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Population Genetic Structure of Gasterophilus Pecorum in the Kalamaili Nature Reserve, Xinjiang, Based on Mitochondrial Cytochrome Oxidase (COI) Gene Sequence

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Population Genetic Structure of Gasterophilus Pecorum in the Kalamaili Nature Reserve, Xinjiang, Based on Mitochondrial Cytochrome Oxidase (COI) Gene Sequence See discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/265177170 Population genetic structure of Gasterophilus pecorum in the Kalamaili Nature Reserve, Xinjiang, based on mitochondrial cytochrome oxidase (COI) gene sequence ARTICLE in MEDICAL AND VETERINARY ENTOMOLOGY · AUGUST 2014 Impact Factor: 2.33 · DOI: 10.1111/mve.12073 · Source: PubMed DOWNLOADS VIEWS 16 50 8 AUTHORS, INCLUDING: wd Wang Dong Zhang VMware Beijing Forestry University 29 PUBLICATIONS 398 CITATIONS 49 PUBLICATIONS 98 CITATIONS SEE PROFILE SEE PROFILE Defu Hu Beijing Forestry University 16 PUBLICATIONS 86 CITATIONS SEE PROFILE Available from: Dong Zhang Retrieved on: 10 September 2015 Medical and Veterinary Entomology (2014) 28 (Suppl. 1), 75–82 Population genetic structure of Gasterophilus pecorum in the Kalamaili Nature Reserve, Xinjiang, based on mitochondrial cytochrome oxidase (COI) gene sequence W.WANG1, D. ZHANG1,D.HU1, H. CHU2,J.CAO3,M.ENTE3, G. JIANG4 and K. L I 1 1Key Laboratory of Non-Invasive Research Technology for Endangered Species, College of Nature Conservation, Beijing Forestry University, Beijing, China, 2Wildlife Conservation Office of Altay Prefecture, Altay, Xinjiang, China, 3Xinjiang Research Centre for Breeding Przewalski’s Horse, Urumqi, Xinjiang, China and 4Huamugou Forest Farm, Keshiketeng Banner, Chifeng, Inner Mongolia, China Abstract. Gasterophilosis is a significant threat to equids in the desert steppe of Xinjiang, China, where Gasterophilus pecorum (Fabricius) (Diptera: Gasterophilidae) is the dominant botfly species. A population analysis was conducted on 195 individual G. pecorum larvae from three host species, Przewalski’s horse, the domestic horse and the Asiatic wild ass. The distribution of haplotypes of the maternally inherited mitochondrial cytochrome oxidase subunit I (COI) gene was analysed to assess the population differentiation of G. pecorum. High haplotype diversity was observed among G. pecorum populations from all host species, indicating that the G. pecorum infecting one host had multiple maternal ancestors. A phylogenetic tree showed six clades, suggesting a high degree of genetic differentiation. A constructed haplotype network described both the origin of the haplotypes and the population structure. The findings indicated that G. pecorum infections within Przewalski’s horses were mainly transmitted from Asiatic wild asses. Clade 1 was found to be the most primitive group and to have evolved to be highly adaptable to the desert steppe. Clade 2 originated from Clade 1, potentially as a result of the annual migration of domestic horses. Revealing the differentiation of the G. pecorum population is important for elucidating the aetiology of Gasterophilus infection in Xinjiang and for planning appropriate control measures. Key words. Gasterophilus pecorum, COI, equids, population genetic structure.. Introduction Gasterophilus haemorrhoidalis (Linnaeus) and Gasterophilus inermis (Brauer), have been reported in equids from China The larvae of Gasterophilus species are parasites that (Li et al., 2007). populate the gastrointestinal tracts of equids and occa- Inseminated female G. pecorum lay eggs on grass and in the sionally affect pigs, dogs, birds and humans (Zumpt, 1965; foliage of plants, whereas other species of botfly lay eggs on Soulsby, 1982). Of the nine species known within the genus the hair, forelegs, lips, face and intermandibular area of animals (Zumpt, 1965), six, including Gasterophilus pecorum (Fabri- (Sánchez-Andrade et al., 2010). First-stage larvae are introduced cius), Gasterophilus intestinalis (De Geer), Gasterophilus into the oral cavity during host feeding. After moulting, second nasalis (Linnaeus), Gasterophilus nigricornis (Loew), instars migrate to specific areas of the digestive system (e.g. Correspondence: Kai Li, Key Laboratory of Non-Invasive Research Technology for Endangered Species, College of Nature Conservation, Beijing Forestry University, Beijing 100083, China. Tel.: + 86 10 6233 8130; Fax: + 86 10 6233 6013; E-mail: [email protected] © 2014 The Royal Entomological Society 75 76 W. Wang et al. stomach and intestine) where they moult into third instars, which suitable molecular tool for examining intraspecific and inter- can remain attached for 8–10 months (Coles & Pearson, 2000). specific variations in genetic structure, and in phylogenetic The larvae of Gasterophilus can cause gastrointestinal myiasis studies of insects (Lunt et al., 1996). Indeed, the molecular in equids, which manifests as dysphagia, gastric and intestinal identification and