Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-10T07:38:46.407Z Has data issue: false hasContentIssue false
  • English
  • Français

Hybridization experiments indicate incomplete reproductive isolating mechanism between Fasciola hepatica and Fasciola gigantica

Published online by Cambridge University Press:  18 July 2011

T. ITAGAKI ,
M. ICHINOMIYA ,
K. FUKUDA ,
S. FUSYUKU  and
C. CARMONA
T. ITAGAKI*
Affiliation:
Laboratory of Veterinary Parasitology, Faculty of Agriculture, Iwate University, Ueda 3-18-8, Morioka 020-8550, Japan
M. ICHINOMIYA
Affiliation:
Laboratory of Veterinary Parasitology, Faculty of Agriculture, Iwate University, Ueda 3-18-8, Morioka 020-8550, Japan
K. FUKUDA
Affiliation:
Center for Laboratory Animal Science, National Defense Medical College, Tokorozawa 359-8513, Japan
S. FUSYUKU
Affiliation:
Center for Laboratory Animal Science, National Defense Medical College, Tokorozawa 359-8513, Japan
C. CARMONA
Affiliation:
Laboratory of Parasitology, Institute of Hygiene, Montevideo, Uruguay
*
*Corresponding author: Laboratory of Veterinary Parasitology, Faculty of Agriculture, Iwate University, Ueda 3-18-8, Morioka 020-8550, Japan. Tel: and Fax: +81 19 621 6219. E-mail: itagaki@iwate-u.ac.jp
Get access Rights & Permissions [Opens in a new window]

Summary

Experiments on hybridization between Fasciola hepatica and Fasciola gigantica were carried out to clarify whether a reproductive isolating mechanism appears between the two Fasciola species. Molecular evidence for hybridization was based on the DNA sequence of the internal transcribed spacer 1 (ITS1) region in nuclear ribosomal DNA, which differs between the species. The results suggested that there were not pre-mating but post-mating isolating mechanisms between the two species. However, viable adults of the hybrids F1 and F2 were produced from both parental F. hepatica and F. gigantica. The hybrids inherited phenotypic characteristics such as ratio of body length and width and infectivity to rats from parental Fasciola hepatica and F. gigantica. These findings suggest that reproductive isolation is incomplete between Fasciola hepatica and F. gigantica. Adults of the hybrids F1 and F2 were completely different in mode of reproduction from aspermic Fasciola forms that occur in Asia and seem to be offspring originated from hybridization between F. hepatica and F. gigantica and to reproduce parthenogenetically.

Keywords

Fasciola hepaticaFasciola giganticahybridizationhybridsF1F2reproductive isolation
Type
Research Article
Information
Parasitology , Volume 138 , Issue 10 , September 2011 , pp. 1278 - 1284
Copyright
Copyright © Cambridge University Press 2011

