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Update on the genetic diversity and population structure of Echinococcus granulosus in Gansu Province, Tibet Autonomous Region, and Xinjiang Uygur Autonomous Region, Western China, inferred from mitochondrial cox1, nad1, and nad5 sequences

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Abstract

The identification of additional Echinococcus granulosus sensu lato (s.l.) complex species/genotypes in recent years raises the possibility that there might be more variation among this species in China than is currently understood. The aim of this study was to explore intra- and inter-species variation and population structure of Echinococcus species isolated from sheep in three areas of Western China. Of the isolates, 317, 322, and 326 were successfully amplified and sequenced for cox1, nad1, and nad5 genes, respectively. BLAST analysis revealed that the majority of the isolates were E. granulosus s.s., and using the cox1, nad1, and nad5 genes, respectively, 17, 14, and 11 isolates corresponded to Elodea canadensis (genotype G6/G7). In the three study areas, G1 genotypes were the most prevalent. There were 233 mutation sites along with 129 parsimony informative sites. A transition/transversion ratio of 7.5, 8, and 3.25, respectively, for cox1, nad1, and nad5 genes was obtained. Every mitochondrial gene had intraspecific variations, which were represented in a star-like network with a major haplotype with observable mutations from other distant and minor haplotypes. The Tajima’s D value was significantly negative in all populations, indicating a substantial divergence from neutrality and supporting the demographic expansion of E. granulosus s.s. in the study areas. The phylogeny inferred by the maximum likelihood (ML) method using nucleotide sequences of cox1–nad1–nad5 further confirmed their identity. The nodes assigned to the G1, G3, and G6 clades as well as the reference sequences utilized had maximal posterior probability values (1.00). In conclusion, our study confirms the existence of a significant major haplotype of E. granulosus s.s. where G1 is the predominant genotype causing of CE in both livestock and humans in China.

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All data generated or analyzed in this paper are provided as supplementary material file.

Abbreviations

AIC:

Akaike Information Criterion

AMOVA:

Analysis of molecular variance

BIC:

Bayesian Information Criterion

CDC:

Centers for Disease Control and Prevention

CE:

Cystic echinococcosis

DALYs:

Disability-adjusted life-years

FERG:

Foodborne Disease Burden Epidemiology Reference Group

MCMC:

Markov Chain Monte Carlo

NCBI:

National Center for Biotechnology Information

OIE:

Office International des Epizooties

PopART:

Population Analysis with Reticulate Trees

PSRF:

Potential scale reduction factor

References

  • Addy F, Wassermann M, Kagendo D, Ebi D, Zeyhle E, Elmahdi IE, Umhang G, Casulli A, Harandi MF, Aschenborn O, Kern P, Mackenstedt U, Romig T (2017) Genetic differentiation of the G6/7 cluster of Echinococcus canadensis based on mitochondrial marker genes. Int J Parasitol 47:923–931. https://doi.org/10.1016/j.ijpara.2017.06.003

    Article  CAS  PubMed  Google Scholar 

  • Ahmadi NA, Badi F (2011) Human hydatidosis in Tehran, Iran: a retrospective epidemiological study of surgical cases between 1999 and 2009 at two university medical centers. Trop Biomed 28:450–456

    CAS  PubMed  Google Scholar 

  • Alvi MA, Ohiolei JA, Saqib M, Li L, Tayyab MH, Alvi AA, Wu YT, Fu BQ, Yan HB, Jia WZ (2020) Echinococcus granulosus (sensu stricto) (G1, G3) and E. ortleppi (G5) in Pakistan: phylogeny, genetic diversity and population structural analysis based on mitochondrial DNA. Parasit Vectors 13(1):347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, p 447

    Book  Google Scholar 

  • Bai TJ, Yang WD, Bai TX, Ma YS (2011) Investigation and control measures of hydatid infection in sheep in Tianzhu County. Anim Husb Vet Med 61:73–75 (In Chinese)

    Google Scholar 

  • Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48

    Article  CAS  PubMed  Google Scholar 

  • Barazesh A, Sarkari B, Ebrahimi S, Hami M (2018) DNA extraction from hydatid cyst protoscolices: comparison of five different methods. Vet World 11:231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonelli P, Dei Giudici S, Peruzzu A, Piseddu T, Santucciu C, Masu G, Mastrandrea S, Delogu ML, Masala G (2020) Genetic diversity of Echinococcus granulosus sensu stricto in Sardinia (Italy). Parasitol Int 77:102120. https://doi.org/10.1016/j.parint.2020.102120

    Article  CAS  PubMed  Google Scholar 

  • Boubaker G, Macchiaroli N, Prada L, Cucher MA, Rosenzvit MC, Ziadinov I, Deplazes P, Saarma U, Babba H, Gottstein B, Spiliotis M (2013) A multiplex PCR for the simultaneous detection and genotyping of the Echinococcus granulosus complex. PLoS Negl Trop Dis 7(1):e2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boufana B, Lahmar S, Rebaï W, Ben Safta Z, Jebabli L, Ammar A, Kachti M, Aouadi S, Craig PS (2014) Genetic variability and haplotypes of Echinococcus isolates from Tunisia. Trans R Soc Trop Med Hyg 108(11):706–714. https://doi.org/10.1093/trstmh/tru138

    Article  CAS  PubMed  Google Scholar 

  • Bowles J, McManus DP (1993) NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. Int J Parasitol 23:969–972

    Article  CAS  PubMed  Google Scholar 

  • Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54:165–173

    Article  CAS  PubMed  Google Scholar 

  • Bowles J, Blair D, McManus D (1994) Molecular genetic characterization of the cervid strain (‘northern form’) of Echinococcus granulosus. Parasitology 109:215–221

