High Crimean-Congo hemorrhagic fever incidence linked to greater genetic diversity and differentiation in Hyalomma marginatum populations in Türkiye

Background: Ticks are crucial vectors of a wide range of pathogens, posing significant threats to human and animal health globally. Understanding the genetic basis of tick biology and host–parasite interactions is essential for developing effective control programs. This study investigates the fine-scale genetic structure of Hyalomma marginatum Koch, 1844, the primary vector of Crimean-Congo hemorrhagic fever (CCHF) in Türkiye. Despite its significant public health importance, information regarding its population structure and genetic diversity is quite limited. Methods: We used restriction site-associated DNA sequencing (RAD-Seq) to obtain genome-wide sequence data from 10 tick populations in Türkiye, collected from regions with low, moderate, and high incidence rates of CCHF. Based on these data, we determined population structure and diversity of populations using principal component analysis (PCA) and admixture analysis. Furthermore, we calculated pairwise F_ST and utilized discriminant analysis of principal components (DAPC) to understand genetic differentiation between populations. Results: PCA and admixture analysis indicated minimal genetic structure between populations, but we detected notable genetic differentiation and high genetic diversity from regions with high CCHF rates. Furthermore, our DAPC identified 31 significant single-nucleotide polymorphisms (SNPs) associated with regions with high CCHF incidence, with 25 SNPs located near genes involved in critical biological functions such as nucleic acid binding, transmembrane transport, and proteolysis. These findings suggest that genetic variations in these regions may confer adaptive advantages in environments with high pathogen loads. Conclusions: This study provides the first comprehensive analysis of H. marginatum genetic diversity in Türkiye, revealing significant differentiation in populations from CCHF-endemic regions. These results underscore the importance of considering fine-scale genetic diversity to fully understand the drivers of genetic variation in ticks and their implications for vectorial capacity. Graphical Abstract: (Figure presented.)