Phylogeographic investigation of tick-borne pathogens in host-seeking Dermacentor marginatus in Anatolia: Significant correlation between population genetic structure and SFG rickettsiae

Abstract

Characterizing the population structure of vector ticks and their associated microorganisms in natural foci is essential for understanding of the ecology of tick-borne disease (TBD) and developing effective control strategies. Dermacentor marginatus is an important vector species in the Palearctic realm, yet its vectorial role remains poorly defined, particularly due to the lack of studies integrating population genetics with pathogen data. In this study, we performed a phylogeographic analysis of tick-borne pathogens (TBPs) in host-seeking D. marginatus from natural foci across Anatolia, integrating these data with the population genetic information from the same specimens. A total of 696 ticks from 151 locations were screened. PCR and sequencing revealed that 58.8 % (409/696) of ticks carried at least one causative agent, including spotted fever group (SFG) rickettsiae (Rickettsia slovaca and R. raoultii), Coxiella burnetii, Francisella tularensis subsp. holarctica, Francisella-like endosymbionts, Babesia spp. (B. occultans, B. vulpes, and B. bigemina), Theileria ovis, and Hepatozoon spp. (H. canis and two unidentified species). Our findings revealed distinct phylogeographic patterns of SFG rickettsiae between Central and Northeastern populations, providing the first evidence of a population-level evolutionary association between D. marginatus and R. slovaca/raoultii. Previously unrecognized natural foci of C. burnetii and F. tularensis subsp. holarctica associated with D. marginatus were also identified. Several novel tick-pathogen associations were documented. These results indicate a high prevalence of human-pathogenic agents in D. marginatus populations in Anatolia suggest that population genetic structure may influence silent tick-pathogen interactions. By integrating population genetics with pathogen screening, this study offers new insights into the ecology and evolutionary dynamics of D. marginatus and associated TBPs.