New insights into the genetic variability of Fasciola hepatica (Trematoda) in Algeria and relationships with other geographic regions revealed by mitochondrial DNA
By: M. Chaouadi, F. Scarpa, I. Azzena, P. Cossu, K. Harhoura, M. Aissi, F. Tazerouti, G. Garippa, P. Merella, M. Casu and D. Sanna
References
- Ai, L., Weng, Y.B., Elsheikha, H.M., Zhao, G.H., Alasaad, S., Chen, J.X., Li, J., Li, H.L., Wang, C.R., Chen, M.X., Lin, R.Q., Zhu, X.Q. (2011): Genetic diversity and relatedness of Fasciola spp. isolates from different hosts and geographic regions revealed by analysis of mitochondrial DNA sequences. Vet Parasitol, 181: 329–334. DOI: 10.1016/j.vetpar.2011.03.057
- Aissi, M., Harhoura, K.H., Gaid, S., Hamrioui, B. (2009): Étude préliminaire sur la prévalence de la fasciolose due à Fasciola hepatica dans quelques élevages bovins du nord centre algérien (la Mitidja). [Preliminary study on the prevalence of fasciolosis due to Fasciola hepatica in some cattle farms in northern central Algeria (Mitidja).] Bull Soc Pathol Exot, 102: 177–178
- Alasaad, S., Huang, C.Q., Li, Q.Y., Granados, J.E., Garcia-Romero, C., Perez, J.M., Zhu, X.Q. (2007): Characterization of Fasciola samples from different host species and geographical localities in Spain by sequences of internal transcribed spacers of rDNA. Parasitol Res, 101: 1245–1250. DOI: 10.1007/s00436-007-0628-2
- Amer, S., Elkhatam, A., Zidan, S., Feng, Y., Xiao, L. (2016): Identity of Fasciola spp. in sheep in Egypt. Parasit Vectors, 9: 623. DOI: 10.1186/s13071-016-1898-2
- Amor, N., Farjallah, S., Merella, P., Alagaili, A. N., Mohammed, O.B. (2020): Multilocus approach reveals discordant molecular markers and corridors for gene flow between North African populations of Fasciola hepatica Vet Parasitol, 278: 109035. DOI: 10.1016/j.vet-par.2020.109035
- Amor, N., Halajian, A., Farjallah, S., Merella, P., Said, K., Slimane, B.B. (2011): Molecular characterization of Fasciola spp. from the endemic area of northern Iran based on nuclear ribosomal DNA sequences. Exp Para, 128: 196–204. DOI: 10.1016/j.exppara.2011.03.011
- Ashrafi, K., Valero, M.A., Panova, M., Periago, M.V., Massoud, J., Mas-Coma, S. (2006): Phenotypic analysis of adults of Fasciola hepatica Fasciola gigantica and intermediate forms from the endemic region of Gilan. Iran Parasitol Int, 55: 249–260. DOI: 10.1016/j. parint.2006.06.003
- Bandelt, H.J., Forster, P., Rohl, A. (1999): Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol, 16: 37–48. DOI: 10.1093/oxfordjournals.molbev.a026036
- Beesley, N.J., Williams, D.J., Paterson, S., Hodgkinson, J. (2017): Fasciola hepatica demonstrates high levels of genetic diversity, a lack of population structure and high gene flow: possible implications for drug resistance. Int. J. Parasitol., 47(1): 11–20. DOI: 10.1016/j.ijpara.2016.09.007
- Birky, C.W. (2013): Species detection and identification in sexual organisms using population genetic theory and DNA sequences. PLoS One, 8: e52544. DOI: 10.1371/journal.pone.0052544
