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Phylogenetic Analysis of the Australasian Paralysis Ticks and Their Relatives (Ixodidae: Ixodes: Sternalixodes) Mackenzie L

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Phylogenetic Analysis of the Australasian Paralysis Ticks and Their Relatives (Ixodidae: Ixodes: Sternalixodes) Mackenzie L Kwak et al. Parasites & Vectors (2017) 10:122 DOI 10.1186/s13071-017-2045-4 RESEARCH Open Access Phylogenetic analysis of the Australasian paralysis ticks and their relatives (Ixodidae: Ixodes: Sternalixodes) Mackenzie L. Kwak1, Ian Beveridge1, Anson V. Koehler1, Mallik Malipatil2,3, Robin B. Gasser1 and Abdul Jabbar1* Abstract Background: The Australasian paralysis ticks and their relatives, Ixodes Latrielle, subgenus Sternalixodes Schulze, are some of the most important ticks in the region. However, very little is known about their phylogenetic relationships. The aim of this study was to elucidate the evolutionary relationships of members of the subgenus Sternalixodes by undertaking phylogenetic analyses of morphological and molecular datasets. Methods: Adult females (n =64)ofSternalixodes, including Ixodes anatis Chilton, 1904, Ixodes confusus Roberts, 1960, Ixodes cornuatus Roberts, 1960, Ixodes cordifer Neumann, 1908, Ixodes dendrolagi Wilson, 1967, Ixodes hirsti Hassall, 1931, Ixodes holocyclus Neumann, 1899, Ixodes myrmecobii Roberts, 1962 and Ixodes trichosuri Roberts, 1960, were examined morphologically. Subsequently, these Ixodes spp. were genetically characterised using cytochrome c oxidase subunit 1 (cox1) gene and the internal transcribed spacer 2 (ITS-2) of the rRNA. Both morphological and molecular datasets were analysed using various phylogenetic methods to assess the evolutionary relationship of various members of the subgenus Sternalixodes. Results: Phylogenetic analyses of the cox1 sequences and morphological characters datasets revealed that the Australian and Papuan Sternalixodes formed a distinct clade with the New Zealand member of the group I. anatis positioned basally, in a separate clade. Ixodes holocyclus, I. cornuatus and I. myrmecobii formed a distinctive clade in both the cox1and morphological phylogenies. However, based on phylogenetic analysis of the ITS-2 data, I. holocyclus formed a separate clade whereas I. cornuatus and I. myrmecobii grouped in a different clade. Conclusions: The cox1 and morphological data suggest that the subgenus Sternalixodes is paraphyletic, and I. anatis is not a sternalixodid tick; hence, it should not be included in the subgenus. Based on the phylogenetic analyses of cox1 and ITS-2 sequences, it appears that I. myrmecobii and I. cornuatus are not subspecies of I. holocyclus. Although this study provided better insights into the taxonomic status of the subgenus Sternalixodes, a complete morphological and molecular (using multiple markers) phylogenetic analysis including all members of the subgenus would be required to more accurately elucidate the evolutionary relationships within the subgenus. Keywords: Ixodes, Sternalixodes, Phylogeny, Molecular, Morphological, Tick * Correspondence: [email protected] 1Department of Veterinary Biosciences, Melbourne Veterinary School, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Werribee, Victoria 3030, Australia Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kwak et al. Parasites & Vectors (2017) 10:122 Page 2 of 12 Background cordifer, I. dendrolagi, I. hirsti, I. holocyclus, I. myrmeco- Ticks (Arachnida: Ixodidae) are important ectoparasites bii and I. trichosuri [11]. However, the majority of stud- of humans and animals and can cause direct (e.g., ies have focussed on I. holocyclus and I. cornuatus,a paralysis, anaemia) as well as indirect (e.g., transmission species morphologically similar to I. holocyclus,aimingto of pathogens) effects on their hosts [1–3]. Ticks can be determine their distribution [1, 12], morphological and mo- found on all continents and are known to feed on all lecular identification [1, 13] and phylogenetic relationships types of terrestrial vertebrates, including mammals, [14]. A number of questions therefore remain to be an- birds, reptiles and amphibians [1, 3]. The life-cycle of swered regarding the members of the subgenus Sternalix- ixodid ticks consists of four developmental stages, the odes.Forinstance,thestatusofI. myrmecobii as subspecies egg, and three active parasitic stages, larva, nymph, and of I. holocyclus as proposed by Roberts [1] needs to be adult (male and female). Depending on the type (hard, tested. To date, Australian paralysis ticks and their relatives Ixodidae or soft, Argasidae) and