    Article  CAS  PubMed  Google Scholar 

  • Brunetti E, Garcia HH, Junghanss T (2011) Cystic echinococcosis: chronic, complex, and still neglected. PLoS Negl Trop Dis 5:e1146. https://doi.org/10.1371/journal.pntd.0001146

    Article  PubMed  PubMed Central  Google Scholar 

  • Carlos M, Tamara O (2016) Molecular epidemiology of cystic echinococcosis: genotypic characterization in humans and different livestock. Int J Morphol 34:1472–1481

    Article  Google Scholar 

  • Carmena D, Cardona GA (2014) Echinococcosis in wild carnivorous species: epidemiology, genotypic diversity, and implications for veterinary public health. Vet Parasitol 202:69–94

    Article  PubMed  Google Scholar 

  • Casulli A, Interisano M, Sreter T, Chitimia L, Kirkova Z, La Rosa G, Pozio E (2012) Genetic variability of Echinococcus granulosus sensu stricto in Europe inferred by mitochondrial DNA sequences. Infect Genet Evol l 12:377

    Article  CAS  Google Scholar 

  • CDC (2022) Resources for Health Professionals. Available at https://www.cdc.gov/parasites/echinococcosis/health_professionals/index.html. Last accessed on 12 Feb 2022

  • Craig PS, Hegglin D, Lightowlers MW, Torgerson PR, Wang Q (2017) Echinococcosis: control and prevention. Adv Parasitol 96:55–158

    Article  CAS  PubMed  Google Scholar 

  • Crandall KA, Posada D, Vasco D (1999) Effective population sizes: missing measures and missing concepts. Anim Conserv 2:317–319

    Article  Google Scholar 

  • Cucher MA, Macchiaroli N, Baldi G, Camicia F, Prada L, Maldonado L, Avila HG, Fox A, Gutierrez A, Negro P, Lopez R, Jensen O, Rosenzvit M, Kamenetzky L (2016) Cystic echinococcosis in South America: systematic review of species and genotypes of Echinococcus granulosus sensu lato in humans and natural domestic hosts. Trop Med Int Health 21(2):166–175. https://doi.org/10.1111/tmi.12647

    Article  PubMed  Google Scholar 

  • Dao JC, Ge D, Wan DC (2006) Epidemiological investigation of hydatid disease in Maqu County, Gannan Prefecture. China Anim Health 9:34–36 (In Chinese)

    Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deplazes P, Rinaldi L, Rojas CA, Torgerson PR, Harandi MF, Romig T, Antolova D, Schurer JM, Lahmar S, Cringoli G, Magambo J (2017) Global distribution of alveolar and cystic echinococcosis. Adv Parasitol 95:315–493. https://doi.org/10.1016/bs.apar.2016.11.001

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10(3):564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farhadi M, Fazaeli A, Haniloo A (2015) Genetic characterization of livestock and human hydatid cyst isolates from northwest Iran, using the mitochondrial cox1 gene sequence. Parasitol Res 114:4363–4370

    Article  PubMed  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galeh TM, Spotin A, Mahami-Oskouei M, Carmena D, Rahimi MT, Barac A, Ghoyounchi R, Berahmat R, Ahmadpour E (2018) The seroprevalence rate and population genetic structure of human cystic echinococcosis in the Middle East: a systematic review and meta-analysis. Int J Surg 51:39–48

    Article  PubMed  Google Scholar 

  • Gao Y, Wang W, Lyu C, Wei XY, Chen Y, Zhao Q, Ran ZG, Xia YQ (2021) Meta-analysis of the prevalence of Echinococcus in sheep in China from 1983 to 2020. Front Cell Infect Microbiol 11:711332. https://doi.org/10.3389/fcimb.2021.711332

    Article  PubMed  PubMed Central  Google Scholar 

  • Gelman A, Rubin DA (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–472

    Article  Google Scholar 

  • Giraudoux P, Zhao Y, Afonso E, Yan HB, Knapp J, Rogan MT, Shi DZ, Jia WZ, Craig PS (2019) Long-term retrospective assessment of a transmission hotspot for human alveolar echinococcosis in mid-west China. PLoS Negl Trop Dis 30:e0007701

    Article  Google Scholar 

  • Gong QL, Ge GY, Wang Q, Tian T, Liu F, Diao NC, Nie LB, Zong Y, Li JM, Shi K, Leng X (2021) Meta-analysis of the prevalence of Echinococcus in dogs in China from 2010 to 2019. PLoS Negl Trop Dis 15(4):e0009268. https://doi.org/10.1371/journal.pntd.0009268

    Article  PubMed  PubMed Central  Google Scholar 

  • Gossios KJ, Kontoyiannis DS, Dascalogiannaki M, Gourtsoyiannis NC (1997) Uncommon locations of hydatid disease: CT appearances. Eur Radiol 7:1303–1308. https://doi.org/10.1007/s003300050293

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Guo BP, Zhang ZZ, Zheng XT, Guo YZ, Guo G, Zhao L, Cai R, Wang BJ, Yang M, Shou X, Zhang WB, Jia B (2019) Prevalence and molecular characterization of Echinococcus granulosus sensu stricto in northern Xinjiang, China. Korean J Parasitol 57:153–159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo BP, Zhang ZG, Guo YZ, Guo G, Wang HY, Ma JJ, Chen RG, Zheng XT, Bao JL, He L, Wang T, Qi WJ, Tian MX, Wang JW, Zhou CL, Giraudoux P, Marston CG, McManus DP, Zhang WB, Li J (2021) High endemicity of alveolar echinococcosis in Yili Prefecture, Xinjiang Autonomous Region, the People’s Republic of China: infection status in different ethnic communities and in small mammals. PLoS Negl Trop Dis 15(1):e0008891

