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.

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 specialization 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 specialization 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.

Since neutropenic patients with hematological malignancies are at high risk of contracting life-threatening infections, specific markers of infection are needed in cases of febrile neutropenia. The study presented here assessed serum concentrations of C-reactive protein (CRP), procalcitonin (PCT) and interleukin-6 (IL-6) in samples obtained from 31 febrile neutropenic patients. A total of 53 episodes were evaluated, and 18 of these were associated with positive blood culture results. Procalcitonin and IL-6 concentrations differed significantly between bacteremic and non-bacteremic episodes. Procalcitonin values were 0.22 ng/ml [interquartile range (IR), 0.15-1.9] for patients with pneumonia without bacteremia, 0.22 ng/ml (IR, 0.16-0.55) for patients with fever of unknown origin, 0.2 ng/ml (IR, 0.13-0.57) for patients with non-microbial fever and 1.8 ng/ml (IR, 0.35-5.3) for patients with bacteremia. The differences between bacteremic and non-bacteremic episodes had a P-value of 0.003 using the Mann-Whitney test. For IL-6 the median values were 301 pg/ml (IR, 152-1,879) for patients with pneumonia without bacteremia, 207 pg/ml (IR, 94-445) for patients with fever of unknown origin, 177 pg/ml (IR, 142-208) for patients with non-microbial fever and 942 pg/ml (IR, 181-2,807) for patients with bacteremia. Using the Mann-Whitney test, the differences between bacteremic and non-bacteremic episodes were P=0.006. No differences were found in CRP concentrations. Cutoff levels to distinguish between bacteremic and non-bacteremic episodes were chosen using receiver operating characteristic curves: 0.62 ng/ml for PCT and 297 pg/ml for IL-6. Negative predictive values were 84% for PCT and 70% for IL-6. The results indicate that PCT and IL-6 are more reliable markers than CRP for predicting bacteremia in patients with febrile neutropenia.

Bats are reservoirs for several zoonotic pathogens of medical importance; however, infection dynamics of pathogens in wild bat populations remain poorly understood. Here, we examine the influence of host crowding and population age structure on pathogen transmission and diversity in bat populations. Focusing on two pathogen taxa of medical importance, Leptospira bacteria and paramyxoviruses, we monitored host population and pathogen shedding dynamics within a maternity colony of the tropical bat species Mormopterus francoismoutoui, endemic to Réunion Island. Our data reveal astonishingly similar infection dynamics for Leptospira and paramyxoviruses, with infection peaks during late pregnancy and 2 months after the initial birth pulse. Furthermore, although co-infection occurs frequently during the peaks of transmission, the patterns do not suggest any interaction between the two pathogens. Partial sequencing reveals a unique bat-specific Leptospira strain contrasting with the co-circulation of four separate paramyxovirus lineages along the whole breeding period. Patterns of infection highlight the importance of host crowding in pathogen transmission and suggest that most bats developed immune response and stop excreting pathogens. Our results support that bat maternity colonies may represent hot spots of transmission for bacterial and viral infectious agents, and highlight how seasonality can be an important determinant of host-parasite interactions and disease emergence.

Biodiversity hotspots and associated endemism are ideal systems for the study of parasite diversity within host communities. Here, we investigated the ecological and evolutionary forces acting on the diversification of an emerging bacterial pathogen, Leptospira spp., in communities of endemic Malagasy small mammals. We determined the infection rate with pathogenic Leptospira in 20 species of sympatric rodents (subfamily Nesomyinae) and tenrecids (family Tenrecidae) at two eastern humid forest localities. A multilocus genotyping analysis allowed the characterization of bacterial diversity within small mammals and gave insights into their genetic relationships with Leptospira infecting endemic Malagasy bats (family Miniopteridae and Vespertilionidae). We report for the first time the presence of pathogenic Leptospira in Malagasy endemic small mammals, with an overall prevalence of 13%. In addition, these hosts harbour species of Leptospira (L. kirschneri, L. borgpetersenii and L. borgpetersenii group B) which are different from those reported in introduced rats (L. interrogans) on Madagascar. The diversification of Leptospira on Madagascar can be traced millions of years into evolutionary history, resulting in the divergence of endemic lineages and strong host specificity. These observations are discussed in relation to the relative roles of endemic vs. introduced mammal species in the evolution and epidemiology of Leptospira on Madagascar, specifically how biodiversity and biogeographical processes can shape community ecology of an emerging pathogen and lead to its diversification within native animal communities.

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International audienceA growing number of recent studies have highlighted bats as a reservoir for Leptospira bacteria, pointing out the potential role of bats in the epidemiology of the most widespread zoonotic disease in the world [1]. Because leptospirosis is a largely neglected disease, a number of unan-swered questions remain about the ecology and evolution of Leptospira, especially those associated with bats. Here we summarize what has been recently learned about this emerging but enigmatic host–pathogen association. We show how this system can provide exciting new opportunities to obtain insights into the evolutionary ecology of bat-borne pathogens and propose future directions to disentangle the role of bats in human leptospirosis. What Do We Know, Briefly, about Leptospirosis and Leptospira