Paragonimus skrjabini Chen, 1959 (Digenea: Paragonimidae) and related species in eastern Asia: a combined molecular and morphological approach to identification and taxonomy (original) (raw)

Abstract

A molecular and morphometric investigation is reported on the species complex of mammalian lung.ukes of which Paragonimus skrjabini Chen, 1959 and P.miyazakii Kamo, Nishida, Hatsushika & Tomimura, 1961 are the best-known examples. This species complex (here called the P.skrjabini complex) is shown to be monophyletic using DNA sequences from the nuclear ITS2 region and the mitochondrial cox1gene. The latter marker permits the discrimination of populations, some previously named as distinct species, from various geographical locations in China and Japan. Morphometric analysis of a number of variables accords remarkably closely with the molecular results. Main findings are that (1) nominal P.skrjabini from Fujian Province in eastern China is phylogenetically very close to P.miyazakii from Japan. It is proposed that both taxa should be referred to the same subspecies as P.skrjabini miyazakii. (2) Populations from Guangdong Province, Guangxi Zhuang Autonomous Region, Sichuan and Hubei should be referred to P.skrjabini skrjabini. Specimens of P.skrjabini from the Yangtze basin in Sichuan and Hubei are remarkably similar to one another according to genetic and morphometric data, but are not so different from Guangdong populations that they should be referred to a different subspecies at this stage. Specimens of P.skrjabini from Yunnan have not been assigned to a subspecies at this stage. (3) Partly following earlier studies, we regard the following as synonyms of P.skrjabini: P.miyazakii (reduced to subspecific status); P.szechuanensis Chung & Tsao, 1962 (probably belongs to P.s.skrjabini); and P.hueitungensis Chung, Hsu, Ho, Kao, Shao, Chiu, Pi, Liu, Ouyang, Shen, Yi & Yao, 1975 (probably belongs to P.s.skrjabini ); P.veocularis (Chen & Li, 1979) (specimens from Fujian regarded as belonging to this species should be referred to P.skrjabini miyazakii: the subspecific status of specimens from the type-locality in northern Sichuan is unclear). A number of questions remain unresolved. The name P. hokuoensis Ho & Chung, 1964 was proposed for two individual metacercariae of distinctive appearance from southern Yunnan. DNA sequences from very similar metacercariae from the same locality place this nominal species within, or sister to, the P. skrjabini complex. As yet, nothing is known regarding adult morphology or biology of this taxon and we retain it here as a distinct species. P. heterorchis (Zhou, Pang & Hsiang, 1982) might be a synonym of P. skrjabini: the form of the metacercaria provides evidence against this view and further work is required. P. macrorchis Chen, 1962 has probably been confused with P. skrjabiniin China. Within China, the former probably occurs only on Hainan Island, although P. fukienensis Tang & Tang, 1962 from Fujian Province could be a synonym.