    Article  PubMed  PubMed Central  Google Scholar 

  • Haag KL, Ayala FJ, Kamenetzky L, Gutierrez AM, Rosenzvit M (2004) Livestock trade history, geography, and parasite strains: the mitochondrial genetic structure of Echinococcus granulosus in Argentina. J Parasitol 90:234–239

    Article  CAS  PubMed  Google Scholar 

  • Hajialilo E, Harandi MF, Sharbatkhori M, Mirhendi H, Rostami S (2011) Genetic characterization of Echinococcus granulosus in camels, cattle and sheep from the south-east of Iran indicates the presence of the G3 genotype. J Helminthol 13:1–8

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic Acids Symposium Series 41(41):95–98

    CAS  Google Scholar 

  • Han XM, Jian YN, Zhang XY, Ma LQ, Zhu WJ, Cai QG, Wu SL, Wang XQ, Shi BQ (2019) Genetic characterization of Echinococcus isolates from various intermediate hosts in the Qinghai-Tibetan Plateau Area, China. Parasitology 146(10):1305–1312

    Article  CAS  PubMed  Google Scholar 

  • Holsinger KE, Weir BS (2009) Genetics in geographically structured populations: defining, estimating and interpreting Fst. Nat Rev Genet 10(9):639–650. https://doi.org/10.1038/nrg2611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsieh CM, Falkenheim VC (2022) “Xinjiang”. Encyclopedia Britannica, available at https://www.britannica.com/place/Xinjiang. Accessed 12 Aug 2022

  • Hua RQ, Xie Y, Song HY, Shi Y, Zhan JF, Wu MD, Gu XB, Peng XR, Yang GY (2019) Echinococcus canadensis G8 Tapeworm Infection in a Sheep, China, 2018. Emerg Infect Dis 25:1420–1422

    Article  PubMed  PubMed Central  Google Scholar 

  • Hüttner M, Romig T (2009) Echinococcus species in African wildlife. Parasitology 136(10):1089–1095

    Article  PubMed  Google Scholar 

  • Jenkins DJ, Romig T, Thompson RC (2005) Emergence/re-emergence of Echinococcus spp.–a global update. Int J Parasitol 35:1205–1219. https://doi.org/10.1016/j.ijpara.2005.07.014

    Article  CAS  PubMed  Google Scholar 

  • Joanny G, Mehmood N, Dessì G, Tamponi C, Nonnis F, Hosri C, Saarma U, Varcasia A, Scala A (2021) Cystic echinococcosis in sheep and goats of Lebanon. Parasitology 148(7):871–878

    Article  CAS  PubMed  Google Scholar 

  • Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karki R, Pandya D, Elston RC, Ferlini C (2015) Defining “mutation” and “polymorphism” in the era of personal genomics. BMC Med Genomics 8:37. https://doi.org/10.1186/s12920-015-0115-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kern P, Da Silva AM, Akhan O, Müllhaupt B, Vizcaychipi KA, Budke C, Vuitton DA (2017) The echinococcoses: diagnosis, clinical management and burden of disease. Adv Parasitol 96:259–369. https://doi.org/10.1016/bs.apar.2016.09.006

    Article  CAS  PubMed  Google Scholar 

  • Kinkar L, Laurimäe T, Simsek S, Balkaya I, Casulli A, Manfredi MT, Ponce-Gordo F, Varcasia A, Lavikainen A, Gonzalez LM, Rehbein S (2016) High-resolution phylogeography of zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1 with an emphasis on its distribution in Turkey, Italy and Spain. Parasitology 143(13):1790–1801. https://doi.org/10.1017/S0031182016001530

    Article  PubMed  Google Scholar 

  • Kinkar L, Laurimäe T, Acosta-Jamett G, Andresiuk V, Balkaya I, Casulli A, Gasser RB, González LM, Haag KL, Zait H, Irshadullah M, Jabbar A, Jenkins DJ, Manfredi MT, Mirhendi H, M’rad S, Rostami-Nejad M, Oudni-M’rad M, Pierangeli NB, Ponce-Gordo F, Rehbein S, Sharbatkhori M, Kia EB, Simsek S, Soriano SV, Sprong H, Šnábel V, Umhang G, Varcasia A, Saarma U (2018a) Distinguishing Echinococcus granulosus sensu stricto genotypes G1 and G3 with confidence: a practical guide. Infect Genet Evol 64:178–184. https://doi.org/10.1016/j.meegid.2018.06.026

    Article  PubMed  Google Scholar 

  • Kinkar L, Laurimäe T, Balkaya I, Casulli A, Zait H, Irshadullah M, Sharbatkhori M, Mirhendi H, Rostami Nejad M, Ponce-Gordo F, Rehbein S, Kia EB, Simsek S, Šnabel V, Umhang G, Varcasia A, Saarma U (2018b) Genetic diversity and phylogeography of the elusive, but epidemiologically important Echinococcus granulosus sensu stricto genotype G3. Parasitology 145:1613–1622. https://doi.org/10.1017/S0031182018000549

    Article  CAS  PubMed  Google Scholar 

  • Kinkar L, Laurimäe T, Acosta-Jamett G, Andresiuk V, Balkaya I, Casulli A, Gasser RB, Giessen J, Miguel González L, Haag KL, Zait H, Irshadullah M, Jabbar A, Jenkins DJ, Kia EB, Manfredi MT, Mirhendi H, M’rad S, Rostami-Nejad M, Oudni-M’rad M, Beatriz Pierangeli N, Ponce-Gordo F, Rehbein S, Sharbatkhori M, Simsek S, Viviana Soriano S, Sprong H, Šnábel V, Umhang G, Varcasia A, Saarma U (2018c) Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1. Int J Parasitol 48(9–10):729–742. https://doi.org/10.1016/j.ijpara.2018.03.006

