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Genetic Analysis Confirms the Presence of Dicrocoelium Dendriticum in the Himalaya Ranges of Pakistan. Muhammad Asim Khana, Kira

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Genetic Analysis Confirms the Presence of Dicrocoelium Dendriticum in the Himalaya Ranges of Pakistan. Muhammad Asim Khana, Kira bioRxiv preprint doi: https://doi.org/10.1101/2020.06.02.130070; this version posted June 3, 2020. The copyright holder has placed this preprint (which was not certified by peer review) in the Public Domain. It is no longer restricted by copyright. Anyone can legally share, reuse, remix, or adapt this material for any purpose without crediting the original authors. 1 Genetic analysis confirms the presence of Dicrocoelium dendriticum in the 2 Himalaya ranges of Pakistan. 3 4 Muhammad Asim Khana, Kiran Afshana*, Muddassar Nazara, Sabika Firasata, Umer 5 Chaudhryb*, Neil D. Sargisonb 6 7 a Department of Zoology, Faculty of Biological Sciences, Quaid-i-Azam University, 8 Islamabad, 45320, Pakistan. 9 10 b University of Edinburgh, Royal (Dick) School of Veterinary Studies and Roslin 11 Institute, Easter Bush Veterinary Centre, UK, EH25 9RG 12 13 *Corresponding Authors 14 15 Kiran Afshan 16 Email: [email protected] , Tel:00925190643252 17 Department of Zoology, Faculty of Biological Sciences, Quaid-i-Azam University, 18 Islamabad, 45320, Pakistan. 19 20 Umer Chaudhry 21 Email: [email protected], Tel: 00441316519244 22 University of Edinburgh, R(D)SVS, Easter Bush Veterinary Centre, UK, EH25 9RG 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 Abstract 49 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.02.130070; this version posted June 3, 2020. The copyright holder has placed this preprint (which was not certified by peer review) in the Public Domain. It is no longer restricted by copyright. Anyone can legally share, reuse, remix, or adapt this material for any purpose without crediting the original authors. 50 Lancet liver flukes of the genus Dicrocoelium (Trematoda: Digenea) are 51 recognised parasites of domestic and wild herbivores. The aim of the present study 52 was to address a lack of knowledge of lancet flukes in the Himalaya ranges of 53 Pakistan by characterising Dicrocoelium species collected from the Chitral valley. 54 The morphology of 48 flukes belonging to eight host populations was examined in 55 detail and according to published keys, they were identified as either D. dendriticum 56 or Dicrocoelium chinensis. PCR and sequencing of fragments of ribosomal cistron 57 DNA, and cytochrome oxidase-1 (COX-1) and NADH dehydrogenase-1 (ND-1) 58 mitochondrial DNA from 34, 14 and 3 flukes revealed 10, 4 and 1 unique haplotypes, 59 respectively. Single nucleotide polymorphisms in these haplotypes were used to 60 differentiate between D. chinensis and D. dendriticum, and confirm the molecular 61 species identity of each of the lancet flukes as D. dendriticum. Phylogenetic 62 comparison of the D. dendriticum rDNA, COX-1 and ND-1 sequences with those 63 from D. chinensis, Fasciola hepatica and Fasciola gigantica species was performed 64 to assess within and between species variation and validate the use of species- 65 specific markers for D. dendriticum. Genetic variations between D. dendriticum 66 populations derived from different locations in the Himalaya ranges of Pakistan 67 illustrate the potential impact of animal movements on gene flow. This work provides 68 a proof of concept for the validation of species-specific D. dendriticum markers and 69 is the first molecular confirmation of this parasite species from the Himalaya ranges 70 of Pakistan. The characterisation of this parasite will allow research questions to be 71 addressed on its ecology, biological diversity, and epidemiology. 72 73 74 Keywords: Dicrocoelium dendriticum; ribosomal and mitochondrial markers; 75 morphological measurements. 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 1. Introduction 98 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.02.130070; this version posted June 3, 2020. The copyright holder has placed this preprint (which was not certified by peer review) in the Public Domain. It is no longer restricted by copyright. Anyone can legally share, reuse, remix, or adapt this material for any purpose without crediting the original authors. 99 Digenean lancet liver flukes of the family Dicrocoeliidae (Trematoda: Digenea) 100 can infect the bile ducts of a variety of wild and domesticated mammals and humans 101 around the globe. Three species of the genus Dicrocoelium, namely Dicrocoelium 102 dendriticum, Dicrocoelium hospes and Dicrocoelium chinensis have been described 103 as causes of dicrocoeliosis in domestic and wild ruminants (Otranto and Traversa, 104 2003). Among these, D. dendriticum is the most common and is distributed 105 throughout Europe, Asia, North and South America, Australia, and North Africa 106 (Arias et al., 2011). The main economic impact of dicrocoeliosis in livestock is due to 107 the rejection of livers from slaughtered animals at meat inspection (Rojo-Vazquez et 108 al., 2012). However, in severe infections, affected animals may show clinical signs 109 including poor food intake, ill thrift, poor milk production, alteration in fecal 110 consistency, photosensitisation and anaemia (Manga-Gonzalez et al., 2004; 111 Sargison et al., 2012). 