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Nuclear and mitochondrial DNA analysis reveals that hybridization between Fasciola hepatica and Fasciola gigantica occurred in China

  • MADOKA ICHIKAWA-SEKI (a1), MAO PENG (a2), KEI HAYASHI (a1), TAKUYA SHORIKI (a1), UDAY KUMAR MOHANTA (a1), TOSHIYUKI SHIBAHARA (a3) and TADASHI ITAGAKI (a1)...

Summary

The well-known pathogens of fasciolosis, Fasciola hepatica (Fh) and Fasciola Gigantica (Fg), possess abundant mature sperms in their seminal vesicles, and thus, they reproduce bisexually. On the other hand, aspermic Fasciola flukes reported from Asian countries, which have no sperm in their seminal vesicles, probably reproduce parthenogenetically. The aim of this study was to reveal the origin of aspermic Fasciola flukes. The nuclear single copy markers, phosphoenolpyruvate carboxykinase and DNA polymerase delta, were employed for analysis of Fasciola species from China. The hybrid origin of aspermic Fasciola flukes was strongly suggested by the presence of the Fh/Fg type, which includes DNA fragments of both F. hepatica and F. gigantica. China can be regarded as the cradle of the interspecific hybridization because F. hepatica and F. gigantica were detected in the northern and southern parts of China, respectively, and hybrids flukes were distributed between the habitats of the two species. The Chinese origin was supported by the fact that a larger number of mitochondrial NADH dehydrogenase subunit 1 (nad1) haplotypes was detected in Chinese aspermic Fasciola populations than in aspermic populations from the neighbouring countries. Hereafter, ‘aspermic’ Fasciola flukes should be termed as ‘hybrid’ Fasciola flukes.

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Corresponding author

*Corresponding author: Laboratory of Veterinary Parasitology, Faculty of Agriculture, Iwate University, Ueda 3-18-8, Morioka 020-8550, Japan. E-mail: itagaki@iwate-u.ac.jp