    Article  PubMed  Google Scholar 

  • Kinkar L, Korhonen PK, Cai H, Gauci CG, Lightowlers MW, Saarma U, Jenkins DJ, Li J, Li J, Young ND, Gasser RB (2019) Long-read sequencing reveals a 4.4 kb tandem repeat region in the mitogenome of Echinococcus granulosus (sensu stricto) genotype G1. Parasites Vectors 12(1):1–7

    Article  CAS  Google Scholar 

  • Knight A, Mindell DP (1993) Substitution bias, weighting of DNA sequence evolution, and the phylogenetic position of Fea’s viper. Syst Biol 42(1):18–31

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laurimaa L, Davison J, Süld K, Plumer L, Oja R, Moks E, Keis M, Hindrikson M, Kinkar L, Laurimäe T, Abner J (2015) First report of highly pathogenic Echinococcus granulosus genotype G1 in dogs in a European urban environment. Parasit Vectors 8(1):1–5

    Article  Google Scholar 

  • Laurimäe T, Kinkar L, Andresiuk V, Haag KL, Ponce-Gordo F, Acosta Jamett G, Garate T, Gonzalez LM, Saarma U (2016) Genetic diversity and phylogeography of highly zoonotic Echinococcus granulosus genotype G1 in the Americas (Argentina, Brazil, Chile and Mexico) based on 8279 bp of mtDNA. Infect Genet Evol 45:290–296. https://doi.org/10.1016/j.meegid.2016.09.015

    Article  CAS  PubMed  Google Scholar 

  • Laurimäe T, Kinkar L, Romig T, Omer RA, Casulli A, Umhang G, Gasser R, Jabbar A, Sharbatkori M, Mirhendi H, Ponce-Gordo F, Lazzarini L, Soriano SV, Varcasia A, Rostami-Nejad M, Andresiuk V, Maravilla P, Gonzalez L, Dybicz M, Gawor J, Šarkunas M, Snabel V, Kuzmina T, Saarma U (2018) The benefits of analysing complete mitochondrial genomes: deep insights into the phylogeny and population structure of Echinococcus granulosus sensu lato genotypes G6 and G7. Infect Genet Evol 64:85–94. https://doi.org/10.1016/j.meegid.2018.06.016

    Article  CAS  PubMed  Google Scholar 

  • Laurimäe T, Kinkar L, Romig T, Umhang G, Casulli A, Omer RA, Sharbatkhori M, Mirhendi H, Ponce-Gordo F, Lazzarini LE, Soriano SV (2019) Analysis of nad2 and nad5 enables reliable identification of genotypes G6 and G7 within the species complex Echinococcus granulosus sensu lato. Infect Genet Evol 74:103941

    Article  PubMed  Google Scholar 

  • Lavikainen A, Lehtinen MJ, Meri T, Hirvelä-Koski V, Meri S (2003) Molecular genetic characterization of the Fennoscandian cervid strain, a new genotypic group (G10) of Echinococcus granulosus. Parasitology 127:207–215

    Article  CAS  PubMed  Google Scholar 

  • Leigh JW, Bryant D (2015) PopART: Full-feature software for haplotype network construction. Methods Ecol Evol 6(9):1110–1116. https://doi.org/10.1111/2041-210X.12410

    Article  Google Scholar 

  • Li JF (2018) Epidemiological investigation of sheep echinococcosis in Yumen City. Gansu Agr Univ 50:1–50 (In Chinese)

    Google Scholar 

  • Li D, Gao Q, Liu J, Feng Y, Ning WH, Dong YQ, Tao LX, Li JY, Tian XJ, Gu J, Xin D (2015) Knowledge, attitude, and practices (KAP) and risk factors analysis related to cystic echinococcosis among residents in Tibetan communities, Xiahe County, Gansu Province, China. Acta Trop 147:17–22

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma SM, Maillard S, Zhao HL, Huang X, Wang H, Geng PL, Bart JM, Piarroux R (2008) Assessment of Echinococcus granulosus polymorphism in Qinghai province, People’s Republic of China. Parasitol Res 102(6):1201–1206

    Article  CAS  PubMed  Google Scholar 

  • Ma T, Jiang D, Hao MM, Fan PW, Zhang SZ, Quzhen GS, Xue CZ, Han S, Wu WP, Zheng CJ, Ding FU (2021) Geographical detector-based influence factors analysis for echinococcosis prevalence in Tibet, China. Plos Negl Trop Dis 15(7):e0009547

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahami-Oskouei M, Kaseb-Yazdanparast A, Spotin A, Shahbazi A, Adibpour M, Ahmadpour E, Ghabouli-Mehrabani N (2016) Gene flow for Echinococcus granulosus meta-populations determined by mitochondrial sequences: a reliable approach for reflecting epidemiological drift of parasite among neighboring countries. Exp Parasitol 171:77–83

    Article  PubMed  Google Scholar 

  • Martín JP, Hernández Bermejo JE (2000) Genetic variation in the endemic and endangered Rosmarinus tomentosus Huber-Morath and Maire (Labiatae) using RAPD markers. Heredity 85(5):434–443

    Article  PubMed  Google Scholar 

  • Mehmood N, Muqaddas H, Arshad M, Ullah MI, Khan ZI (2020a) Comprehensive study based on mtDNA signature (nad1) providing insights on Echinococcus granulosus s.s. genotypes from Pakistan and potential role of buffalo-dog cycle. Infect Genet Evol 81:104271. https://doi.org/10.1016/j.meegid.2020.104271

    Article  CAS  PubMed  Google Scholar 

  • Mehmood S, Simsek S, Celik F, Kesik HK, Kilinc SG, Ahmed H (2020b) Molecular survey on cattle and sheep hydatidosis and first detection of Echinococcus canadensis (G6/G7) in sheep in Turkey. Parasitology 147(9):1055–1062

