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Phylogenetic data suggest the reclassification of Fasciola jacksoni (Digenea: Fasciolidae) as Fascioloides jacksoni comb. nov.

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Abstract

Fasciola jacksoni (Cobbold, 1869) is a highly prevalent (18–62 %) species colonizing the liver (less frequently the lungs, kidneys, pericardia, and intestines) of Elephas maximus indicus and Elephas maximus maximus in the Indomalayan region, causing cirrhosis, hemorrhages, and connective tissue proliferation. The phylogenetic relationships of Fasciola jacksoni in relation to representative species of the superfamily Echinostomatoidea was assessed using four independent DNA regions. The analysis involved conserved (28S rDNA) and highly variable (ITS1, ITS2, and ND1) loci utilizing both mitochondrial (ND1) and nuclear (28S rDNA, ITS1, and ITS2) DNA. Although the analyses confirmed the monophyletic origin of the Fasciolidae family, all four analyzed regions suggested high similarity of Fasciola jacksoni to Fascioloides magna, member of a hitherto monotypic genus, parasitizing a variety of wild and domestic ruminants through the Holarctic. Supporting evidence stems also from the morphological similarities, host spectrum overlaps, and similarities in disease onset and progression. Fasciola jacksoni was reclassified to its genus in the nineteenth century by Cobbold based on the shared possession of dendriform system of gastric canals. However, Fascioloides magna (discovered later) shares this feature as well. Conversely, Fascioloides magna and Fasciola hepatica possess long median intestinal branches, whereas relatively shorter median intestinal branches are characteristic for Fasciola hepatica and Fasciola gigantica only. Both, Fascioloides magna and Fasciola hepatica, are also similar in their possession of small, but distinctive cephalic cone, while the larger one is typical for Fasciola hepatica and Fasciola gigantica. Reflecting the combined data, reclassification of Fasciola jacksoni as Fascioloides jacksoni comb. nov. is suggested.

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References

  • Alahakoon J (1994) Presence of liver fluke Fasciola jacksoni in a Sri Lankan elephant. Gajah 12:46–47

    Google Scholar 

  • Ashrafi K, Valero MA, Panova M, 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

    Article  PubMed  CAS  Google Scholar 

  • Bhalerao GD (1933) The trematode parasites of the Indian elephant, Elephas indicus. Indian J Vet Sci Anim Husb 3:103–155

    Google Scholar 

  • Bhalerao GD (1935) Helminth parasites of the Indian elephant from the Andamans and Burma. Indian J Vet Sci Anim Husb 5:35–48

    Google Scholar 

  • Caple IW, Jainudeen MR, Buick TD, Song CY (1978) Some clinico-pathologic findings in elephants (Elephas maximus) infected with Fasciola jacksoni. J Wildl Dis 14:110–115

    PubMed  CAS  Google Scholar 

  • Chakraborthy A, Chaudhury B (1992) Pathology of Fasciola jacksoni infestation in elephants. Ind J Vet Pathol 162:98–101

    Google Scholar 

  • Cobbold TS (1882) VII. The parasites of elephants. Trans Linn Soc Lond, 2nd series: Zoology 2:223–258

    Article  Google Scholar 

  • Dinnik JA, Dinnik NN (1961) On the morphology and life history of Fasciola nyanzae Leiper, 1910 from the hippopotamus. J Helminthol 35:53–62

    Article  Google Scholar 

  • Evans GH (1910) Elephants and their diseases: a treatise on elephants. Government Press, Rangoon

    Google Scholar 

  • Farias IP, Ortí G, Sampaio I, Schneider H, Meyer A (2001) The cytochrome b gene as a phylogenetic marker: the limits of resolution for analyzing relationships among cichlid fishes. J Mol Evol 53:89–103

    PubMed  CAS  Google Scholar 

  • Feng DF, Doolitle RF (1987) Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J Mol Evol 25:351–360

    Google Scholar 

  • Fletcher HL, Hoey EM, Orr EM, Trudgett A, Fairweather I, Robinson MV (2004) The occurrence and significance of triploidy in the liver fluke, Fasciola hepatica. Parasitology 128:69–72

    Article  PubMed  CAS  Google Scholar 

  • Fowler ME, Mikota SK (eds) (2006) Elephant biology, medicine, and surgery. Blackwell Publishing, Ames

    Google Scholar 

  • Ichikawa M, Itagaki T (2010) Discrimination of the ITS1 types of Fasciola spp. based on a PCR-RFLP method. Parasitol Res 106:757–761