- Birky, C.W., Adams, J., Gemmel, M., Perry , J. (2010): Using population genetic theory and DNA sequences for species detection and identification in asexual organisms. PLoS One, 5: e10609. DOI: 10.1371/journal.pone.0010609
- Bozorgomid, A., Rouhani, S., Harandi, M.f., Ichikawa-Seki, M., Raeghi, S. (2019): Genetic diversity and distribution of Fasciola hepatica haplotypes in Iran: Molecular and phylogenetic studies. Vet Parasitol Reg Stud Reports, 19: 100359. DOI: 10.1016/j. vprsr.2019.100359
- Chaouadi, M., Harhoura, K., Aissi, M., Zait, H., Zenia, S., Tazerouti, F. (2019): A post-mortem study of bovine fasciolosis in the Mitidja (north center of Algeria): Prevalence, risk factors, and comparison of diagnostic methods. Trop Anim Health Prod, 51: 2315–2321. DOI: 10.1007/s11250-019-01951-w
- Chougar, L., Mas-Coma, S., Artigas, P., Harhoura, K., Aissi, M., Agramunt, V.H., Bargues, M.D. (2020): Genetically “pure” Fasciola gigantica discovered in Algeria: DNA multimarker characterization, trans-Saharan introduction from a Sahel origin and spreading risk into northwestern Maghreb countries. Transbound Emerg Dis, 67: 2190–2205. DOI: 10.1111/tbed.13572
- Chougar, L., Amor, N., Farjallah, S., Harhoura, K., Aissi, M., Alagaili, A.N., Merella, P. (2019): New insight into genetic variation and haplotype diversity of Fasciola hepatica from Algeria. Parasitol Res, 118: 1179–1192. DOI: 10.1007/s00436-019-06270-5
- Cossu, P., Dedola, G.L., Scarpa , F., Sanna, D., Lai, T., Maltagliati, F., Curini-Galletti, M., Casu, M. (2015): Patterns of spatial genetic variation in Patella ulyssiponensis: Insights from the western Mediterranean marine ecoregion. Hydrobiologia, 755: 39–55. DOI: 10.1007/s10750-015-2216-2
- Cwiklinski, K., Dalton, J.P., Dufresne, P.J., La Course, J., Williams, D.Jl., Hodgkinson, J., Paterson, S. (2015): The Fasciola hepatica genome: gene duplication and polymorphism reveals adaptation to the host environment and the capacity for rapid evolution. Genome Biol, 16: 71. DOI: 10.1186/s13059-015-0632-2
- Cwiklinski, K., Allen, K., Lacourse, J., Williams, D.J., Paterson, S., Hodgkinson, J.E. (2015): Characterization of a novel panel of polymorphic microsatellite loci for the liver fluke, Fasciola hepatica, using a next generation sequencing approach. Infect Genet Evol, 32: 298–304. DOI: 10.1186/s13059-015-0632-2
- Drummond, A.J., Rambaut, A. (2007): BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol, 7: e214. DOI: 10.1186/1471-2148-7-214
- Elliott, T., Muller, A., Brockwell, Y., Murphy, N., Grillo, V., Toet, H.M., Andersone, G., Sangster, N., Spithill, T.W. (2014): Evidence for high genetic diversity of NAD1 and COX1 mitochondrial haplotypes among triclabendazole resistant and susceptible populations and field isolates of Fasciola hepatica (liver fluke) in Australia. Vet Parasitol, 200: 90–96. DOI: 10.1016/j.vetpar.2013.11.019 Ezard, T., Fujisawa, T., Barraclough, T.G. (2009): SPLITS: SPecies’ LImits by Threshold Statistics. R package version 1.0-11, Available at http://R-Forge.R-project.org/projects/splits.