    Article  CAS  PubMed  Google Scholar 

  • Mehmood N, Dessì G, Ahmed F, Joanny G, Tamponi C, Cappai MG, Varcasia A, Scala A (2021) Genetic diversity and transmission patterns of Echinococcus granulosus sensu stricto among domestic ungulates of Sardinia, Italy. Parasitol Res 120(7):2533–2542

    Article  PubMed  PubMed Central  Google Scholar 

  • Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061–1064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moro P, Schantz PM (2009) Echinococcosis: a review. Int J Infect Dis 13(2):125–133

    Article  CAS  PubMed  Google Scholar 

  • Nakamura K, Ito A, Yara S, Haranaga S, Hibiya K, Hirayasu T, Sako Y, Fujita J (2011) Case report: a case of pulmonary and hepatic cystic echinococcosis of CE1 stage in a healthy Japanese female that was suspected to have been acquired during her stay in the United Kingdom. Am J Trop Med Hyg 85(3):456–459

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakao M, Yokoyama N, Sako Y, Fukunaga M, Ito A (2002) The complete mitochondrial DNA sequence of the cestode Echinococcus multilocularis (Cyclophyllidea: Taeniidae). Mitochondrion 1(6):497–509

    Article  CAS  PubMed  Google Scholar 

  • Nakao M, Sako Y, Ito A (2003) The mitochondrial genome of the tapeworm Taenia solium: a finding of the abbreviated stop codon U. J Parasitol 89(3):633–635

    Article  CAS  PubMed  Google Scholar 

  • Nakao M, McManus DP, Schantz PM, Craig PS, Ito A (2006) A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134(5):713–722

    Article  PubMed  Google Scholar 

  • Nakao M, Li T, Han X, Ma X, Xiao N, Qiu J, Wang H, Yanagida T, Mamuti W, Wen H, Moro PL, Giraudoux P, Craig PS, Ito A (2010) Genetic polymorphisms of Echinococcus tapeworms in China as determined by mitochondrial and nuclear DNA sequences. Int J Parasitol 40:379–385

    Article  CAS  PubMed  Google Scholar 

  • Nakao M, Lavikainen A, Yanagida T, Ito A (2013a) Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae). Int J Parasitol 43(12–13):1017–1029

    Article  CAS  PubMed  Google Scholar 

  • Nakao M, Yanagida T, Konyaev S, Lavikainen A, Odnokurtsev VA, Zaikov VA, Ito A (2013b) Mitochondrial phylogeny of the genus Echinococcus (Cestoda: Taeniidae) with emphasis on relationships among Echinococcus canadensis genotypes. Parasitology 140(13):1625–1636

    Article  CAS  PubMed  Google Scholar 

  • Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300

    Article  CAS  PubMed  Google Scholar 

  • Obwaller A, Schneider R, Walochnik J, Gollackner B, Deutz A, Janitschke K, Aspöck H, Auer H (2004) Echinococcus granulosus strain differentiation based on sequence heterogeneity in mitochondrial genes of cytochrome c oxidase-1 and NADH dehydrogenase-1. Parasitology 128(5):569–575

    Article  CAS  PubMed  Google Scholar 

  • Ohiolei JA, Xia CY, Li L, Liu JZ, Tang WQ, Wu YT, Danqulamu, Zhu GQ, Shi B, Fu BQ, Yin H, Yan HB, Jia WZ (2019) Genetic variation of Echinococcus spp. in yaks and sheep in the Tibet Autonomous Region of China based on mitochondrial DNA. Parasit Vectors 12:608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohiolei JA, Yan HB, Odeniran PO, Li L, Shumuye NA, Qurishi SA, Isaac C, Fu BQ, Jia WZ (2022) Echinococcus granulosus sensu lato in animal intermediate hosts: what is with the organ location? Vet Parasitol 304:109695. https://doi.org/10.1016/j.vetpar.2022.109695

    Article  CAS  PubMed  Google Scholar 

  • OIE (2022) Echinococcosis. Available at https://www.oie.int/en/disease/echinococcosis/. Last accessed on 12 Feb 2022

  • Okonechnikov K, Golosova O, Fursov M, UGENE team (2012) Unipro UGENE: a unified bioinformatics toolNit. Bioinformatics 28(8):1166–1167. https://doi.org/10.1093/bioinformatics/bts091

    Article  CAS  PubMed  Google Scholar 

  • Omer RA, Dinkel A, Romig T, Mackenstedt U, Elnahas AA, Aradaib IE, Ahmed ME, Elmalik KH, Adam A (2010) A molecular survey of cystic echinococcosis in Sudan. Vet Parasitol 169(3–4):340–346

    Article  CAS  PubMed  Google Scholar 

  • Pednekar RP, Gatne ML, Thompson RC, Traub RJ (2009) Molecular and morphological characterization of Echinococcus from food producing animals in India. Vet Parasitol 165:58–65. https://doi.org/10.1016/j.vetpar.2009.06.021

    Article  PubMed  Google Scholar 

  • Qi YZ, Wen ZQ, Song T, Wang YS (2002) Epidemiological investigation of hydatidosis in Tianzhu Tibetan Autonomous County, Gansu Province. Endemic Dis Bull 18:51–53 (In Chinese)

    Google Scholar 

  • Qian MB, Abelaridder B, Wu WP, Zhou XN (2017) Combating echinococcosis in China: strengthening the research and development. Infect Dis Poverty 6:161. https://doi.org/10.1186/s40249-017-0374-3

    Article  PubMed  PubMed Central  Google Scholar 

  • Rojas CAA, Romig T, Lightowlers MW (2014) Echinococcus granulosus sensu lato genotypes infecting humans–review of current knowledge. Int J Parasitol 44(1):9–18. https://doi.org/10.1016/j.ijpara.2013.08.008