    Article  PubMed  Google Scholar 

  • Islam S (1997) Studies on some aspects of fascioliasis in Asian elephants (Elephas maximus). J Vet Parasitol 11:109

    Google Scholar 

  • Islam S, Mukit A, Das M (1999) Pathology of concurrent Gastrodiscus secundus and Pseudodiscus collinsi infection in two captive Asian elephants (Elephas maximus). J Vet Parasitol 13:151–152

    Google Scholar 

  • Itagaki T, Tsutsumi K (1998) Triploid form of Fasciola in Japan: genetic relationships between Fasciola hepatica and Fasciola gigantica determined by ITS-2 sequence of nuclear rDNA. Int J Parasitol 28:777–781

    Article  PubMed  CAS  Google Scholar 

  • Itagaki T, Tsutsumi K, Ito K, Tsutsumi Y (1998) Taxonomic status of the Japanese triploid forms of Fasciola: comparison of mitochondrial ND1 and COI sequences with F. hepatica and F. gigantica. J Parasitol 84:445–448

    Article  PubMed  CAS  Google Scholar 

  • Jones A (2005) Keys to the Trematoda. CABI Publishing and the Natural History Museum, Cambridge

    Google Scholar 

  • Karki KB (2005) Incidence of gastrointestinal helminthes in captive elephants in wildlife reserves of Nepal. Available at http://www.articlesbase.com/health-articles/incidence-of-gastrointestinal-helminthes-in-captive-elephants-in-wildlife-reserves-of-nepal-335689.html. Accessed 18 July 2012

  • Li GQ, Jin JS, Wang PY (1988) A study on the chromosomes of Fasciola hepatica. Chin J Veter Sci Technol 6:11–16

    Google Scholar 

  • Lotfy WM, Brant SV, DeJong RJ, Le TH, Demiaszkiewicz A, Rajapakse RPVJ, Perera VBVP, Laursen JR, Loker ES (2008) Evolutionary origins, diversification, and biogeography of liver flukes (Digenea, Fasciolidae). AmJTrop Med Hyg 79:248–255

    CAS  Google Scholar 

  • Mas-Coma S, Valero MA, Bargues MD (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

    Article  PubMed  Google Scholar 

  • Maxie MG (ed) (2007) Jubb, Kennedy and Palmer’s pathology of domestic animals, 5th edn. Saunders, Philadelphia

    Google Scholar 

  • Odhner T (1926) Protofasciola n. g. ein Prototypus des grossen Leberegels. Arkiv Zool 18(20):1–7

    Google Scholar 

  • Peng M, Ichinomiya M, Ohtori M, Ichikawa M, Shibahara T, Itagaki T (2009) Molecular characterization of Fasciola hepatica, Fasciola gigantica, and aspermic Fasciola sp. in China based on nuclear and mitochondrial DNA. Parasitol Res 105:809–815

    Article  PubMed  Google Scholar 

  • Perera BVP, Rajapakse RPVJ (2009) Mortality and morbidity of wild elephants (Elephas maximus maximus) of Sri Lanka, as a result of liver flukes (Fasciola jacksoni) infestation. In: Wibbelt G, Kretschmar P, Hofer H, Seet S (eds) Proceedings of the International Conference on Diseases of Zoo and Wild Animals, Beekse Bergen, The Netherlands, 20–24 May 2009, pp 191

  • Periago MV, Valero MA, 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

    Article  PubMed  CAS  Google Scholar 

  • Periago MV, Valero MA, El Sayed M, Ashrafi K, El Wakeel A, Mohamed MY, Desquesnes M, Curtale F, Mas-Coma S (2008) First phenotypic description of Fasciola hepatica/Fasciola gigantica intermediate forms from the human endemic area of the Nile Delta, Egypt. Infect Genet Evol 8:51–58

    Article  PubMed  CAS  Google Scholar 

  • Phillimore AB, Price TD (2008) Density-dependent cladogenesis in birds. PLoS Biol 6:e71

    Article  PubMed  Google Scholar 

  • Reblánová M, Špakulová M, Orosová M, Bazsalovicsová E, Rajský D (2010) A description of karyotype of giant liver fluke Fascioloides magna (Trematoda, Platyhelminthes) and a review of Fasciolidae cytogenetics. Helminthologia 47:69–75

