Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-15T23:26:39.941Z Has data issue: false hasContentIssue false
  • English
  • Français

Fasciola hepatica from naturally infected sheep and cattle in Great Britain are diploid

Published online by Cambridge University Press:  20 May 2015

N. J. BEESLEY ,
K. CWIKLINSKI ,
D. J. L. WILLIAMS  and
J. HODGKINSON
N. J. BEESLEY*
Affiliation:
Veterinary Parasitology, Institute of Infection and Global Health, University of Liverpool, Liverpool, L3 5RF, UK
K. CWIKLINSKI
Affiliation:
Veterinary Parasitology, Institute of Infection and Global Health, University of Liverpool, Liverpool, L3 5RF, UK
D. J. L. WILLIAMS
Affiliation:
Veterinary Parasitology, Institute of Infection and Global Health, University of Liverpool, Liverpool, L3 5RF, UK
J. HODGKINSON
Affiliation:
Veterinary Parasitology, Institute of Infection and Global Health, University of Liverpool, Liverpool, L3 5RF, UK
*
* Corresponding author. Veterinary Parasitology, Department of Infection Biology, Institute of Infection and Global Health, University of Liverpool, Liverpool, L3 5RF, UK. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Diploid (2n = 2x = 20) and triploid (2n = 3x = 30) Fasciola hepatica have been reported in the UK, and in Asia diploid, triploid and mixoploid (2x/3x) Fasciola spp. exist but there is little information to indicate how common triploidy is, particularly in UK fluke. Here the ploidy of 565 adult F. hepatica from 66 naturally infected British sheep and 150 adult F. hepatica from 35 naturally infected British cattle was determined. All 715 of these parasites were diploid, based on observation of 10 bivalent chromosomes and sperm (n = 335) or, since triploids are aspermic, sperm alone (n = 380). This constitutes the first extensive analysis of the ploidy of F. hepatica field isolates from Great Britain and shows that most F. hepatica isolated from cattle and sheep are diploid and have the capacity to sexually reproduce. These data suggest that triploidy, and by extension parthenogenesis, is rare or non-existent in wild British F. hepatica populations. Given that F. hepatica is the only species of Fasciola present in Britain our results indicate that the parasite is predominantly diploid in areas where F. hepatica exists in isolation and suggests that triploidy may only originate in natural populations where co-infection of F. hepatica and its sister species Fasciola gigantica commonly occurs.