    Article  Google Scholar 

  • Rojas CAA, Ebi D, Paredes R, Acosta-Jamett G, Urriola N, Roa JC, Manterola C, Cortes S, Romig T, Scheerlinck JP, Lightowlers MW (2017) High intraspecific variability of Echinococcus granulosus sensu stricto in Chile. Parasitol Int 66(2):112–115. https://doi.org/10.1016/j.parint.2016.12.001

    Article  Google Scholar 

  • Romig T, Ebi D, Lato MW (2015) Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Vet Parasitol 213:76–84

    Article  CAS  PubMed  Google Scholar 

  • Romig T, Deplazes P, Jenkins D, Giraudoux P, Massolo A, Craig PS, Wassermann M, Takahashi K, de la Rue M (2017) Ecology and life cycle patterns of Echinococcus species. Adv Parasitol 95:213–314. https://doi.org/10.1016/bs.apar.2016.11.002

    Article  CAS  PubMed  Google Scholar 

  • Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao Librado P, Ramos-Onsins SE, Sanchez-Gracia A (2017) DnaSP v6: DNA sequence polymorphism analysis of large datasets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248

    Article  CAS  PubMed  Google Scholar 

  • Scott JC, Stefaniak J, Pawlowski ZS, McManus DP (1997) Molecular genetic analysis of human cystic hydatid cases from Poland: identification of a new genotypic group (G9) of Echinococcus granulosus. Parasitology 114:37–43

    Article  CAS  PubMed  Google Scholar 

  • Sharbatkhori M, Tanzifi A, Rostami S, Rostami M, Harandi MF (2016) Echinococcus granulosus sensu lato genotypes in domestic livestock and humans in Golestan Province, Iran. Rev Inst Med Trop Sao Paulo 58:38

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma M, Fomda BA, Mazta S, Sehgal R, Bagicha Singh B, Malla N (2013) Genetic diversity and population genetic structure analysis of Echinococcus granulosus sensu stricto complex based on mitochondrial DNA signature. PLoS ONE 8(12):e82904

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi YL, Wan XL, Wang ZY, Li J, Jiang ZH, Yang YC (2019) First description of Echinococcus ortleppi infection in China. Parasit Vectors 12:398

    Article  PubMed  PubMed Central  Google Scholar 

  • Siyadatpanah A, Daryani A, Sarvi S, Spotin A, Sharif M, Dizaji RE, Anvari D, Zeydi AE, Kohansal MH, Higuita NIA, Hosseini SA (2020) Phylogeography and genetic diversity of human hydatidosis in bordering the Caspian Sea, northern Iran by focusing on Echinococcus granulosus sensu stricto complex. Iranian J Public Health 49(9):1758–1768

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson RCA (2017) Biology and systematics of Echinococcus. Adv Parasitol 95:65–109

    Article  CAS  PubMed  Google Scholar 

  • Thompson RCA, McManus DP (2001) Aetiology: parasites and life-cycles. In: Eckert J, Gemmell M, Meslin F-X, Pawlowski Z (eds) WHOI/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. World Organization for Animal Health, 1–19

  • Wang JH, Wang N, Hu DD, Zhong XQ, Wang SX, Gu XB, Peng XR, Yang GY (2014) Genetic diversity of Echinococcus granulosus in southwest China determined by the mitochondrial NADH dehydrogenase subunit 2 gene. Sci World J 214:e867839

    Google Scholar 

  • Wang N, Wang JH, Hu DD, Zhong XQ, Jiang ZR, Yang A, Deng SJ, Guo L, Tsering D, Wang SX, Gu XB, Peng XR, Yang GY (2015) Genetic variability of Echinococcus granulosus based on the mitochondrial 16S ribosomal RNA gene. Mitochondrial DNA 26:396–401

    Article  CAS  PubMed  Google Scholar 

  • Wang N, Xie Y, Liu TY, Zhong XQ, Wang JH, Hu DD, Wang SX, Gu XB, Peng XR, Yang GG (2016) The complete mitochondrial genome of G3 genotype of Echinococcus granulosus (Cestoda: Taeniidae). Mitochondrial DNA Part A 27(3):1701–1702

    CAS  Google Scholar 

  • Wen XH, Wu XQ, Gao M (2017) Spatiotemporal variability of temperature and precipitation in Gansu Province (northwest China) during 1951–2015. Atmos Res 197:132–149

    Article  Google Scholar 

  • Wen H, Vuitton L, Tuxun TJ, Li J, Vuitton DA, Zhang WB, McManus DP (2019) Echinococcosis: advances in the 21st century. Clin Microbiol Rev 32:e00075-e118. https://doi.org/10.1128/CMR.00075-18

    Article  PubMed  PubMed Central  Google Scholar 

  • WHO (2021) Echinococcosis. Fact sheet (Updated May 2021). World Health Organization. Available at https://www.who.int/news-room/fact-sheets/detail/echinococcosis. Last accessed on 08 Nov 2021

  • Wu CC, Zhang WB, Ran B, Fan HN, Wang H, Guo BP, Zhou CL, Shao YM, Zhang W, Giraudoux P, Knapp J, Wen H, Kuang L, Li J (2017) Genetic variation of mitochondrial genes among Echinococcus multilocularis isolates collected in Western China. Parasit Vectors 10(1):1–7

    Article  Google Scholar 

  • Wu WP, Wang H, Wang Q, Zhou XN, Wang LY, Zheng CJ, Cao JP, Xiao N, Wang Y, Zhu YY, Niu YL, Xue CZ, Zeng XM, Fang Q, Han S, Yu Q, Yang SJ, Fu Q, Bai XF, Tian T, Li JJ, Zhang MY, Wu WT, Zhang SS, Hou YY, Feng Y, Ma X, Li B, Li FK, Guo WD, Yang YM, Wu XJ, Jin XJ, Zhang HW, Yu SC (2018a) A nationwide sampling survey on echinococcosis in China during 2012–2016. Chin J Parasitol Parasitic Dis 36(1):1–14

