Population genetic structure and demographic history of Dermacentor marginatus Sulzer, 1776 in Anatolia

Abstract

Dermacentor marginatus is a medically important tick species due to its preference humans and domestic animals as hosts and its vectorial competence, yet it remains understudied in many regions. This study aimed to examine the population structure and demographic history of D. marginatus using the cox1 and ITS2 genes, focusing on populations from Central and Northeast Anatolia-two regions on either side of the Anatolian Diagonal, a natural biogeographical barrier. A total of 361 host-seeking adult D. marginatus ticks from 31 sampling sites were analyzed, revealing 131 haplotypes for cox1 and 104 genotypes for ITS2. Neutrality tests and mismatch distribution patterns rejected the null hypothesis of the neutral theory, indicating that the population of D. marginatus in Anatolia has undergone a recent demographic expansion. Significant genetic differentiation and population structuring were observed between the Central and Northeastern Anatolian populations of D. marginatus, correlating with geographic distance and suggesting that the Anatolian Diagonal acts as a potential barrier to gene flow. Intrapopulation gene flow was higher in Central Anatolian populations compared to Northeastern Anatolian populations. Bayesian phylogeny revealed a highly divergent D. marginatus haplotype within the Northeastern Anatolian population, clustering into a Central Asian clade. Additionally, phylogenetic trees of the subgenus Serdjukovia revealed taxonomic ambiguities, including the absence of a distinct clade for D. niveus and potential misidentifications of D. marginatus and D. raskemensis specimens. Furthermore, the monophyletic relationship between D. marginatus and D. raskemensis supports the likelihood of sympatric speciation. These findings enhance our understanding of the genetic structure, phylogeography, and evolutionary dynamics of D. marginatus while providing a framework for future research on tick populations.

Keywords: Dermacentor marginatus complex; Serdjukovia; cox1; ITS2; Phylogeography; Tick evolution.

Fig. 1

Maps showing the study areas and locations where Dermacentor marginatus specimens were collected. Sampling sites determined in this study are indicated on both elevation and vegetation-based maps. The position of the Anatolian Diagonal on the map is drawn based on Kuzguncuoğlu et al. (2019). Maps were generated using ArcGIS 10.6.1 software, and the final figure composition was created using Inkscape 1.2.

Fig. 2

Population structure of Dermacentor marginatus in Anatolia. (A) Ancestry of individual ticks (361 Anatolian D. marginatus individuals from 150 sites) assuming K cluster of genetic similarity, based on the results of STRUCTURE analyses using cox1 gene (K = 3). The first 19 sampling sites (L1-LM) contain samples from the CE population and the remaining locations groups (L16-27) contain samples from the NE population. Each bar corresponds to a tick specimen, vertical dashed yellow lines indicate the boundaries between sampling sites, and the vertical axis represents the membership probability of an individual to each cluster. (B) Maps showing genetic clusters of D. marginatus individuals (n = 361) according to 31 sampling sites, based on the results of SAMOVA using cox1 gene. The value K refers to the number of simulated groups. Satellite images were processed using SAMOVA 2.0 software.

Fig. 3

Haplotype distribution, network and pairwise distances of Dermacentor marginatus (n = 361) based on cox1 gene. (A) Distribution map of haplotypes according to sampling sites. The CN haplotypes are colored in shades of red, the NE haplotypes in shades of blue and shared haplotypes in shades of yellow. (B) TCS network tree of haplotypes. Individuals from CN are colored in red, while individuals from the NE in blue. The names of major haplotypes with multiple samples are indicated on the tree. (C) Color coded matrix of pairwise similarity scores belonging to haplotypes. Maps were generated using ArcGIS 10.6.1 software.

Fig. 4

Phylogenetic tree based on Bayesian inference under the TN93(TrN) + Γ + I model using cox1 data from 201 Dermacentor marginatus (131 haplotypes characterized in this study + 71 GenBank records), 53 D. nuttalli, 15 D. silvarum, eight D. niveus and one D. raskemensis sequence. D. reticulatus sequences (MT478096, OM142141 and OQ947121) were used as outgroup. The node labels refer to the posterior probability and are omitted below the value 0.5. The haplotype characterized in this study is indicated in red and the determined main clades are indicated on the roots.