    Article  Google Scholar 

  • Reblánová M, Špakulová M, Orosová M, Králová-Hromadová I, Bazsalovicsová E, Rajský D (2011) A comparative study of karyotypes and chromosomal location of rDNA genes in important liver flukes Fasciola hepatica and Fascioloides magna (Trematoda: Fasciolidae). Parasitol Res 109:1021–1028

    Article  PubMed  Google Scholar 

  • Revell LJ, Harmon LJ, Glor RE (2005) Underparametrized model of sequence evolution leads to bias in the estimation of diversification rates from molecular phylogenies. Syst Biol 54:973–983

    Article  PubMed  Google Scholar 

  • Romanenko LN, Pleshanova NM (1975) [Chromosome sets of Fasciola hepatica and Fasciola gigantica]. Trudy Vsesoyuznogo Instituta Geĺmintologii im Kl Skryabina Teoreticheskie Problemy Veterinarnoi Geĺmintologii 22:137–141 (in Russian)

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Salzert W (1982) Elephants. In: Klös HG, Lang EM (eds) Handbook of zoo medicine: diseases and treatment of wild animals in zoos, game parks, circuses and private collections. Van Nostrand Reinhold Company, New York, pp 152–186

    Google Scholar 

  • Sanderson AR (1953) Maturation and probable gynogenesis in the liver fluke, Fasciola hepatica L. Nature 172:110–112

    Article  PubMed  CAS  Google Scholar 

  • Schmidt M (1978) Elephants and perissodactylids (Proboscidae and Perissodactyla): elephants. In: Fowler ME (ed) Zoo and wild animal medicine, 1st edn. WB Saunders Company, Orlando, pp 709–752

    Google Scholar 

  • Sinclair KB (1962) Observations on the clinical pathology of ovine fascioliasis. Brit vet J 118:37–53

    Google Scholar 

  • Singh KP, Srivastava VK, Prasad A, Pandey AP (1994) Pathology due to Fasciola jacksoni in Indian elephants (Elephas indicus). Indian J Anim Sci 648:802–804

    Google Scholar 

  • Sinitsin DF (1934) Studien über die Phylogenie der Trematoden. VI. The life histories of some American liver flukes. Z Parasitenk 6:170–191

    Google Scholar 

  • Smith JM, Smith NH (1996) Synonymous nucleotide divergence: what is “saturation”? Genetics 142:1033–1036

    PubMed  CAS  Google Scholar 

  • Soulsby EJL (1982) Helminths, arthropods and protozoa of domesticated animals, 7th edn. Bailliere Tyndall, London

    Google Scholar 

  • Špakulová M, Králová I (1991) Chromosomes of Fasciola hepatica (Digenea: Fasciolidae) from western Bohemia (ČSFR). Helminthologia 28:197–200

    Google Scholar 

  • Van Den Berghe L (1943) Enquȇte parasitologique. II. Helminthes parasites. Fasc. 2, Mission (van den Berghe). Exploration du Parc national Albert (1936). Hayez, Bruxelles, pp 3–30

  • Ward H (1917) On the structure and classification of North American parasitic worms. J Parasitol 4:1–12

    Article  Google Scholar 

  • World Health Organization (2007) Report of the WHO Informal Meeting on use of triclabendazole in fascioliasis control. WHO Headquarters, Geneva, Switzerland, 17–18 October 2006. Available at http://www.who.int/neglected_diseases/preventive_chemotherapy/WHO_CDS_NTD_PCT_2007.1.pdf. Accessed 7 August 2012

  • Yamaguti S (1971) Synopsis of digenetic trematodes of vertebrates, vol 1 and 2. Keigaku Publishing Co., Tokyo

    Google Scholar 

Download references

Acknowledgments

The study was supported by the UNCE Project 204015 and by the PRVOUK Project P31/2012 from the Charles University in Prague, by the Czech Science Foundation Project P301/12/1686, and by the Internal Grant Agency of the Ministry of Health of the Czech Republic Project NT13663-3/2012.

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  1. Third Faculty of Medicine, Charles University in Prague, Ruská 87, CZ - 100 00, Prague, Czech Republic

    Petr Heneberg

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Heneberg, P. Phylogenetic data suggest the reclassification of Fasciola jacksoni (Digenea: Fasciolidae) as Fascioloides jacksoni comb. nov.. Parasitol Res 112, 1679–1689 (2013). https://doi.org/10.1007/s00436-013-3326-2

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