- Farjallah, S., Sanna, D., Amor, N., Ben Mehel, B., Piras, M.C., Merella, P., Casu, M., Curini-Galletti, M., Said, K., Garippa , G. (2009): Genetic characterization of Fasciola hepatica from Tunisia and Algeria based on mitochondrial and nuclear DNA sequences. Parasitol Res, 105: 1617–1621. DOI: 10.1007/s00436-009-1601-z
- Farjallah, S., Slimane, B., Piras, C.M., Amor, N., Garippa , G., Merella, P. (2013): Molecular characterization of Fasciola hepatica from Sardinia based on sequence analysis of genomic and mitochondrial gene markers. Exp Parasitol, 135: 471–478. DOI: 10.1016/j.exppara.2013.08.006
- Fu, Y.X. (1997): Statistical tests of neutrality of mutations against population growth, hitchhiking and backgroud selection. Genetics, 147: 915–925. DOI: 10.1093/genetics/147.2.915
- Gelman, A., Rubin, D.B. (1992): Inference from iterative simulation using multiple sequences. Stat Sci, 7: 457–472. DOI: 10.1214/ss/1177011136
- Hewitt, G. (2000): The genetic legacy of the Quarternary ice ages. Nature, 405: 907–913. DOI: 10.1038/35016000
- Itagaki, T., Kikawa, M., Sakaguchi, K., Shimo, J., Terasaki, K., Shibahara, T., Fukuda, K. (2005): Genetic characterization of parthenogenic Fasciola sp. in Japan on the basis of the sequences of ribosomal and mitochondrial DNA. Parasitol, 131: 679–685. DOI: 10.1017/S0031182005008292
- Itagaki, T., Sakaguchi, K., Terasaki, K., Sasaki, O., Yoshihara, S., Van Dung, T. (2009): Occurrence of spermic diploid and aspermic triploid forms of Fasciola in Vietnam and their molecular characterization based on nuclear and mitochondrial DNA. Parasitol Int, 58: 81–85. DOI: 10.1016/j.parint.2008.11.003
- Kimura, M. (1980): A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol, 16: 111–120. DOI: 10.1007/BF01731581
- Latamna, A.E., Tashiro, M., Zokbi, Z., Chibout, Y., Megrane, S., Mebarka, F., Ichikawa-Seki, M. (2021): Molecular characterization and phylogenetic analysis of Fasciola hepatica from high-plateau and steppe areas in Algeria. Parasitol Int, 80: 102234. DOI: 10.1016/j. parint.2020.102234
- Le, T., De, N., Agatsuma, T., Thi, Nguyen, T., Nguyen, Q., Mcmanus, D., Blair, D. (2008): Human fascioliasis and the presence of hybrid/introgressed forms of Fasciola hepatica and Fasciola gigantica in Vietnam. Int J Parasitol, 38: 725–730. DOI: 10.1016/j. ijpara.2007.10.003
- Le, T.H., Blair, D., Agatsuma, T., Humair, P.F., Campbel, N.J., Iwagami, M., Littlewood, D.T., Peacock, B., Johnston, D.A., Bartley, J., Rolinson, D., Herniou, E.A., Zarlenga, D.S., Mcmanus, D.P. (2000): Phylogenies inferred from mitochondrial gene orders-a cautionary tale from the parasitic flatworms. Mol Biol Evol, 17: 1123–1125. DOI: 10.1093/oxfordjournals.molbev.a026393
- Librado, P., Rozas, J. (2009): DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452. DOI: 10.1093/bioinformatics/btp187
- Lotfy, W.M., Brant, S.V., Dejong, R.J., Le, T.H., Demiaszkiewicz, A., Rajapa kse, R.P., Perera, V.B., Laursen, J.R., Loker, E.S. (2008): Evolutionary origins, diversification, and biogeography of Liver Flukes. Am J Trop Med Hyg, 79: 248–255. DOI: 10.4269/ajtmh.2008.79.248
- Luton, K., Walker, D., Blair, D. (1992): Comparisons of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Mol Biochem Parasitol, 56: 323–327. DOI: 10.1016/0166-6851(92)90181-I
- Martinez-Valadares, M., Rojo-Vazquez, F.A. (2014): Intraspecific mitochondrial DNA variation of Fasciola hepatica eggs from sheep with different level of anthelmintic resistance. Parasitol Res, 113: 2733–2741. DOI: 10.1007/s00436-014-3934-5
- Mas-Coma, S., Bargues, M.D., Valero, M.A. (2005): Fascioliasis and other plant-borne trematode zoonoses. Int J Parasitol, 35: 1255–1278. DOI: 10.1016/j.ijpara.2005.07.010
- Mas-Coma, S., Valero, M.A., Bargues, M.D. (2009): Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol, 69: 41–146. DOI: 10.1016/S0065-308X(09)69002-3
- Massot, M., Senouci-Hor, K. (1983): Étude de la répartition de Lymnaea truncatola dans le nord-ouest algérien et de sa réceptivité a Fasciola hepatica. [Study of the distribution of Lymnaea truncatola in northwestern Algeria and its receptivity to Fasciola hepatica.] Ann. Parasitol. Hum. Comp., 58: 19–25. DOI: 10.1051/parasite/1983581019
- Mehmood, K., Hui, Z., Sabir, A.J., Abas, R.Z., Ijaz, M., Durani, A.Z., Saleem, M.H., Rehman, M.U., Iqbal, M.K., Wang, Y., Ahmad, H.I., Abas, T., Hussain, R., Ghori, M.T., Ali, S., Khan, A.U., Li, J. (2017): A review on epidemiology, global prevalence and economical losses of fasciolosis in ruminants. Microb Pathog, 109: 253–262. DOI: 10.1016/j.micpath.2017.06.006.
