Range-wide genetic analysis of Dermacentor variabilis and its Francisella-like endosymbionts demonstrates phylogeographic concordance between both taxa

Abstract

BackgroundThe American dog tick, Dermacentor variabilis, is an important vector of pathogens to humans, wildlife and domestic animals in North America. Although this tick species is widely distributed in the USA and Canada, knowledge of its range-wide phylogeographic patterns remains incomplete.MethodsWe carried out a phylogenetic analysis of D. variabilis using samples collected from 26 USA states and five Canadian provinces. Tick samples (n = 1053 in total) originated from two main sources: existing archives (2000–2011), and new collections made from 2012 to 2013. We sequenced a 691 bp fragment of the cox1 gene from a subset (n = 332) of geographically diverse D. variabilis. DNA extracted from individual ticks (n = 1053) was also screened for a Francisella-like endosymbiont, using a targeted 16S rRNA sequencing approach, and important pathogens (Rickettsia spp. and Coxiella burnetii), using species-specific quantitative PCR assays.ResultsMaximum parsimony analysis of cox1 sequences revealed two major groups within D. variabilis with distinct geographical distributions: one from the eastern USA/Canada (Group 1) and one from the west coast states of the USA (California and Washington; Group 2). However, genetic subdivisions within both of these two major groups were weak to moderate and not tightly correlated with geography. We found molecular signatures consistent with Francisella-like endosymbionts in 257 of the DNA extracts from the 1053 individual ticks, as well as Rickettsia spp. and Coxiella burnetii in a small number of ticks (n = 29 and 2, respectively). Phylogenetic patterns for Francisella-like endosymbionts, constructed using sequence data from the bacterial 16S rRNA locus, were similar to those for D. variabilis, with two major groups that had a nearly perfect one-to-one correlation with the two major groups within D. variabilis.ConclusionsOur findings reveal a distinct phylogenetic split between the two major D. variabilis populations. However, high levels of genetic mixture among widely separated geographical localities occur within each of these two major groups. Furthermore, our phylogenetic analyses provide evidence of long-term tick-symbiont co-evolution. This work has implications for understanding the dispersal and evolutionary ecology of D. variabilis and associated vector-borne diseases.Electronic supplementary materialThe online version of this article (10.1186/s13071-018-2886-5) contains supplementary material, which is available to authorized users.

Genomic evidence for host‐associated differentiation in an animal parasite, Dermacentor variabilis, the American dog tick

“…A previous study also identified SNPs in D. variabilis using ddRADseq (Lado et al., 2019). Their study agreed with the existence of two geographic clades of D. variabilis identified using 16S rRNA (Krakowetz et al., 2010) and CO1 (Kaufman et al., 2018), but allowed for additional resolution to identify genetic structuring within the eastern clade forming a ‘northern’ group and an ‘east of the Rockies’ group. Our results provide further resolution to identify genetic structuring according to host in the eastern clade within the state of Texas.…”

“…Population genetic studies of D. variabilis in the USA have focused on characterizing the genetic structure at a wide geographic scale using various molecular markers including 16s rRNA, mitochondrial COI (Kaufman et al., 2018), microsatellites (Dharmarajan et al., 2009), AFLPs (Araya‐Anchetta et al., 2013), and SNPs (Lado et al., 2019). These studies showed that there are two main populations of this tick in the continental USA originally identified using 16S rRNA with a western population being geographically isolated from the eastern population differing by 14 mutational steps (nucleotide differences) (Krakowetz et al., 2010).…”

Comparative mitogenomics elucidates the population genetic structure of Amblyomma testudinarium in Japan and a closely related Amblyomma species in Myanmar

“…of Myanmar. In fact, the evolution of mitochondrial genes can be affected by several ecological factors such as endosymbionts and animal host diversity (Kaufman et al, 2018 ; Sassera et al, 2006 ). The difference in diversity between A. testudinarium in Japan and Amblyomma sp.…”

Mechanisms Affecting the Acquisition, Persistence and Transmission of Francisella tularensis in Ticks

“…However, those authors noted that their sequencing methods may not have been optimal for detecting low abundance organisms [ 108 ]. A more comprehensive study examined D. variabilis tick microbiomes from 26 U.S. states and five Canadian provinces, finding FLEs in only 24% of those ticks [ 109 ]. However, those authors also noted that a low abundance of endosymbiont DNA may have contributed to false negatives.…”

“…Given that previous studies have demonstrated how differences in microbiomes alter tick competence for pathogen infections [ 99 , 110 ], more comprehensive studies are needed to examine tick microbiomes and understand how those microbiomes influence F. tularensis infections of ticks. Importantly, none of the above studies examined tick microbiomes from the south-central United States, where tularemia is most prevalent [ 28 , 109 ], nor did they examine A. americanum tick microbiomes. Additionally, is it unclear how identified non-pathogenic Francisella sp.…”