    Google Scholar 

  • Wu YT, Li L, Zhu GQ, Li WH, Zhang NZ, Li SN, Yao G, Tian WJ, Fu BQ, Yin H, Zhu XQ, Yan HB, Jia WZ (2018b) Mitochondrial genome data confirm that yaks can serve as the intermediate host of Echinococcus canadensis (G10) on the Tibetan Plateau. Parasit Vectors 11:166

    Article  PubMed  PubMed Central  Google Scholar 

  • Xia CY, Liu JZ, Tsering D, Yuan ZJ, Gesang D, Ban D (2014) Investigation of three finds of tapeworm larvae infections in Tibetan domestic animals. Chin Vet Sci 44:1205–1209. https://doi.org/10.16656/j.issn.1673-4696.2014.11.017 (In Chinese)

  • Xiao N, Qiu JM, Nakao M, Li TY, Yang W, Chen XW, Schantz PM, Craig PS, Ito A (2005) Echinococcus shiquicus n. sp., a taeniid cestode from Tibetan fox and plateau pika in China. Int J Parasitol 35:693–701

    Article  CAS  PubMed  Google Scholar 

  • Yan N, Nie HM, Jiang ZR, Yang AG, Deng SJ, Guo L, Yu H, Yan YB, Tsering D, Kong WS, Wang N, Wang JH, Xie Y, Fu Y, Yang DY, Wang SX, Gu XB, Peng XR, Yang GY (2013) Genetic variability of Echinococcus granulosus from the Tibetan plateau inferred by mitochondrial DNA sequences. Vet Parasitol 196(1–2):179–183

    Article  CAS  PubMed  Google Scholar 

  • Yan B, Liu XF, Wu JY, Zhao SS, Yuan WM, Wang BJ, Wureli H, Tu CC, Chen CF, Wang YZ (2018) Genetic diversity of Echinococcus granulosus genotype G1 in Xinjiang, northwest of China. Korean J Parasitol 56(4):391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan HB, Li L, Li WH, Zhu GQ, Li JQ, Wu YT, Zhang NZ, Wu YD, Li M, Zhang LS, Yao G, Tian WJ, Li L, Li WJ, Guo AM, Dai GD, Fu AQ, Ohiolei JA, Jia WZ (2021) Echinococcus shiquicus in Qinghai-Tibet plateau: population structure and confirmation of additional endemic areas. Parasitology 148(7):879–886

    Article  CAS  PubMed  Google Scholar 

  • Yang YR, Rosenzvit MC, Zhang LH, Zhang JZ, McManus DP (2005) Molecular study of Echinococcus in west-Central China. Parasitology 131(4):547–555. https://doi.org/10.1017/S0031182005007973

    Article  CAS  PubMed  Google Scholar 

  • Yang YR, Clements ACA, Gray DJ, Atkinson JAM, Williams GM, Barnes TS, McManus DP (2012) Impact of anthropogenic and natural environmental changes on Echinococcus transmission in Ningxia Hui Autonomous Region, the People’s Republic of China. Parasit Vectors 5(1):1–9

    Article  CAS  Google Scholar 

  • Yang SJ, Wu WP, Tian T, Zhao JS, Chen K, Wang QY, Feng Z (2015) Prevalence of cystic echinococcosis in slaughtered sheep as an indicator to assess control progress in Emin County, Xinjiang, China. Korean J Parasitol 53:355–359. https://doi.org/10.3347/kjp.2015.53.3.355

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu SH, Wang H, Wu XH, Ma X, Liu PY, Liu YF, Zhao YM, Morishima Y, Kawanaka M (2008) Cystic and alveolar echinococcosis: an epidemiological survey in a Tibetan population in southeast Qinghai, China. Jpn J Infect Dis 61(3):242–246

    Article  PubMed  Google Scholar 

  • Zhang KF, Wu TJ, Zhao ZY (2014) Analysis of surveillance results of Hydatid disease in Minle County from 2009 to 2010. Fifth cross strait (Qinghai) featured agr. industrialization forum 18, 258–260. (In Chinese)

  • Zhao YP, Gesang DZ, Wan L, Li JD, Qiangba G, Danzeng WM, Basang ZG, Renzhen N, Yin JF, Gongsang QZ, Cai HM, Pang HS, Wang DX, Asan, Zhang QD, Li JH, Chen WJ (2022) Echinococcus spp. and genotypes infecting humans in Tibet Autonomous Region of China: a molecular investigation with near-complete/complete mitochondrial sequences. Parasit Vectors 15(1):1–14

    Article  Google Scholar 

  • Zhao YM (2008) Epidemiological study on Hydatid disease in the eastern section of the Qinghai-Tibet Plateau (Gannan Tibetan Autonomous Prefecture). Gansu Agr Univ 1–98. (In Chinese)

  • Zhong XQ, Wang N, Hu DD, Wang JH, Liu TY, Gu XB, Wang SX, Peng XR, Yang GG (2014) Sequence analysis of cytb gene in Echinococcus granulosus from Western China. Korean J Parasitol 52:205–209

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu GQ, Yan HB, Li L, Ohiolei JA, Wu YT, Li WH, Zhang NZ, Fu BQ, Jia WZ (2020) First report on the phylogenetic relationship, genetic variation of Echinococcus shiquicus isolates in Tibet Autonomous Region, China. Parasit Vectors 13(1):1–8

    Article  Google Scholar 

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Acknowledgements

The authors wish to thank the heads of the slaughter houses found in the study areas, many colleagues, and field workers for their helpful assistance in collecting samples. We want to extend our gratitude to the Gansu Provincial Center for Animal Disease Control and Prevention for facilitating the sample collection process.