- Mekroud, A., Benakhla, A., Vignoles, P., Rondelaud, D., Dreyfus, J. (2004): Preliminary studies on the prevalences of natural fasciolosis in cattle, sheep, and the host snail (Galba truncatula) in north-eastern Algeria. Parasitol Res, 92: 502–505. DOI: 10.1007/s00436-004-1072-1
- Miler, M.A., Pfeifer, W., Schwartz, T. (2010): Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the 2010 gateway computing environments workshop (GCE), New Orleans, LA, USA, 14 November 2010
- Mucheka, V.T., Lamb, J.M., Pfukenyi, D.M., Mukaratirwa, S. (2015): DNA sequence analyses reveal co-occurrence of novel genotypes of Fasciola gigantica (Fasciolidae, Echinostomida, Trematoda) with F. hepatica in South Africa and Zimbabwe. Vet Parasitol, 214: 144–151. DOI: 10.1016/j.vetpar.2015.09.024
- Nolan, M.J., Crib, T.H. (2005): The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Adv Parasitol, 60: 102–163. DOI: 10.1016/S0065-308X(05)60002-4
- Ouchene-Khelifi, N.A., Ouchene, N., Dahmani, H., Dahmani, A., Said, M., Douifi, M. (2018): Fasciolosis due to Fasciola hepatica in ruminants in abattoirs and its economic impact in two regions in Algeria. Trop Biomed, 35: 181–187
- Paradis, E., Claude, J., Strimer, K. (2004): APE: Analyses of phylogenetics and evolution in R language. Bioinformatics, 20: 289–290. DOI: 10.1093/bioinformatics/btg412
- Peakal, R., Smouse, P.E. (2012): GenAlEx 6.5: Genetic analysis in excel. Population genetic software for teaching and research - an update. Bioinformatics, 28: 2537–2539. DOI: 10.1093/bioinformatics/bts460
- Periago, M., Valero, M., Sayed, M., Ashrafi, K., Wakeel, A., Mohamed, M., Desquesnes, M., Curtale, F., Mas-Coma, S. (2008): First phyenotypic description of Fasciola hepatica/Fasciola gigantica intermediate forms from human endemic area of the Nile Delta Egypt. Infect Genet Evol, 8: 51–58. DOI: 10.1016/j.meegid.2007.10.001
- Periago, M.V., Valero, M.A., Panova, M., Mas-Coma, S. (2006): Phenotypic comparison of allopatric populations of Fasciola hepatica and Fasciola gigantica from European and African bovines using a computer image analysis system (CIAS). Parasitol Res, 99: 368–378. DOI: 10.1007/s00436-006-0174-3
- Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin, W.D., Vogler, A.P. (2006): Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol, 55: 595–609. DOI: 10.1080/10635150600852011
- Posada, D. (2008): jModelTest: Phylogenetic Model Averaging. Mol Biol Evol, 25, 1253–1256. DOI: 10.1093/molbev/msn083
- Puillandre, N., Brouillet, S., Achaz, G. (2020): ASAP: assemble species by automatic partitioning. Mol Ecol Resour, 21: 609–620. DOI: 10.1111/1755-0998.13281
- Robinson, M.W., Dalton, J.P. (2009): Zoonotic helminth infections with particular emphasis on fasciolosis and other trematodiases. Philos Trans R Soc Lond B Biol Sci, 364: 2763–2776. DOI: 10.1098/rstb.2009.0089
- Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A., Huelsenbeck, J.P. (2012): MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol, 61: 539–542. DOI: 10.1093/sysbio/sys029
- Saitou, N., Nei, M. (1987): The neighbor-joining method: A new method for reconstruction of phylogenetic trees. Mol Biol Evol, 4: 406–425
- Santos, R. (2012): Genetic characterization of Portuguese Fasciola hepatica isolates. Master’s degree in molecular, Genetics and Biomedicine. Universidade Nova de Lisboa, Portugal, pp. 80
