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Downloaded from Genbank and Used A, Horak IG, Et Al Zhou et al. Parasites Vectors (2021) 14:135 https://doi.org/10.1186/s13071-021-04639-z Parasites & Vectors SHORT REPORT Open Access Records of three mammal tick species parasitizing an atypical host, the multi-ocellated racerunner lizard, in arid regions of Xinjiang, China Qi Zhou1†, Jiao Li1†, Xianguang Guo2, Jinlong Liu2, Qi Song2, Xiong Gong2, Han Chen1, Jianhui Zhang1, Jinlei He1, Zhiwan Zheng1, Dali Chen1* and Jianping Chen1,3* Abstract Background: Ticks are ectoparasites that feed on blood of a broad taxonomical range of terrestrial and fying verte- brates and are distributed across a wide range of environmental settings. To date, the species identity, diversity, and relationships among the ticks on lizards in China have been poorly understood. Methods: In this study, 30 ticks, collected from the multi-ocellated racerunner (Eremias multiocellata) lizard in the Tarim Basin and adjacent Yanqi Basin of the Xinjiang Uygur Autonomous Region in China, were identifed by mor- phological observation and confrmed by DNA-based techniques. The mitochondrially encoded 12S rRNA, 16S rRNA, and COI gene fragments of ticks were amplifed and sequenced. To understand the genetic polymorphisms, 47 ticks collected from hedgehogs and 1 from brushwood in the Tarim Basin were also included. Species identifcation was based on both morphological and molecular characters. The median-joining network approach was used to evaluate the intraspecifc genealogies of the ticks and their relatedness with the geographical origin or hosts. Results: The sequence similarity analysis confrmed that the 30 ticks belong to three genera and three species including 11 individuals of Hyalomma asiaticum, 3 of Rhipicephalus turanicus, and 16 of Haemaphysalis sulcata. A network approach revealed paraphyletic populations of R. turanicus and Hy. asiaticum at the intraspecies level regard- ing geographical origin and low host specifcity. For R. turanicus and Hy. asiaticum, common ancestry was observed between COI sequences from lizards and other sequence types from diferent hosts and countries. Conclusions: To our knowledge, our study is the frst to conduct a molecular survey of ticks from lizards in the arid regions of Xinjiang, China. Eremias multiocellata is an atypical host of the three tick species. Notably, two species of ticks, Hy. asiaticum and R. turanicus, have been collected and identifed from lizards in China for the frst time. Star-like networks suggest both of them might have experienced recent population expansion. The discoveries are closely related to the geographical environments in Xinjiang and will provide information for the control of ticks and tick- borne pathogens in Northwest China. Keywords: Tick, Lizard, Xinjiang, Hyalomma asiaticum, Rhipicephalus turanicus, Haemaphysalis sulcata, Eremias multiocellata *Correspondence: [email protected]; [email protected] †Qi Zhou and Jiao Li contributed equally to this work 1 Department of Pathogenic Biology, School of Basic Medical Sciences and Forensic Medicine, Sichuan University, Chengdu, West China, China Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://crea- tivecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdo- main/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Zhou et al. Parasites Vectors (2021) 14:135 Page 2 of 12 Background to species accurately [17]. Molecular taxonomy is an Ticks are obligate hematophagous ectoparasites of verte- alternative method [18]. Molecular analyses based on brate animals, including amphibians, reptiles, birds, and DNA sequences could reveal species groups and assign mammals [1, 2]. Ticks can be found in areas around the unknown individuals to species. Te PCR amplifca- world, ranging from the Arctic to tropical regions, and tion of molecular markers has been developed and has are considered signifcant vectors of diseases in humans, become an essential method in the species identifca- livestock, and wildlife [2]. Extant ticks comprise three tion of ticks [19–21]. Several genetic markers, such as families: Argasidae, Ixodidae, and Nuttalliellidae [3]. In the mitochondrial 12S ribosomal RNA gene (12S rRNA) China, ticks have high species diversity (~ 125 species) [22, 23], 16S ribosomal RNA gene (16S rRNA) [24, 25], and have been classifed into