112 The life history of Dicrocoelium spp. is indirect and may take at least six 113 months to complete. Monoecious and both sexually reproducing and self-fertilising 114 adults are found in the bile ducts. Eggs containing fully-developed miracidia are shed 115 in faeces and must be eaten by land snails before hatching. Miracidia penetrate the 116 gut wall of the snails and undergo asexual replication and development into 117 cercariae, which then escape from the snails in their slime trails, and are eaten by 118 ants. One cercaria migrates to the head of the ant and associates with the sub- 119 oesophageal ganglion; while up to about 50 cercariae encyst in the gaster as 120 metacercariae (Martín-Vega et al., 2018). The larval stage that develops in the ant’s 121 head alters its behaviour, making it cling to herbage and increasing the probability of 122 its being eaten by a herbivorous definitive host. Unlike Fasciola spp., larval flukes 123 migrate to the liver via the biliary tree and develop to adults in the bile ducts (Manga- 124 Gonzalez et al., 2001). Several species of land snails and ants are known to be 125 intermediate hosts within the same geographical location (Mitchell et al., 2017). 126 Most cases of dicrocoeliosis are subclinical, hence remain undetected 127 (Ducommun and Pfister, 1991). Dicrocoelium spp. cause cholangitis; with the 128 thickened bile ducts appearing as white spots on cut surfaces of the liver (Jithendran 129 and Bhat, 1996). The diagnosis of dicrocoeliosis in live animals is usually based on 130 the identification of characteristic eggs in faecal samples, for example by floatation in 131 saturated zinc sulphate solution (Sargison et al., 2012). However, coprological 132 methods only detect patent infections, and their sensitivity may be low. Experimental 133 immunodiagnostic methods have been developed to detect anti-Dicrocoelium 134 antibodies (Jithendran et al., 1996; Gonzalez-Lanza et al., 2000; Broglia et al., 135 2009), but these are not available in the field. 136 Molecular methods amplifying fragments of the ribosomal cistron or 137 mitochondrial loci DNA have been developed (Rehman et al., 2020); but as with all 138 molecular diagnostic tools, these depend on accurate speciation of the reference 139 parasites. There are few studies shown the value of ribosomal cistron or 140 mitochondrial loci DNA for the accurate species differentiation of Dicrocoeliidae 141 genera including D. dendriticum and D. chinensis with little or no information of D. 142 hospes (Maurelli et al., 2007; Otranto et al., 2007; Martinez-Ibeas et al., 2011; Bian 143 et al., 2015; Gorjipoor et al., 2015). These molecular methods have also been 144 adapted to demonstrate the genetic variability and phylogeny of various trematode 145 parasite species affecting ruminant livestock (Chaudhry et al., 2016; Ali et al., 2018; 146 Sargison et al., 2019; Rehman et al., 2020) with limited information on Dicrocoeliidae 147 genera. bioRxiv preprint doi: https://doi.org/10.1101/2020.06.02.130070; this version posted June 3, 2020. The copyright holder has placed this preprint (which was not certified by peer review) in the Public Domain. It is no longer restricted by copyright. Anyone can legally share, reuse, remix, or adapt this material for any purpose without crediting the original authors. 148 In this study, we describe the morphological features of Dicrocoelium spp. 149 infecting sheep in the Himalaya ranges of Pakistan. The fragments of ribosomal 150 DNA, cytochrome oxidase-1 (COX-1) and NADH dehydrogenase-1 (ND-1) mtDNA 151 were amplified to confirm the species identity of D. dendriticum. The genomic 152 sequence data were used to describe the genetic variability and phylogenetic 153 relationships of the Pakistani D. dendriticum with the limited number of other 154 Dicrocoelium spp. for which matching sequence data are available. Finally, the 155 sequence data were compared with those of Fasciola hepatica and Fasciola 156 gigantica liver flukes that are the important differential clinical and pathological 157 diagnosis for dicrocoeliosis in ruminant livestock in northern Pakistan. 158 159 2. Materials and Methods 160 161 2.1. Fluke collection 162 163 A total of 144 sheep from the Chitral valley were examined; comprising of 68 164 from Booni, 26 from Torkhow, 33 from Mastuj and 17 from the Laspoor valley (Fig. 165 1). Overall, 639 adult flukes (25 to 50 flukes per animal) were obtained from the 166 livers 16 infected sheep, slaughtered at each of the different localities in the Chitral 167 valley. In all cases, the size and gross morphology of the flukes were typical of 168 Dicrocoelium spp. The flukes were washed with phosphate-buffered saline (PBS) to 169 remove adherent debris and fixed in 70% ethanol for subsequent morphometric and 170 molecular characterisation.
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