References

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Avise, J. C., Quattro, J. M. and Vrijenhoek, C. (1992). Molecular clones within organismal clones: mitochondrial DNA phylogenies and the evolutionary histories of unisexual vertebrates. In Evolutionary Biology (ed. Hecht, M. K., Wallace, B. and Macintyre, R. J.), pp. 225246. Plenum Press, New York, USA.
Bandelt, H. J., Forster, P. and Rohl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 3748.
Beja-Pereira, A., Caramelli, D., Lalueza-Fox, C., Vernesi, C., Ferrand, N., Casoli, A., Goyache, F., Royo, L. J., Conti, S., Lari, M., Martini, A., Ouragh, L., Magid, A., Atash, A., Zsolnai, A., Boscato, P., Triantaphylidis, C., Ploumi, K., Sineo, L., Mallegni, F., Taberlet, P., Erhardt, G., Sampietro, L., Bertranpetit, J., Barbujani, G., Luikart, G. and Bertorelle, G. (2006). The origin of European cattle: evidence from modern and ancient DNA. Proceedings of the National Academy of Sciences of the United States of America 103, 81138118.
Cai, X., Chen, H., Lei, C., Wang, S., Xue, K. and Zhang, B. (2007). mtDNA diversity and genetic lineages of eighteen cattle breeds from Bos taurus and Bos indicus in China. Genetica 131, 175183.
Chaichanasak, P., Ichikawa, M., Sobhon, P. and Itagaki, T. (2012). Identification of Fasciola flukes in Thailand based on their spermatogenesis and nuclear ribosomal DNA, and their intraspecific relationships based on mitochondrial DNA. Parasitology International 61, 545549.
Chang, T. T. (1976). The rice cultures. In The early history of agriculture (ed. Hutchinson, J., Clark, J. G. G., Jope, E. M. and Riley, R.), pp. 143155. Oxford, London, UK.
Chen, S., Lin, B. Z., Baig, M., Mitra, B., Lopes, R. J., Santos, A. M., Magee, D. A., Azevedo, M., Tarroso, P., Sasazaki, S., Ostrowski, S., Mahgoub, O., Chaudhuri, T. K., Zhang, Y. P., Costa, V., Royo, L. J., Goyache, F., Luikart, G., Boivin, N., Fuller, D. Q., Mannen, H., Bradley, D. G. and Beja-Pereira, A. (2010). Zebu cattle are an exclusive legacy of the South Asia Neolithic. Molecular Biology and Evolution 27, 16.
Flad, R., Yuan, J. and Li, S. (2007). Zooarchaeological evidence for animal domestication in northwest China. In Late quaternary climate change and human adaptation in arid China. (ed. Madsen, D. B., Chen, F. H. and Gao, X.), pp. 167204. Elsevier, Amsterdam, the Netherland.
Hayashi, K., Ichikawa-Seki, M., Mohanta, U. K., Singh, T. S., Shoriki, T., Sugiyama, H. and Itagaki, T. (2015). Molecular phylogenetic analysis of Fasciola flukes from eastern India. Parasitology International 64, 334338.
Higham, C. (1996). The Bronze Age of Southeast Asia. Cambridge University Press, Cambridge, UK.
Huang, W. Y., He, B., Wang, C. R. and Zhu, X. Q. (2004). Characterisation of Fasciola species from Mainland China by ITS-2 ribosomal DNA sequence. Veterinary Parasitology 120, 7583.
Ichikawa, M. and Itagaki, T. (2012). Molecular analysis of aspermic Fasciola flukes from Korea on the basis of the nuclear ITS1 region and mitochondrial DNA markers and comparison with Japanese aspermic Fasciola flukes. Journal of Veterinary Medical Science 74, 899904.
Ichikawa, M., Iwata, N. and Itagaki, T. (2010). DNA types of aspermic Fasciola species in Japan. The Journal of Veterinary Medical Science 72, 13711374.
Ichikawa, M., Bawn, S., Maw, N. N., Htun, L. L., Thein, M., Gyi, A., Sunn, K., Katakura, K. and Itagaki, T. (2011). Characterization of Fasciola spp. in Myanmar on the basis of spermatogenesis status and nuclear and mitochondrial DNA markers. Parasitology International 60, 474479.
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, 679685.
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, 11151118.
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, 8185.
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.
Lin, R. Q., Dong, S. J., Nie, K., Wang, C. R., Song, H. Q., Li, A. X., Huang, W. Y. and Zhu, X. Q. (2007). Sequence analysis of the first internal transcribed spacer of rDNA supports the existence of the intermediate Fasciola between F. hepatica and F. gigantica in mainland China. Parasitology Research 101, 813817.
Mas-Coma, S., Valero, M. A. and Bargues, M. D. (2009). Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionarygenetics, molecular epidemiology and control. Advances in Parasitology 69, 41146.
Miyazaki, T. and Kobayashi, T. (2010). Visualization of the dynamic behavior of ribosomal RNA gene repeats in living yeast cells. Genes to Cells 16, 491502.
Mohanta, U. K., Ichikawa-Seki, M., 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, 24932501.
Mukai, F., Tsuji, S., Fukazawa, K., Ohtagaki, S. and Nambu, Y. (1989). History and population structure of a closed strain of Japanese Black cattle. Journal of Animal Breeding and Genetics 106, 254264.
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, 809815.
Phillips, R. W. (1961). World distribution of the major types of cattle. Journal of Heredity 52, 207213.
Shoriki, T., Ichikawa-Seki, M., Devkota, B., Rana, H. B., Devkota, S. P., Humagain, S. K. and Itagaki, T. (2014). Molecular phylogenetic identification of Fasciola flukes in Nepal. Parasitology International 63, 758762.
Shoriki, T., Ichikawa-Seki, M., Suganuma, K., Niato, I., Hayashi, K., Nakao, M., Aita, J., Mohanta, U. K., Inoue, N., Murakami, K. and Itagaki, T. (2015). Novel methods for the molecular discrimination of Fasciola spp. on the basis of nuclear protein-coding genes. Parasitology International 65, 180183.
Terasaki, K., Akahane, H. and Habe, S. (1982). The geographical distribution of common liver flukes (the Genus Fasciola) with normal and abnormal spermatogenesis. Japanese Journal of Veterinary Science 44, 223231.
Terasaki, K., Moriyama, N. and Noda, Y. (1998). Abnormal spermatogenesis in the common liver fluke (Fasciola sp.) from Japan and Korea. Journal of Veterinary Medical Science 60, 13051309.
Terasaki, K., Noda, Y., Shibahara, T. and Itagaki, T. (2000). Morphological comparison and hypothesis on the origin of polyploids in parthenogenetic Fasciola sp. Journal of Parasitology 86, 724729.
Terasaki, K., Itagaki, T., Shibahara, T., Noda, Y. and Moriyama-Gonda, N. (2001). Comparative study of the reproductive organs of Fasciola groups by optical microscope. Journal of Veterinary Medical Science 63, 735742.
Torgerson, P. and Claxton, J. (1999). Epidemiology and Control. In Fasciolosis (ed. Dalton, J. P.), pp. 113149. CABI, New York, USA.
Troy, C. S., MacHugh, D. E., Bailey, J. F., Magee, D. A., Loftus, R. T., Cunningham, P., Chamberlain, A. T., Sykes, B. C. and Bradley, D. G. (2001). Genetic evidence for Near-Eastern origins of European cattle. Nature 410, 10881091.

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