two families: Argasidae and cytochrome c oxidase subunit 1 (COI) [23, 26], and the Ixodidae [4, 5]. second internal transcribed spacer (ITS2) [27, 28], have Te Xinjiang Uygur Autonomous Region, located in been widely used for systematic studies on ticks. the northwest of China, covers more than one sixth of In the present study, we amplifed mitochondrial the country’s territory. Large areas of mountains, deserts, 12S rRNA, 16S rRNA, and COI genes to identify ticks and other additional characteristics constitute the par- isolated from desert lizards in Northwest China. Te ticular landscape of Xinjiang [6]. Additionally, this region obtained sequences were used for alignment in conjunc- is mainly occupied with animal husbandry. Both the tion with some tick sequences retrieved from GenBank. landscape and livestock population contribute to the sur- Our work is a frst attempt to investigate ticks infesting vival of ticks. More than 40 tick species have been con- lizards in the arid desert regions of Xinjiang, China, by frmed to be distributed in Xinjiang, constituting about both morphological examination and DNA sequencing. one third of the species found in China, and most of the We further conducted a preliminary survey of sequence parasitifers are livestock [7]. diversity at the intraspecies level to examine geographical Generally, wild animals serve as a huge and often and/or host specifcity. unknown reservoir of hosts for zoonotic disease, includ- ing tick-borne infections [8]. Many wild animals, such Methods as wild boars, hedgehogs, lizards, and snakes, have been Study area and sampling procedures identifed as tick hosts [5, 9]. However, studies on lizard- Tirty ticks were collected with tweezers from the body tick associations are rare, especially in China. To date, surfaces of lizards, which were identifed as the multi- only fve tick species have been reported from lizards in ocellated racerunner, Eremias multiocellata, via mor- China: Amblyomma javanense, Amblyomma varanense, phological determination following the commonly used Amblyomma crassipes, Ixodes nipponensis, and Haena- classifcation system of lizards in China [29]. Te lizards physalis sulcata [5, 10]. Among them, only the immature were hand-captured alive at three sites in the arid desert stage (larva or nymph) of H. sulcata has been recorded regions of the Xinjiang Uygur Autonomous Region of on desert lizards in Xinjiang [11]. Meanwhile, lizards China (Fig. 1; Table 1). Tese sites are characteristic of serve as a suitable host for many tick species [9, 10] and arid deserts in the Tarim Basin and adjacent Yanqi Basin. commonly share their habitats with domestic animals In addition, 1 tick from brushwood (P4) and 47 ticks from and human beings. A recent increase in human and ani- 1 hedgehog (Hemiechinus auritus) (P5) were collected mal infections from tick bites has been partly caused by and used as reference samples, as shown in Additional a change in the hosts of ticks. Because two or three hosts fle 1: Table S1. Tese ticks were collected and preserved are involved in the life history of many tick species, tick- separately in 2-ml sample tubes containing 2 ml 95% eth- associated agents, including bacteria, viruses, protozoa, anol for later identifcation and DNA extraction. All 77 and helminths, carried by lizards might infect domestic ticks were tentatively identifed morphologically using animals and eventually result in human infection [12, microscopic examination and stored at the Chengdu 13]. Diferent tick species are suited to carrying diferent Institute of Biology, Chinese Academy of Sciences. Te pathogens. Tus, it is imperative to identify tick species protocol was approved by the medical ethics committee rapidly and accurately. of Sichuan University (no. K2018056) and carried out Traditionally, ticks are identifed using morphological under the National Guidelines for Experimental Animal methods and criteria [14]. However, these methods are Welfare (MOST of the People’s Republic of China, 2006). insufcient for the identifcation of damaged, engorged, or immature specimens because of the loss or lack of DNA extraction, amplifcation, cloning, and sequencing morphological characteristics [15, 16]. Because of these protocols limitations, only a limited number of experts such as Te ticks were washed
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