- Scarpa , F., Sanna, D., Cossu, P., Lai, T., Casu, M., Curini-Galletti, M. (2019a): How to achieve internal fertilization without a vagina: the study case of the genus Archilina Ax, 1959 (Platyhelminthes, Proseriata) from Canary Islands. Mar Biodivers, 49: 2057–2073. DOI: 10.1007/s12526-018-0890-9
- Scarpa , F., Cossu, P., Sanna, D., Lai, T., Casu, M., Curini-Galletti, M. (2019b): New insights on the genus Otoplana Du Plessis, 1889 (Platyhelminthes: Proseriata), with description of two new species from the Canary Islands. Mar Biodivers, 49: 2075–2087. DOI: 10.1007%2Fs12526-017-0785-1
- Scarpa , F., Sanna, D., Cossu, P., Lai, T., Curini-Galletti, M., Casu, M. (2018): A molecular approach to the reconstruction of the pre-Lessepsian fauna of the Isthmus of Suez: the case of the interstitial flatworm Monocelis lineata sensu lato (Platyhelminthes: Proseriata). J Exp Mar Biol Ecol, 502: 174–181. DOI: 10.1016/j. jembe.2017.08.011
- Semyenova, S.K., Morozova, E.V., Chrisanfova, G.G., Gorokhov, V.V., Arkhipov, I.A., Moskvin, A.S., Movsessyan, S.O., Ryskov, A.P. (2006): Genetic differentiation in eastern European and western Asian populations of the liver fluke, Fasciola hepatica, as revealed by mitochondrial nad1 and cox1 genes. J Parasitol, 92: 525–530. DOI: 10.1645/GE-673R.1
- Shoriki, T., Ichikawa-Seki, M., Suganuma, K., Naito, I., Hayashi, K., Nakao, M., Aita, J., Mohanta, U.K., Inoue, N., Murakami, K., Itagaki, T. (2016): Novel methods for the molecular discrimination of Fasciola spp. on the basis of nuclear protein-coding genes. Parasitol Int, 65: 180–183. DOI: 10.1016/j.parint.2015.12.002
- Sievers, F., Higgins, D.G. (2014): Clustal Omega. Curr Protoc Bioinformatics, 48: 1.25.1–1.25.33. DOI: 10.1002/0471250953. bi0313s48
- Simsek, S., Utuk, A.E., Balkaya, I. (2011): Molecular differentiation of Turkey cattle isolates of Fasciola hepatica and Fasciola gigantica Helmintologia, 48(1): 3–7. DOI: 10.2478/s11687-011-0001-y
- Soriano A.R., Ramos-Onsins S.E., Rozas J., Calafell F., Navarro A. (2008): Statistical power analysis of neutrality tests under demographic expansions, contractions and bottlenecks with recombination. Genetics, 179: 555–567. DOI: 10.1534/genetics.107.083006 Tajima, F. (1989): Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123: 585–589
- Thang, T.N., Vázquez-Prieto, S., Vilas, R., Paniagua, E., Ubeira, F.M., Ichikawa-Seki, M. (2020): Genetic diversity of Fasciola hepatica in Spain and Peru. Parasitol Int, 76: 102100. DOI: 10.1016/j. parint.2020.102100
- Valero, M.A., Bargues, M.D., Calderon, L., Artigas, P., Mas-Coma, S. (2018): First phenotypic and genotypic description of Fasciola hepatica infecting highland cattle in the state of Mexico. Infect Genet Evol, 64: 231–240. DOI: 10.1016/j.meegid.2018.06.032
- Walker, S.M., Prodohl, P.A., Fletcher, H.L., Hanna, R.E., Kantzoura, V., Hoey, E.M., Trudgett, A. (2007): Evidence for multiple mitochondrial lineages of Fasciola hepatica (liver fluke) within infrapopulations from cattle and sheep. Parasitol Res, 101: 117–125. DOI: 10.1007/s00436-006-0440-4
Language: English
Page range: 152 - 164
Submitted on: Jan 19, 2022
Accepted on: Jul 14, 2022
Published on: Sep 3, 2022
Published by: Slovak Academy of Sciences, Institute of Parasitology
In partnership with: Paradigm Publishing Services
Publication frequency: Volume open
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© 2022 M. Chaouadi, F. Scarpa, I. Azzena, P. Cossu, K. Harhoura, M. Aissi, F. Tazerouti, G. Garippa, P. Merella, M. Casu, D. Sanna, published by Slovak Academy of Sciences, Institute of Parasitology
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