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

Abstract Background The 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 incom...

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Main Authors: Emily L. Kaufman, Nathan E. Stone, Glen A. Scoles, Crystal M. Hepp, Joseph D. Busch, David M. Wagner
Format: Article
Language:English
Published: BMC 2018-05-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-018-2886-5
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spelling doaj-533c30ca2f8545fd8a18314fd59a51282020-11-25T02:09:25ZengBMCParasites & Vectors1756-33052018-05-0111111110.1186/s13071-018-2886-5Range-wide genetic analysis of Dermacentor variabilis and its Francisella-like endosymbionts demonstrates phylogeographic concordance between both taxaEmily L. Kaufman0Nathan E. Stone1Glen A. Scoles2Crystal M. Hepp3Joseph D. Busch4David M. Wagner5Pathogen and Microbiome Institute, Northern Arizona UniversityPathogen and Microbiome Institute, Northern Arizona UniversityUSDA, ARS, Animal Disease Research Unit, 3003 ADBF, Washington State UniversitySchool of Informatics, Computing, and Cyber Systems, Northern Arizona UniversityPathogen and Microbiome Institute, Northern Arizona UniversityPathogen and Microbiome Institute, Northern Arizona UniversityAbstract Background The 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. Methods We 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. Results Maximum 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. Conclusions Our 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.http://link.springer.com/article/10.1186/s13071-018-2886-5Coxiella burnetiiCytochrome c oxidase subunit 1 (cox1)Dermacentor variabilisFrancisella-like endosymbiontsMitochondrial phylogeographyRickettsia spp.
collection DOAJ
language English
format Article
sources DOAJ
author Emily L. Kaufman
Nathan E. Stone
Glen A. Scoles
Crystal M. Hepp
Joseph D. Busch
David M. Wagner
spellingShingle Emily L. Kaufman
Nathan E. Stone
Glen A. Scoles
Crystal M. Hepp
Joseph D. Busch
David M. Wagner
Range-wide genetic analysis of Dermacentor variabilis and its Francisella-like endosymbionts demonstrates phylogeographic concordance between both taxa
Parasites & Vectors
Coxiella burnetii
Cytochrome c oxidase subunit 1 (cox1)
Dermacentor variabilis
Francisella-like endosymbionts
Mitochondrial phylogeography
Rickettsia spp.
author_facet Emily L. Kaufman
Nathan E. Stone
Glen A. Scoles
Crystal M. Hepp
Joseph D. Busch
David M. Wagner
author_sort Emily L. Kaufman
title Range-wide genetic analysis of Dermacentor variabilis and its Francisella-like endosymbionts demonstrates phylogeographic concordance between both taxa
title_short Range-wide genetic analysis of Dermacentor variabilis and its Francisella-like endosymbionts demonstrates phylogeographic concordance between both taxa
title_full Range-wide genetic analysis of Dermacentor variabilis and its Francisella-like endosymbionts demonstrates phylogeographic concordance between both taxa
title_fullStr Range-wide genetic analysis of Dermacentor variabilis and its Francisella-like endosymbionts demonstrates phylogeographic concordance between both taxa
title_full_unstemmed Range-wide genetic analysis of Dermacentor variabilis and its Francisella-like endosymbionts demonstrates phylogeographic concordance between both taxa
title_sort range-wide genetic analysis of dermacentor variabilis and its francisella-like endosymbionts demonstrates phylogeographic concordance between both taxa
publisher BMC
series Parasites & Vectors
issn 1756-3305
publishDate 2018-05-01
description Abstract Background The 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. Methods We 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. Results Maximum 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. Conclusions Our 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.
topic Coxiella burnetii
Cytochrome c oxidase subunit 1 (cox1)
Dermacentor variabilis
Francisella-like endosymbionts
Mitochondrial phylogeography
Rickettsia spp.
url http://link.springer.com/article/10.1186/s13071-018-2886-5
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