species of ticks, their have not been analysed using morphological as well as mo- life-cycle can vary significantly. lecular phylogenetics. Being an important subgenus, Sterna- To date, 70 species (56 and 14 members of families lixodes requires systematic investigations to address a Ixodidae and Argasidae, respectively) of ticks have been number of taxonomic questions regarding the validity of its recorded from a variety of hosts (humans and domestic members. Therefore, this study was designed to elucidate animals = 16; mammals, reptiles and birds = 54) from the evolutionary relationships of members of the subgenus Australia [4]. Among different genera of hard ticks Sternalixodes by undertaking phylogenetic analyses of mor- prevalent in Australia, Ixodes is arguably the most phological and molecular datasets. important and its members are known to transmit and/ or harbour pathogens, including Rickettsia australis (the Methods causative agent of Queensland tick typhus) in humans Tick collection and morphological identification [5], and flaviviruses, bunyaviruses and Cercopithifilaria Female ticks (n = 74) used in this study were either avail- johnstoni Mackerras (Nematoda: Filarioidea) in wildlife able from The University of Melbourne (Ian Beveridge [6–8]. Some Ixodes species such as I. holocyclus and I. and Abdul Jabbar) or museums in Australia (South cornuatus can also cause paralysis in humans, domestic Australian Museum, Western Australian Museum, and animals, and wildlife [9]. Ixodes holocyclus is known to Australian National Insect Collection), New Zealand (A. have an immunoeffectory action on humans, causing Heath, AgResearch, New Zealand), Papua New Guinea tick bite anaphylaxis [10]. (Ifor L. Owen, National Veterinary Laboratory, Papua Members of the genus Ixodes have not been inten- New Guinea) and South America (A. Guglielmone, sively examined (e.g., phylogeny using combined mor- Instituto Nacional de Technologia Agropecuaria, phological and molecular datasets, biology, life-cycle) Argentina) (Fig. 1; Table 1). Following collection, each tick within Australia. Few life-cycles have been elucidated specimen was stored in 70% ethanol until used. Develop- and the bionomics of very few species are understood. mental stages of all species of Sternalixodes could not be Of the subgenera of Ixodes, Sternalixodes has received examined as many are not yet described. most attention. The subgenus comprises nine members, For morphological identification, each tick was exam- including Ixodes anatis, I. confusus, I. cornuatus, I. ined using a dissecting microscope (Olympus, Japan). In Fig. 1 Collection sites for Ixodes species from Argentina, Australia, New Zealand and Uruguay, used in this study. Information linked to each unique number on the map is provided in Table 1 Kwak et al. Parasites & Vectors (2017) 10:122 Page 3 of 12 Table 1 Specimens of Ixodes spp. used in molecular studies, and their sources and collection sites Species Specimen voucher Locality Hosts/collection method Source Map code I. auritulus S63 Buenos Aires, Argentina Collected via flagging A. Guglielmone 1 S64 Rocha, Uruguay Collected via flagging A. Guglielmone 2 I. anatis S28 Auckland Zoo, New Zealand Apteryx mantelli A. Heath 3 S29 Ponui Island, New Zealand Apteryx mantelli A. Heath 4 I. holocyclus S1 Kioloa, NSW, Australia Collected via flagging This study 5 S4 Kioloa, NSW, Australia Collected via flagging This study 6 S37 Waygara, Vic, Australia Canis lupus familiaris This study 7 S17 Wandecla NP, QLD, Australia Canis lupus familiaris This study 8 S39 Atherton, QLD, Australia Canis lupus familiaris This study 9 I. myrmecobii S26 Cape Le Grand NP, WA, Australia Unknown WAM 10 S46 Munglinup, WA, Australia Homo sapiens WAM 11 S56 Quaalup Station, WA, Australia Unknown WAM 12 S44 Cranbrook, WA, Australia Homo sapiens WAM 13 S25 Stirling Ranges NP, WA, Australia Unknown WAM 14 S42 Stirling Ranges NP, WA, Australia Unknown WAM 15 I. cornuatus S19 Mt William NP, Tas, Australia Vombatus ursinus ANIC 16 S20 Acton Park, Tas, Australia Unknown This study 17 S18 Bullengarook, Vic, Australia Canis lupus familiaris ANIC 18 S41 Kinglake, Vic, Australia Canis lupus familiaris This study 19 I. dendrolagi S14 Gondom, Papua New Guinea Dendrolagus matschiei This study 20 I. trichosuri S23 Bellbird Creek, Vic, Australia Trichosurus caninus ANIC 21 S21 Nowa Nowa, Vic, Australia Unknown ANIC 22 I. hirsti S10 Anglesea, Vic, Australia Macropus giganteus This study 23 S12 Mansfield, Vic, Australia Felis catus ANIC 24 S9 Anglesea, Vic, Australia Macropus giganteus This study 25 I. tasmani S68
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