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., 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.CrossRefGoogle ScholarPubMed
Ashrafi, K., Valero, M. A., Panova, M., Periago, M. V., Massoud, J. and Mas-Coma, S. (2006). Phenotypic analysis of adults of Fasciola hepatica, Fasciola gigantica and intermediate forms from the endemic region of Gilan, Iran. Parasitology International 55, 249–260.CrossRefGoogle ScholarPubMed
Byrne, M. and Anderson, M. J. (1994). Hybridization of sympatric Patiriella species (Echinoderma: Asteroidea) in New South Walls. Evolution 48, 564–576.CrossRefGoogle Scholar
Chu, J. K. and Kim, Y. K. (1967). Taxonomical study on the Fasciolidae in Korea. Korean Journal of Parasitology 5, 139–146.CrossRefGoogle Scholar
Cosgrove, C. L. and Southgate, V. R. (2002). Mating interactions between Schistosoma mansoni and S. margrebowiei. Parasitology 125, 233–243.Google ScholarPubMed
Fan, P. C. and Lin, L. H. (2005). Hybridization of Schistosoma mansoni and Schistosoma japonicum in mice. The Southeast Asian Journal of Tropical Medicine and Public Health 36, 89–96.Google ScholarPubMed
Ichikawa, M. and Itagaki, T. (2010). Discrimination of the ITS1 types of Fasciola spp. based on a PCR-RFLP method. Parasitology Research 106, 757–761.CrossRefGoogle ScholarPubMed
Itagaki, T., Fujiwara, S., Mashima, K. and Itagaki, H. (1988). Experimental infection of Japanese Lymnaea snails with Australian Fasciola hepatica. Japanese Journal of Veterinary Science 50, 1085–1091.Google ScholarPubMed
Itagaki, T., Kikawa, M., Sakaguchi, K., Shimo, J., Terasaki, K., Shibahara, T. and Fukuda, K. (2005 a). Genetic characterization of parthenogenic Fasciola sp. in Japan on the basis of the sequences of ribosomal and mitochondrial DNA. Parasitology 131, 679–685.CrossRefGoogle ScholarPubMed
Itagaki, T., Kikawa, M., Terasaki, K., Shibahara, T. and Fukuda, K. (2005 b). 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Itagaki, T., Sakamoto, T., Tsutsumi, Y. and Itagaki, H. (1994). Infectivity of three species of Fasciola to Wistar rats. Journal of Veterinary Medical Science 56, 977–979.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Itagaki, T., Uchida, A. and Itagaki, H. (1989). Susceptibility of Japanese Lymnaea ollula to Nigerian Fasciola gigantica. Japanese Journal of Veterinary Science 51, 853–854.Google ScholarPubMed
Kimura, S., Shimizu, A. and Kawano, J. (1984). Morphological observation on liver fluke detected from naturally infected carabaos in the Philippines. The Science Reports of the Faculty of Agriculture, Kobe University 16, 353–357.Google Scholar
Koch, M. A., Dobes, C. and Mitchell-Olds, T. (2003). Multiple hybrid formation in natural populations: concerted evolution of the internal transcribed spacer of nuclear ribosomal DNA (ITS) in North American Arabis divaricarpa (Brassicaceae). Molecular Biology and Evolution 20, 338–350.CrossRefGoogle Scholar
Mango, A. M., Mango, C. K. and Esamal, D. (1972). A preliminary note on the susceptibility, prepatency and recovery of Fasciola gigantica in small laboratory animals. Journal of Helminthology 46, 381–386.CrossRefGoogle ScholarPubMed
Morgan, J. A. T., Dejong, R. J., Lwanbo, N. J. S., Mungai, B. N., Mkoji, G. M. and Loker, E. S. (2003). First report of a natural hybrid between Schistosoma mansoni and S. rodhaini. Journal of Parasitology 89, 416–418.CrossRefGoogle ScholarPubMed
Morgan-Richards, M. and Trewick, S. (2005). Hybrid origin of a parthenogenetic genus? Molecular Ecology 14, 2133–2142.CrossRefGoogle ScholarPubMed
Moriyama, N., Tsuji, M. and Seto, T. (1979). Three karyotypes and their phenotypes of Japanese liver flukes (Fasciola sp.). Japanese Journal of Parasitology 28, 23–33 (in Japanese with English summary).Google Scholar
Nollen, P. M. (1983). Patterns of sexual reproduction among parasitic playhelminths. Parasitology 86, 99–120.CrossRefGoogle Scholar
Nollen, P. M. (1990). Echinostoma caproni : mating behavior and the timing of development and movement of reproductive cells. Journal of Parasitology 76, 784–789.CrossRefGoogle ScholarPubMed
Nollen, P. M. (1996). Mating behaviour of Echinostoma caproni and E. paraensei in concurrent infections in mice. Journal of Helminthology 70, 133–136.CrossRefGoogle Scholar
Oshima, T., Akahane, H. and Shimazu, T. (1968). Patterns of the variation of the common liver fluke (Fasciola sp.) in Japan. I. Variations in the sizes and shapes of the worms and eggs. Japanese Journal of Parasitology 17, 97–105 (in Japanese with English summary).Google Scholar
Pages, J. R., Southgate, V. R., Tchuem Tchuente, L. A. and Jourdane, J. (2002). Experimental evidence of hybrid breakdown between the two geographical strains of Schistosoma intercalatum. Parasitology 124, 169–175.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Periago, M. V., Valero, M. A., El Sayed, M., Ashrafi, K., El Wakeel, A., Mohamed, M. Y., Desquesnes, M., Curtale, F. and Mas-Coma, S. (2007). First phenotypic description of Fasciola hepatica/Fasciola gigantica intermediate forms from the human endemic area of the Nile Delta, Egypt. Infection Genetics and Evolution 8, 51–58.CrossRefGoogle ScholarPubMed
Reddy, P. V. and Subramanyam, S. (1973). Chromosome studies in the liver fluke, Fasciola gigantica Cobbold, 1856, from Andra Pradesh. Current Science 42, 288–291.Google Scholar
Sakaguchi, Y. (1980). Karyotype and gametogenesis of the common liver fluke, Fasciola sp., in Japan. Japanese Journal of Parasitology 29, 507–513.Google Scholar
Sanderson, A. R. (1953). Maturation and probable gynogenesis in the liver fluke, Fasciola hepatica L. Nature, London 172, 110–112.CrossRefGoogle ScholarPubMed
Tchuem Tchuente, L. A., Southgate, V. R., Jourdane, J., Kaukas, A. and Vercruysse, J. (1997). Hybridisation between the digeneans Schistosoma haematobium and S. mattheei: viability of hybrids and their development in sheep. Systematic Parasitology 36, 123–131.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Thorpe, E. (1965). Liver damage and the host-parasite relationship in experimental fascioliasis in the albino rat. Research in Veterinary Science 6, 498–509.CrossRefGoogle ScholarPubMed
Torgerson, P. and Claxton, J. (1999). Epidemiology and control. In Fasciolosis (ed. Dalton, J. P.), pp. 113–149. CABI Publishing, Oxon, UK.Google Scholar
Trouve, S., Renaud, F., Durand, P. and Jourdane, J. (1998). Experimantal evidence of hybrid breakdown between genetically distinct populations of Echinostoma caproni. Parasitology 117, 133–135.CrossRefGoogle Scholar
Varma, A. K. (1953). On Fasciola indica n. sp. with some observations on F. hepatica and F. gigantica. Journal of Helminthology 27, 185–198.CrossRefGoogle Scholar
Watanabe, S. and Iwata, S. (1954). Fasciola species in Japan. Journal of Japanese Veterinary Medical Association 7, 124–126 (in Japanese).Google Scholar
Webster, B. L. and Southgate, V. R. (2003). Mating interactions of Schistosoma haematobium and S. intercalatum with their hybrid offspring. Parasitology 126, 327–338.CrossRefGoogle ScholarPubMed