Complete mitochondrial genomes reveal the intraspecific variation and phylogeography of the Caucasian soft tick relapsing fever vector; Ornithodoros (pavlovskyella) verrucosus (Ixodida: Argasidae)

Authors: FILATOV, SERHII - Baylor College Of Medicine; KNEUBEHL, ALEXANDER - Baylor College Of Medicine; KRISHNAVAJHALA, APARNA - Baylor College Of Medicine; MELASHVILI, GIORGI - Baylor College Of Medicine; TSITSISHVILI, ANA - Baylor College Of Medicine; MAMEDOVA, KUSVER - Baylor College Of Medicine; Saelao, Perot; Perez De Leon, Adalberto - Beto; LOPEZ, JOB - Baylor College Of Medicine

Submitted to: Infection, Genetics and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/24/2024
Publication Date: 9/26/2024
Citation: Filatov, S., Kneubehl, A.R., Krishnavajhala, A., Melashvili, G., Tsitsishvili, A., Mamedova, K., Saelao, P., Perez De Leon, A.A., Lopez, J.E. 2024. Complete mitochondrial genomes reveal the intraspecific variation and phylogeography of the Caucasian soft tick relapsing fever vector; Ornithodoros (pavlovskyella) verrucosus (Ixodida: Argasidae). Infection, Genetics and Evolution. https://doi.org/10.1016/j.meegid.2024.105673.
DOI: https://doi.org/10.1016/j.meegid.2024.105673

Interpretive Summary: The causitive agent for tick-boerne relapsing fever is transmitted exclusively by the tick, Ornithodoros verrucosus. This artical attempts to track the distribution and genetic diversity of the tick and its tick-boerne spirochete through regions of Eastern Europe and the Caucasus. Using the mitogenome of 54 individual ticks from Ukraine, Georgie, and Azerbaijan we detected unique genetic signatures specific to distinct populations. Our analysis finds that each population maintains strong genetic isolation demonstrating very little distribution of the tick suggesting populations remain largely isolated. Overall, we do identify some genetic admixture between populations but more information will be needed to better understand how these species navigate spatial variation and colonization of novel ecological spaces.

Technical Abstract: Territories in southern parts of Eastern Europe and in the Caucasus are endemic for tick-borne relapsing fever (TBRF), caused by Borrelia caucasica. This spirochete is transmitted exclusively by the bites of Ornithodoros verrucosus; however, the distribution and genetic diversity of the tick vector have not been explored. To address this, we performed a phylogeographic study of O. verrucosus specimens collected across a large geographic distribution. We sequenced and analyzed complete mitochondrial genomes of 54 individual O. verrucosus ticks representing 23 geographically diverse populations from Ukraine, Georgia, and Azerbaijan. We detected 47 unique haplotypes, with every collection site exhibiting distinct polymorphisms. This, along with other population genetic indices, suggests little evidence of gene flow between populations. The Bayesian coalescent analysis revealed the presence of four lineages that diverged in the Middle Pleistocene (770-126 kya). Two lineages were widespread and present in all study regions, the other two were restricted to the southern foothills of the Lesser Caucasus mountain range. The sympatry of these ancient lineages suggests that isolation by environment, in addition to geographic distance, may play a role in the intraspecific divergence of tick populations. Using a phylogeographic approach, we provide a snapshot of genetic diversity in O. verrucosus and discuss the evolutionary history of the tick vector.