The Crimean-Congo haemorrhagic fever tick vector Hyalomma marginatum in the south of France: Modelling its distribution and determination of factors influencing its establishment in a newly invaded area.

We developed a correlative model at high resolution for predicting the distribution of one of the main vectors of Crimean-Congo haemorrhagic fever virus (CCHFV), Hyalomma marginatum, in a recently colonised area, namely southern France. About 931 H. marginatum adult ticks were sampled on horses from 2016 to 2019 and 2021 in 14 southern French departments, which resulted in the first H. marginatum detection map on a large portion of the national territory. Such updated presence/absence data, as well as the mean number of H. marginatum per examined animal (mean parasitic load) as a proxy of tick abundance, were correlated to multiple parameters describing the climate and habitats characterising each collection site, as well as movements of horses as possible factors influencing tick exposure. In southern France, H. marginatum was likely detected in areas characterised by year-long warm temperatures and low precipitation, especially in summer and mostly concentrated in autumn, as well as moderate annual humidity, compared to other sampled areas. It confirms that even in newly invaded areas this tick remains exclusively Mediterranean and cannot expand outside this climatic range. Regarding the environment, a predominance of open natural habitats, such as sclerophyllous vegetated and sparsely vegetated areas, were also identified as a favourable factor, in opposition to urban or peri-urban and humid habitats, such as continuous urban areas and inland marshes, respectively, which were revealed to be unsuitable. Based on this model, we predicted the areas currently suitable for the establishment of the tick H. marginatum in the South of France, with relatively good accuracy using internal (AUC = 0.66) and external validation methods (AUC = 0.76 and 0.83). Concerning tick abundance, some correlative relationships were similar to the occurrence model, as well as the type of horse movements being highlighted as an important factor explaining mean parasitic load. However, the limitations of estimating and modelling H. marginatum abundance in a correlative model are discussed.

Gene flow and adaptive potential in a generalist ectoparasite.

BACKGROUND: In host-parasite systems, relative dispersal rates condition genetic novelty within populations and thus their adaptive potential. Knowledge of host and parasite dispersal rates can therefore help us to understand current interaction patterns in wild populations and why these patterns shift over time and space. For generalist parasites however, estimates of dispersal rates depend on both host range and the considered spatial scale. Here, we assess the relative contribution of these factors by studying the population genetic structure of a common avian ectoparasite, the hen flea Ceratophyllus gallinae, exploiting two hosts that are sympatric in our study population, the great tit Parus major and the collared flycatcher Ficedula albicollis. Previous experimental studies have indicated that the hen flea is both locally maladapted to great tit populations and composed of subpopulations specialized on the two host species, suggesting limited parasite dispersal in space and among hosts, and a potential interaction between these two structuring factors. RESULTS: C. gallinae fleas were sampled from old nests of the two passerine species in three replicate wood patches and were genotyped at microsatellite markers to assess population genetic structure at different scales (among individuals within a nest, among nests and between host species within a patch and among patches). As expected, significant structure was found at all spatial scales and between host species, supporting the hypothesis of limited dispersal in this parasite. Clustering analyses and estimates of relatedness further suggested that inbreeding regularly occurs within nests. Patterns of isolation by distance within wood patches indicated that flea dispersal likely occurs in a stepwise manner among neighboring nests. From these data, we estimated that gene flow in the hen flea is approximately half that previously described for its great tit hosts. CONCLUSION: Our results fall in line with predictions based on observed patterns of adaptation in this host-parasite system, suggesting that parasite dispersal is limited and impacts its adaptive potential with respect to its hosts. More generally, this study sheds light on the complex interaction between parasite gene flow, local adaptation and host specialization within a single host-parasite system.

Strong evidence for the presence of the tick Hyalomma marginatum Koch, 1844 in southern continental France.

Hyalomma ticks can transmit several human and animal pathogens in Eurasia and Africa. Interest in Hyalomma marginatum has increased since the recent (re)emergence of Crimean-Congo Hemorrhagic fever in the Palearctic region. Until now, continental France has been considered free of this tick species. Nevertheless, the existence of incomplete and occasionally incorrect records has maintained confusion about its status. Based on several tick sampling campaigns conducted on horses and birds from 2007 to 2016, we provided very strong evidence for the presence of reproducing populations of H. marginatum in parts of southern continental France. We also confirmed the introduction of immature developmental stages of H. marginatum, as well as H. rufipes, into France probably through trans-Mediterranean bird migrations.

The Recent Evolution of a Maternally-Inherited Endosymbiont of Ticks Led to the Emergence of the Q Fever Pathogen, Coxiella burnetii.

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.