intraspecific differentiation of 18 species of ulceration, or gastric obstruction or volvulus, and can further the myiasis-inducing Oestridae (Diptera) were studied using induce anaemia, diarrhoea, gastric rupture, peritonitis, perfo- the most variable portion of the COI gene (Otranto et al., 2003). rating ulcers and other complications (Soulsby, 1982; Sequeira The COI gene was also used in the identification and phyloge- et al., 2001). netic analysis of five Gasterophilus species, and the reliability Gasterophilosis epidemics in the desert steppe of Xinjiang, of these results was confirmed by a high degree of correla- China, have been reported to be quite severe and to have tion with the results of morphological identification (Otranto caused health problems in Przewalski’s horse [Equus przewal- et al., 2005b). The utilization of the COI gene in the genetic skii (Perissodactyla: Equidae)] (Li et al., 2007). Przewalski’s identification of Polish and Italian specimens of G. nasalis horses [listed as endangered by the International Union for Con- and G. intestinalis further demonstrated that the COI gene is servation of Nature (IUCN) in 2011] were once widely dis- an informative tool for the genetic identification of species tributed in the Eurasian desert steppe; however, they became from different geographical areas (Pawlas-Opiela et al., 2010). extinct in the middle of the last century (Mohr, 1972). To The most variable part of the COI gene, encoding the amino re-populate this species, Przewalski’s horses were released in acid region spanning the external loop (E4) to the carboxy August 2001 into the Kalamaili Nature Reserve (KNR) in Xin- terminus (−COOH), has proved suitable as an evolutionary jiang, located in northwest China, since when their population marker for lower-level evolutionary analyses, such as in studies has increased significantly. Although deworming is performed of intraspecific variation, as well as for phylogenetic studies annually during the winter in these Przewalski’s horses, recur- of closely related species and population genetic studies, and ring Gasterophilus infections remain prevalent and the parasitic has been applied in various invertebrate taxa (Lunt et al., 1996; burden is severe at an infection of 100% (Liu, 2012). It is pos- Zhang & Hewitt, 1997; Prabhakar et al., 2012). tulated that the Gasterophilus infection in these horses may be The present study exploited this region of the mtDNA to closely related to that in sympatric equids. Previous data gath- investigate the maternal origin and population genetic structure ered in the KNR indicated that the level of Gasterophilus infec- of the G. pecorum prevalent in the desert steppe of Xinjiang, tion was highest in Przewalski’s horse, followed by that in the China, with the aims of elucidating the mechanism behind the sympatric Asiatic wild ass, Equus hemionus (Perissodactyla: differences in infection levels of Gasterophilus among three host Equidae), and lowest in the domestic horse, Equus caballus. species, and providing guidance for the control of this parasite Gasterophilus pecorum was the dominant species and was found and for the conservation of Przewalski’s horse. to aggressively attack equids in the KNR and to account for the vast majority of all parasites infecting equids (Liu, 2012). The reason for the differences in levels of infection among the Materials and methods three host species remains unknown. It is possible that the level of infection was most severe in Przewalski’s horses because Larvae collection they had been affected by inbreeding depression (Anna et al., 2008). Other plausible explanations include a specific host pref- Gasterophilus pecorum larvae were collected from the KNR in erence of G. pecorum or a variable population of G. pecorum, January 2013. A total of 116, 31 and 48 samples of G. pecorum in which different variants infect specific host species. Elucidat- larvae were collected from the three host species of Przewalski’s ing the mechanisms underpinning the disparate levels of infec- horse, the domestic horse and the Asiatic wild ass, respectively. tion may clarify mechanisms of parasite infection in general and Gasterophilus pecorum larvae from the faeces of Przewalski’s specifically provide management and conservation measures to horses and domestic horses were collected after deworming; aid in the control of Gasterophilus infections in Przewalski’s larvae from the Asiatic wild ass were collected at autopsy from horses. The finding that G. pecorum is the dominant botfly con- an animal killed in an accident at the same time as the other trasts with reports indicating that G. intestinalis and G. nasalis two species were dewormed. All larvae were placed in ethanol are the dominant species in other regions of the world (Horak and identified using morphology (Zumpt, 1965). The larvae et al., 1984; Otranto et al., 2005a). Given the desert steppe con- identified
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