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References

• Anonymous (1976) Preliminary survey of paragonimiasis in Jain’ou County of Fujian Province. Compiled by the Jian’ou County Paragonimiasis Control Study Group. Brief Reports on Parasitic Disease Control Research, (5), 25-26 (in Chinese).
• D. Blair T. Agatsuma T. Watanobe M. Okamoto A. Ito (1997)ArticleTitleGeographical genetic structure within the human lung fluke, Paragonimuswestermani, detected from DNA sequences_Parasitology._ 115 411–417
  Google Scholar
• Blair, D., Waikagul, J., Honzako, Y. & Agatsuma, T. (1998) Phylogenetic relationships among the Thai species of Paragonimus inferred from DNA sequences. In: Tada, I., Kojima, S. & Tsuji, M. (Eds) Proceedings of the 9th International Congress of Parasitology, Chiba, Japan, 24-28 August 1998. Bologna: Monduzzi International, pp. 643-647.
• Blair, D., Watanobe, T. & Agatsuma, T. (1997b) Molecular evidence for the synonymy of three species of Paragonimus, P. ohirai Miyazaki, 1939, P. iloktsuenensis Chen, 1940 and P. sadoensis Miyazaki et al., 1968. Journal of Helminthology, 71, 305
• D. Blair G.M. Davis B. Wu (2001)ArticleTitleEvolutionary relationships between trematodes and snails emphasizing schistosomes and paragonimids_Parasitology._ 123 S229–S243
  Google Scholar
• D. Blair Z.B. Xu T. Agatsuma (1999)ArticleTitleParagonimiasis and the genus Paragonimus_Advances in Parasitology._ 42 113–222
  Google Scholar
• Blair, D., Wu B., Chang Z.S., Gong X., Agatsuma, T., Zhang Y.N., Chen S.H., Lin J.X., Chen M.G., Waikagul, J., Guevara, A.G., Feng Z. & Davis, G.M. (1999b) A molecular perspective on the genera Paragonimus Braun, Euparagonimus Chen and Pagumogonimus Chen. Journal of Helminthology, 73, 295-300.
• J. Bowles M. Hope W.U. Tiu X.S. Liu D.P. McManus (1993)ArticleTitleNuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosomajaponicum_ActaTropica._ 55 217–229
  Google Scholar
• Chen H.T. (1959) The occurrence of a new type of Paragonimusand some clinical problems related to lung flukes in China. Annual Report 1958, Chung Shan Medical College, Guangzhou, pp. 192-193 (in Chinese).
• Chen H.T. (1964) Morphological studies on the adult Paragonimus(M.) macrorchisChen, 1962, with a consideration on the taxonomy of the Paragonimidae. Acta Zoologica Sinica, 16, 381-392 (in Chinese, English abstract).
  Google Scholar
• H.T. Chen H.S. Hu K.T. Ho (1966)ArticleTitleMorphological investigations on the metacercaria of Pagumogonimus skrjabini with notes on the histochemical studies of the cyst wall_Scientia Sinica._ 15 706–715
  Google Scholar
• H.L. Chung C.P. Hsu L.Y. Ho P.C. Kao L. Shao F.H. Chiu W.T. Pi K.H. Liu C.P. Ouyang P.K. Shen C.C. Yi T.S. Yao (1975)ArticleTitleStudies on a new pathogenic lung fluke - Paragonimushueit’ungensis sp. nov_Scientia Sinica._ 18 785–814
  Google Scholar
• Chung H.L., Ho L.Y., Ts’ao W.C., Hsu C.P. & Kao P.C. (1975b) On the metacercariae of some Paragonimus species and other trematodes found in Chinese freshwater crabs. Acta Zoologica Sinica, 21, 155-165 (in Chinese, English abstract).
  Google Scholar
• A.I. Cui Z.S. Chang M.G. Chen Blair D. Y.N. Zhang S.H. Chen Z. Feng (2003)ArticleTitleStudy on DNA sequences of Paragonimus skrjabini populations from five provinces in China_Chinese Journal of Parasitology and Parasitic Diseases._ 21 71–75
  Google Scholar
• C.B. Fu X.M. Zhan X.M. Wu Z.Y. Li Y. Wang A. He (2002)ArticleTitleStudies on application of digital image processing technique to automatic taxonomy of Paragonimus_Chinese Journal of Zoonoses._ 18 39–43
  Google Scholar
• wagami M., Ho L.Y., Su K., Lai P.F., Fukushima M., Nakano M., Blair D., Kawashima, sumatermaniin Asia. Journal of Helminthology, 74, 315-322.
• D.W. Kannangara (1969)ArticleTitleOccurrence of the lung fluke Paragonimus macrorchis Chen, 1962 in Ceylon_Ceylon Journal of Medical Science._ 18 33–38
  Google Scholar
• S. Kumar K. Tamura I.B. Jakobsen M. Nei (2001) MEGA2: Molecular Evolutionary Genetics Analysis software Arizona State University Tempe, Arizona, USA
  Google Scholar
• Y.S. Li (1999)ArticleTitleSpecies index table for the adult and metacercaria of Chinese Paragonimus_Chinese Journal of Veterinary Parasitology._ 7 59–62
  Google Scholar
• Y.S. Li Y. Chen C. Lin_et al._ (2000)ArticleTitleOccurrence of Pagumogonimus veocularis in Fujian Province_Chinese Journal of Parasitology and Parasitic Diseases._ 18 296–300
  Google Scholar
• Maejima J. Kamo H. R. Hatsushika (1971)ArticleTitleStudies on Paragonimus miyazakii Kamo, Nishida, Hatsushika et Tomimura, 1961. 2. Second intermediate host and intracrab stage_Yonago Acta Medica._ 15 35–44
  Google Scholar
• Miyazaki I. (1965). Recent studies on Paragonimus in Japan with special reference to P. ohirai Miyazaki, 1939, P. iloktsuenensis Chen, 1940 and P. miyazaki Kamo, Nishida, Hatsushika et Tomimura, 1961. Progress in Medical Parasitology in Japan, 2, 330-345.
• Miyazaki, I. (1974) Lung flukes in the world: morphology and life history. In: Asymposium on epidemiology of parasitic diseases. Tokyo: International Medical Foundation of Japan, pp. 101-135.
• Miyazaki, I. (1991) Anillustrated book of helminthic zoonoses. Tokyo: International Medical Foundation of Japan, 494 pp.
• I. Miyazaki S. Vajrasthira (1967)ArticleTitleOccurrence of the lung fluke Paragonimus macrorchis Chen,1962 in Thailand_Journal of Parasitology._ 53 894–895
  Google Scholar
• Nicholas, K.B. & Nicholas, H.B., Jr (1997) Genedoc: a tool for editing and annotating multiple sequence alignments. Distributed by the authors.
• D. Posada K.A. Crandall (1998)ArticleTitleModeltest: testing the model of DNA substitution_Bioinformatics._ 14 817–818
  Google Scholar
• T.S. Singh (2003)ArticleTitleOccurrence of the lung .uke Paragonimus hueit’ungensis in Manipur, India_Chinese Medical Journal (Taipei)_ 65 426–429
  Google Scholar
• Swofford, D. L. 2003 PAUP*. Phylogenetic Analysis Using Parsimony(*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
• Vevers, G.M. (1923) Observations on the genus Paragonimus Braun with a re-description of P.compactus(Cobbold, 1859) 1899 [sic]. Journal of Helminthology, 1, 9-20.
  Google Scholar
• J. Waikagul P. Setasuban S. Vajrasthira (1989)ArticleTitleOn a species of Paragonimus lung fluke metacercaria in Thailand_Southeast Asian Journal of Tropical Medicine and Public Health._ 20 495–497
  Google Scholar
• M.B. Wei Z.Y. Bao G. He_et al._ (1993)ArticleTitleDiscovery of human Pagumogonimus macrorchis infection and survey on its distribution_Chinese Journal of Zoonoses._ 9 4–6
  Google Scholar
• X. Xia (2000) Data analysis in molecular biology and evolution Kluwer Academic Publishers Dordrecht 277
  Google Scholar
• X.H. Xia Z. Xie M. Salemia L. Chen Y. Wang (2003)ArticleTitleAn index of substitution saturation and its application_Molecular Phylogenetics and Evolution._ 26 1–7
  Google Scholar
• Yang J.S., Chen M.G., Zheng F. & Blair, D. (2000) Paragonimusand paragonimiasis in China: a review of the literature. Chinese Journal of Parasitology and Parasitic Diseases, special issue, 78 pp.
• Z.M. Zhan Z.Y. Li X.C. Xu Q.Y. Li (1997)ArticleTitleStudies on numerical taxonomy of lung flukes and their application_Supplement to the Journal of Sun Yatsen University._ 1 6–10
  Google Scholar
• S.L. Zhou D.H. Pang Z.S. Hsiang (1982)ArticleTitleA preliminary description of a new lung fluke Pagumogonimus heterorchissp. nov_Hubei Medical Journal._ 3 23–27
  Google Scholar
• S.L. Zhou D.H. Pang P.X. Zhang X.S. Xiang (1986)ArticleTitleA further study on the morphology of Pagumogonimus heterorchis(Trematoda: Paragonimidae)Acta Zoologica Sinica. 32 196–198
  Google Scholar

