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Contributions to the phylogeny of Ixodes ( Pholeoixodes) canisuga, I. ( Ph.) kaiseri, I. ( Ph.) hexagonus and a simple pictorial key for the identification of their females

ORCID
0000-0001-5449-8615
Affiliation
Department of Parasitology and Zoology, University of Veterinary Medicine, Budapest, Hungary. hornok.sandor@univet.hu.
Hornok, Sándor;
Affiliation
Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, Romania.
Sándor, Attila D;
Affiliation
Department for Bacteriology and Parasitology, Croatian Veterinary Institute, Zagreb, Croatia.
Beck, Relja;
Affiliation
Department of Parasitology and Zoology, University of Veterinary Medicine, Budapest, Hungary.
Farkas, Róbert;
Affiliation
U.S. National Tick Collection, Institute for Coastal Plain Science, Georgia Southern University, Statesboro, GA, USA.
Beati, Lorenza;
Affiliation
Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest, Hungary.
Kontschán, Jenő;
Affiliation
Department of Parasitology and Zoology, University of Veterinary Medicine, Budapest, Hungary.
Takács, Nóra;
Affiliation
Department of Parasitology and Zoology, University of Veterinary Medicine, Budapest, Hungary.
Földvári, Gábor;
GND
137068093
Affiliation
National Centre for Vector Entomology, Institute of Parasitology, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland.
Silaghi, Cornelia Hildegard Anita;
Affiliation
State Office for Consumer Protection (TLV), Bad Langensalza, Germany.
Meyer-Kayser, Elisabeth;
Affiliation
Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Vienna, Austria.
Hodžić, Adnan;
Affiliation
Department for Medical Entomology, Institute for Medical Research, University of Belgrade, Belgrade, Serbia.
Tomanović, Snežana;
Affiliation
Veterinary Parasitology and Ecology Group, School of Biological Sciences, Life Sciences Building, University of Bristol, Bristol, UK.
Abdullah, Swaid;
Affiliation
Veterinary Parasitology and Ecology Group, School of Biological Sciences, Life Sciences Building, University of Bristol, Bristol, UK.
Wall, Richard;
Affiliation
Department of Animal Health, Faculty of Veterinary Medicine, Zaragoza, Spain.
Estrada-Peña, Agustín;
Affiliation
Department of Pathobiology, Institute of Parasitology, University of Veterinary Medicine Vienna, Vienna, Austria.
Duscher, Georg Gerhard;
Affiliation
BIOEPAR, INRA, Oniris, Nantes, France.
Plantard, Olivier

In Europe, hard ticks of the subgenus Pholeoixodes (Ixodidae: Ixodes) are usually associated with burrow-dwelling mammals and terrestrial birds. Reports of Pholeoixodes spp. from carnivores are frequently contradictory, and their identification is not based on key diagnostic characters. Therefore, the aims of the present study were to identify ticks collected from dogs, foxes and badgers in several European countries, and to reassess their systematic status with molecular analyses using two mitochondrial markers.Between 2003 and 2017, 144 Pholeoixodes spp. ticks were collected in nine European countries. From accurate descriptions and comparison with type-materials, a simple illustrated identification key was compiled for adult females, by focusing on the shape of the anterior surface of basis capituli. Based on this key, 71 female ticks were identified as I. canisuga, 21 as I. kaiseri and 21 as I. hexagonus. DNA was extracted from these 113 female ticks, and from further 31 specimens. Fragments of two mitochondrial genes, cox1 (cytochrome c oxidase subunit 1) and 16S rRNA, were amplified and sequenced. Ixodes kaiseri had nine unique cox1 haplotypes, which showed 99.2-100% sequence identity, whereas I. canisuga and I. hexagonus had eleven and five cox1 haplotypes, respectively, with 99.5-100% sequence identity. The distribution of cox1 haplotypes reflected a geographical pattern. Pholeoixodes spp. ticks had fewer 16S rRNA haplotypes, with a lower degree of intraspecific divergence (99.5-100% sequence identity) and no geographical clustering. Phylogenetic analyses were in agreement with morphology: I. kaiseri and I. hexagonus (with the similar shape of the anterior surface of basis capituli) were genetically more closely related to each other than to I. canisuga. Phylogenetic analyses also showed that the subgenus Eschatocephalus (bat ticks) clustered within the subgenus Pholeoixodes.A simple, illustrated identification key is provided for female Pholeoixodes ticks of carnivores (including I. hexagonus and I. rugicollis) to prevent future misidentification of these species. It is also shown that I. kaiseri is more widespread in Europe than previously thought. Phylogenetic analyses suggest that the subgenus Pholeoixodes is not monophyletic: either the subgenus Eschatocephalus should be included in Pholeoixodes, or the latter subgenus should be divided, which is a task for future studies.

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