the circulation and evolution of associated pathogens. The question of whether ticks are typically host specialists or host generalists has been subject to much debate over the last half-century. Indeed, early research proposed that morphological diversity in ticks was linked to host specific adaptations and that most ticks were specialists. Later work disputed this idea and suggested that ticks are largely limited by biogeographic conditions and tend to use all locally available host species. The work presented in this review suggests that the actual answer likely lies somewhere between these two extremes. Although recent observational studies support the view that phylogenetically diverse host species share ticks when found on similar ecological ranges, theory on host range evolution predicts that host specialisation should evolve in ticks given their life history characteristics. Contemporary work employing population genetic tools to examine host-associated population structure in several tick systems support this prediction and show that simple species records are not enough to determine whether a parasite is a true host generalist; host specialisation does evolve in ticks at local scales, but may not always lead to speciation. Ticks therefore seem to follow a pattern of being global generalists, local specialists. Given this, the notion of host range needs to be modified from an evolutionary perspective, where one simply counts the number of hosts used across the geographic distribution, to a more ecological view, where one considers host use at a local scale, if we are to better understand the circulation of tick-borne pathogens and exposure risks for humans and livestock.

The ubiquity of ticks and their importance in the transmission of pathogens involved in human and livestock diseases are reflected by the growing number of studies focusing on tick ecology and the epidemiology of tick-borne pathogens. Likewise, the involvement of wild birds in dispersing pathogens and their role as reservoir hosts are now well established. However, studies on tick-bird systems have mainly focused on land birds, and the role of seabirds in the ecology and epidemiology of tick-borne pathogens is rarely considered. Seabirds typically have large population sizes, wide geographic distributions, and high mobility, which make them significant potential players in the maintenance and dispersal of disease agents at large spatial scales. They are parasitized by at least 29 tick species found across all biogeographical regions of the world. We know that these seabird-tick systems can harbor a large diversity of pathogens, although detailed studies of this diversity remain scarce. In this article, we review current knowledge on the diversity and global distribution of ticks and tick-borne pathogens associated with seabirds. We discuss the relationship between seabirds, ticks, and their pathogens and examine the interesting characteristics of these relationships from ecological and epidemiological points of view. We also highlight some future research directions required to better understand the evolution of these systems and to assess the potential role of seabirds in the epidemiology of tick-borne pathogens.

Spatial disease ecology is emerging as a new field that requires the integration of complementary approaches to address how the distribution and movements of hosts and parasites may condition the dynamics of their interactions. In this context, migration, the seasonal movement of animals to different zones of their distribution, is assumed to play a key role in the broad scale circulation of parasites and pathogens. Nevertheless, migration is not the only type of host movement that can influence the spatial ecology, evolution, and epidemiology of infectious diseases. Dispersal, the movement of individuals between the location where they were born or bred to a location where they breed, has attracted attention as another important type of movement for the spatial dynamics of infectious diseases. Host dispersal has notably been identified as a key factor for the evolution of host–parasite interactions as it implies gene flow among local host populations and thus can alter patterns of coevolution with infectious agents across spatial scales. However, not all movements between host populations lead to dispersal per se. One type of host movement that has been neglected, but that may also play a role in parasite spread is prospecting, i.e., movements targeted at selecting and securing new habitat for future breeding. Prospecting movements, which have been studied in detail in certain social species, could result in the dispersal of infectious agents among different host populations without necessarily involving host dispersal. In this article, we outline how these various types of host movements might influence the circulation of infectious disease agents and discuss methodological approaches that could be used to assess their importance. We specifically focus on examples from work on colonial seabirds, ticks, and tick-borne infectious agents. These are convenient biological models because they are strongly spatially structured and involve relatively simple communities of interacting species. Overall, this review emphasizes that explicit consideration of the behavioral and population ecology of hosts and parasites is required to disentangle the relative roles of different types of movement for the spread of infectious diseases.