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Authors and Affiliations

1. School of Tropical Biology, James Cook University, Townsville, Queensland, 4811, Australia
   David Blair & David Corlis
2. National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, 207 Rui Jin Rd II, Shanghai, 200025, P.R., China
   Chang Zhengshan, Chen Minggang, Cui Aili & Wu Bo
3. Department of Environmental Health Science, Kochi Medical School, Nankoku City, Kochi, 783-8505, Japan
   Takeshi Agatsuma & Moritoshi Iwagami
4. Department of Parasitology, Zhong Shan Medical University, Guangzhou, Guangdong, P.R., China
   Fu Chengbin & Zhan Ximei
5. National Measles Laboratory, Chinese Centers for Disease Control, 505#room, 27#Nan Wei Road, Xuan Wu District, Beijing, 100050, P.R., China
   Cui Aili
6. ROOS Lab/Goddard Building, Department of Biology, University of Pennsylvania, Philadelphia, PA, 19104-6018, USA
   Wu Bo

Authors

1. David Blair
2. Chang Zhengshan
3. Chen Minggang
4. Cui Aili
5. Wu Bo
6. Takeshi Agatsuma
7. Moritoshi Iwagami
8. David Corlis
9. Fu Chengbin
10. Zhan Ximei

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Blair, D., Zhengshan, C., Minggang, C. et al. Paragonimus skrjabini Chen, 1959 (Digenea: Paragonimidae) and related species in eastern Asia: a combined molecular and morphological approach to identification and taxonomy.Syst Parasitol 60, 1–21 (2005). https://doi.org/10.1007/s11230-004-1378-5

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• Accepted: 10 May 2004
• Issue date: January 2005
• DOI: https://doi.org/10.1007/s11230-004-1378-5

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