Keywords

Fasciola hepaticaploidypopulation geneticsdiploidtriploid
Type
Research Article
Information
Parasitology , Volume 142 , Issue 9 , August 2015 , pp. 1196 - 1201
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Agatsuma, T., Terasaki, K., Yang, L. and Blair, D. (1994). Genetic variation in the triploids of Japanese Fasciola species, and relationships with other species in the genus. Journal of Helminthology 68, 181–186.Google Scholar
Agatsuma, T., Arakawa, Y., Iwagami, M., Honzako, Y., Cahyaningsih, U., Kang, S-Y. and Hong, S-J. (2000). Molecular evidence of natural hybridization between Fasciola hepatica and F. gigantica . Parasitology International 49, 231–238.Google Scholar
Amer, S., Dar, Y., Ichikawa, M., Fukuda, Y., Tada, C., Itagaki, T. and Nakai, Y. (2011). Identification of Fasciola species isolated from Egypt based on sequence analysis of genomic (ITS1 and ITS2) and mitochondrial (NDI and COI) gene markers. Parasitology International 60, 5–12.CrossRefGoogle ScholarPubMed
Bai, C., Liu, H., Liu, Y., Wu, X., Cheng, L., Bou, S. and Li, G-P. (2011). Diploid oocyte formation and tetraploid embryo development induced by cytochalasin B in bovine. Cellular Reprogramming 13, 37–45.Google Scholar
Cwiklinski, K., Dalton, J. P., Dufresne, P. J., La Course, J., Williams, D. J. L., Hodgkinson, J. and Paterson, S. (2015). The Fasciola hepatica genome: gene duplication and polymorphism reveals adaptation to the host environment and the capacity for rapid evolution. Genome Biology 16, 71.Google Scholar
Dasgupta, S. (1962). Induction of triploidy by hydrostatic pressure in the leopard frog, Rana pipiens . Journal of Experimental Zoology 151, 105–121.Google Scholar
Dufresne, F., Stift, M., Vergilino, R. and Mable, B. K. (2014). Recent progress and challenges in population genetics of polyploidy organisms: an overview of current state-of-the art molecular and statistical tools. Molecular Ecology 23, 40–69.Google Scholar
Fletcher, H. L., Hoey, E. M., Orr, N., Trudgett, A., Fairweather, I. and Robinson, M. W. (2004). The occurrence and significance of triploidy in the liver fluke, Fasciola hepatica . Parasitology 128, 69–72.Google Scholar
Gresson, R. A. R. (1965). Spermatogenesis in the hermaphroditic Digenea (Trematoda). Parasitology 55, 117–125.CrossRefGoogle Scholar
Hanley, J. A. and Lippman-Hand, A. (1983). If nothing is wrong, is everything all right? Journal of the American Medical Association 249, 1743–1745.Google Scholar
Hanna, R. E. B., Edgar, H., Moffett, D., McConnell, S., Fairweather, I., Brennan, G. P., Trudgett, A., Hoey, E. M., Cromie, L., Taylor, S. M. and Daniel, R. (2008). Fasciola hepatica: histology of the testis in egg-producing adults of several laboratory-maintained isolates of flukes grown to maturity in cattle and sheep and in flukes from naturally infected hosts. Veterinary Parasitology 157, 222–234.Google Scholar
Hillyer, G. V. and Apt, W. (1997). Food-borne trematode infections in the Americas. Parasitology Today 13, 87–88.CrossRefGoogle Scholar
Hodgkinson, J., Cwiklinski, K., Beesley, N. J., Paterson, S. and Williams, D. J. (2013). Identification of putative markers of triclabendazole resistance by a genome-wide analysis of genetically recombinant Fasciola hepatica . Parasitology 140, 1523–1533.Google Scholar
Hopkins, D. R. (1992). Homing in on helminths. American Journal of Tropical Medicine and Hygiene 46, 626–634.Google Scholar
Itagaki, T. and 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. International Journal for Parasitology 28, 777–781.Google Scholar
Itagaki, T., Tsutsumi, K., Ito, K. and Tsutsumi, Y. (1998). Taxanomic status of the Japanese triploid forms of Fasciola: comparison of mitochondrial ND1 and COI sequences with F. hepatica and F. gigantica . Journal of Parasitology 84, 445–448.CrossRefGoogle Scholar
Itagaki, T., Kikawa, M., Sakaguchi, K., Shmo, J., Terasaki, K., Shibahara, T. and Fukuda, K. (2005a). Genetic characterization of parthenogenic Fasciola sp. in Japan on the basis of the sequences of ribosomal and mitochondrial DNA. Parasitology 131, 679–685.Google Scholar
Itagaki, T., Kikawa, M., Terasaki, K., Shibahara, T. and Fukuda, K. (2005b). Molecular characterization of parthenogenic Fasciola sp. in Korea on the basis of DNA sequences of ribosomal ITS1 and mitochondrial NDI gene. Journal of Veterinary Medical Science 67, 1115–1118.Google Scholar
Itagaki, T., Sakaguchi, K., Terasaki, K., Sasaki, O., Yoshihara, S. and 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. Parasitology International 58, 81–85.Google Scholar
Itagaki, T., Ichinomiya, M., Fukuda, K., Fusyuku, S. and Carmona, C. (2011). Hybridization experiments indicate incomplete reproductive isolating mechanism between Fasciola hepatica and Fasciola gigantica . Parasitology 138, 1278–1284.CrossRefGoogle ScholarPubMed
John, B. (1953). The behaviour of the nucleus during spermatogenesis in Fasciola hepatica . Quarterly Journal of Microscopical Science 94, 41–55.Google Scholar
Madl, J. E. and Herman, R. K. (1979). Polyploids and sex determination in Caenorhabditis elegans . Genetics 93, 393–402.Google Scholar
McGonigle, L., Mousley, A., Marks, N. J., Brennan, G. P., Dalton, J. P., Spithill, T. W., Day, T. A. and Maule, A. G. (2008). The silencing of cysteine proteases in Fasciola hepatica newly excysted juveniles using RNA interference reduces gut penetration. International Journal for Parasitology 38, 149–155.Google Scholar
Mohanta, U. K., Ichikawa-Seki, M. I., Shoriki, T., Katakura, K. and Itagaki, T. (2014). Characteristics and molecular phylogeny of Fasciola flukes from Bangladesh, determined based on spermatogenesis and nuclear and mitochondrial DNA analyses. Parasitology Research 113, 2493–2501.Google Scholar
Peng, M., Ichinomiya, M., Ohtori, M., Ichikawa, M., Shibahara, T. and Itagaki, T. (2009). Molecular characterization of Fasciola hepatica, Fasciola gigantica, and aspermic Fasciola sp. in China based on nuclear and mitochondrial DNA. Parasitology Research 105, 809–815.Google Scholar
Ramsey, J. and Schemske, D. W. (1998). Pathways, mechanisms, and rates of polyploidy formation in flowering plants. Annual Review of Ecology and Systematics 29, 467–501.Google Scholar
Reblánová, M., Špakulová, M., Orosová, M., Králová-Hromadová, I., Bazsalovicsová, E. and 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). Parasitology Research 109, 1021–1028.CrossRefGoogle ScholarPubMed
Rhee, J. K., Eun, G. S. and Lee, S. B. (1987). Karyotype of Fasciola sp. obtained from Korean cattle. The Korean Journal of Parasitology 25, 37–44.Google Scholar
Rim, H-J., Farag, H. F., Sornmani, S. and Cross, J. H. (1994). Food-borne trematodes: ignored or emerging? Parasitology Today 10, 207–209.CrossRefGoogle Scholar
Sanderson, A. R. (1953). Maturation and probable gynogenesis in the liver fluke, Fasciola hepatica L. Nature 172, 110–112.Google Scholar
Sanderson, A. R. (1959). VI.—Maturation and Fertilization in Two Digenetic Trematodes, Haplometra cylindracea (Zeder 1800) and Fasciola hepatica (L.). Proceedings of the Royal Society of Edinburgh. Section B. Biology 67, 83–98.Google Scholar
Stitt, A. W. and Fairweather, I. (1990). Spermatogenesis and the fine structure of the mature spermatozoon of the liver fluke, Fasciola hepatica (Trematoda: Digenea). Parastiology 101, 395–407.Google Scholar
Terasaki, K., Moriyama-Gonda, N. and Noda, Y. (1998). Abnormal spermatogenesis in the common liver fluke (Fasciola sp.) from Japan and Korea. Journal of Veterinary Medical Science 60, 1305–1309.Google Scholar
Terasaki, K., Noda, Y., Shibahara, T. and Itagaki, T. (2000). Morphological comparisons and hypotheses on the origin of polyploids in parthenogenetic Fasciola sp. Journal of Parasitology 86, 724–729.Google Scholar
World Health Organisation (2015). Neglected Tropical Diseases. [Online] Available from: http://www.who.int/neglected_diseases/diseases/en/ [Accessed 3rd February 2015].Google Scholar