Funding

This study was funded by the National Key Research and Development Program (2022YFC2304000; 2021YFE0191600; 2022YFD1302101), Open Project (SKLVEB2020KFKT008) and Cultivation of Achievements (SKLVEB2020CGPY01) of State Key Laboratory of Veterinary Etiological Biology, NBCITS (CARS-37), and Central Public-Interest Scientific Institution Basal Research Fund (Y2022GH13; 1610312020016).

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Authors and Affiliations

  1. State Key Laboratory of Veterinary Etiological Biology/College of Veterinary Medicine, Lanzhou University/National Para-Reference Laboratory for Animal Echinococcosis/Key Laboratory of Veterinary Parasitology of Gansu Province/Lanzhou Veterinary Research Institute, CAAS, Lanzhou, 730046, People’s Republic of China

    Nigus Abebe Shumuye, Li Li, John Asekhaen Ohiolei, Sayed Ajmal Qurishi, Wen-Hui Li, Nian-Zhang Zhang, Yan-Tao Wu, Yao-Dong Wu, Xue-Qi Tian, Wen-Jun Tian, Lin-Sheng Zhang, Bao-Quan Fu, Hong-Bin Yan & Wan-Zhong Jia

  2. Department of Veterinary Clinical Medicine and Epidemiology, College of Veterinary Sciences, Mekelle University, Kalamino Campus, P.O. Box: 2084, Mekelle, Tigray, Ethiopia

    Nigus Abebe Shumuye

  3. Gansu Provincial Center for Animal Disease Control and Prevention, Lanzhou, 730046, People’s Republic of China

    Sheng-Zhi Gao, Yong-Hong Pan & Fang Zhan

  4. Center for Animal Disease Control and Prevention of Maqu County, Gannan Tibetan Autonomous Prefecture, Maqu, 747300, People’s Republic of China

    Fu-Heng Zhang, Ming-Kuan Guo & Wen-Dong Li

  5. Qinghai Academy of Animal Science and Veterinary Medicine, State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, 810016, People’s Republic of China

    Yong Fu

  6. Qinghai Provincial Center for Animal Disease Control and Prevention, Xining, 810001, People’s Republic of China

    Xie-Zhong Wang

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  1. Nigus Abebe Shumuye
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Contributions

NAs and WZJ wrote the main manuscript text, and YDW prepared Figs. 1, 2, 3, 4, 5, 6, 7, and 8. All authors reviewed the manuscript.

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Correspondence to Hong-Bin Yan or Wan-Zhong Jia.

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Supplementary Information

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Supplementary file 1: Table S1.

Previously reported on molecular epidemiology of echinococcosis in the current study areas of China. Legend: TAR: Tibet Autonomous Region; XUAR: Xinjiang Uygur Autonomous Region. (DOC 38 kb)

Supplementary file 2: Table S2.

Source and GenBank accessions for the reference sequences (cox1, nad1, and nad5) used in the phylogenetic analyses. (DOC 45 kb)

Supplementary file 3: Figure S1.

Representative of agarose gel (1.5%) electrophoretogram showing PCR amplified cox1 (a), nad1 (b) and nad5 (c) fragments from sheep isolates of E. granulosus s.s. from Gansu, TAR and XUAR, China. M: Molecular marker 100-2000bp, lane 1: positive control, lane 2- 10/20: test samples, lane N: negative control. (PNG 614 kb)

High resolution image (TIF 1339 kb)

Supplementary file 4: Figure S2.

Echinococcus granulosus s.s. cox1-nad1-nad5 median-joining network according to genotype, Gansu province. Circle sizes are proportional to the haplotype frequencies. Hatch marks represent the number of mutations. The small black dots denote median vectors (i.e. hypothetical/unsampled haplotypes). (PNG 659 kb)

High resolution image (TIF 948 kb)

Supplementary file 5: Figure S3.

Expected and observed mismatch distributions of the cox1-nad1 (a) and cox1-nad1-nad5 (b) isolates of E. granulosus s.s from sheep in Gansu Province, Tibet Autonomous Region and Xinjiang Uygur Autonomous Region. (PNG 626 kb)

High resolution image (TIF 1087 kb)

Supplementary file 6: Table S3.

Results of the analysis of molecular variance to examine genetic differences among E. granulosus s.s. populations. Legend: df, Degrees of freedom. (DOC 44 kb)

Supplementary file 7: Table S4.

Echinococcus granulosus s.s. cox1 haplotypes showing origin, frequency and their corresponding GenBank accession numbers. (DOC 90 kb)

Supplementary file 8: Table S5.

Echinococcus granulosus s.s. nad1 haplotypes showing origin, frequency and their corresponding GenBank accession numbers. (DOC 48 kb)

Supplementary file 9: Table S6.

Genetic polymorphisms and population indices of Echinococcus granulosus s.l. (genotype G6/7) from sheep in Gansu Province, Tibet Autonomous Region and Xinjiang Uygur Autonomous Region. Legend: N, No. of isolates; M, No. of mutations; NP, No. of polymorphic site; PI, Parsimony informative sites; n, No. of haplotypes; Hd, Haplotype diversity; S.D, Standard deviation; π, Nucleotide diversity; D, Tajima’s D; Fs, Fu’s Fs. (DOC 36 kb)

Supplementary file 10: Table S7.

Echinococcus canadensis (G6) haplotypes showing origin, frequency and their corresponding GenBank accession numbers. (DOC 47 kb)

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Shumuye, N.A., Li, L., Ohiolei, J.A. et al. Update on the genetic diversity and population structure of Echinococcus granulosus in Gansu Province, Tibet Autonomous Region, and Xinjiang Uygur Autonomous Region, Western China, inferred from mitochondrial cox1, nad1, and nad5 sequences. Parasitol Res 122, 1107–1126 (2023). https://doi.org/10.1007/s00436-023-07811-9

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