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Genetic differences in the rat lungworm, Angiostrongylus cantonensis (Nematoda: Angiostrongylidae), in Thailand

Published online by Cambridge University Press:  16 June 2014

S. Dusitsittipon ,
U. Thaenkham ,
D. Watthanakulpanich ,
P. Adisakwattana  and
C. Komalamisra
S. Dusitsittipon
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
U. Thaenkham
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
D. Watthanakulpanich
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
P. Adisakwattana
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
C. Komalamisra*
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
*
*E-mail: [email protected]
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Abstract

This study surveyed the genetic differences among Angiostrongylus cantonensis (A. cantonensis) using the mitochondrial cytochrome b (cytb) gene. Partial cytb sequences were determined for 91 worms from eight locations in Thailand. Using morphological techniques, the nematodes were found to be A. cantonensis. Phylogenetic analysis found two main clades, which were subdivided into four subclades (clusters). Haplotype network analysis showed that 11 distinct cytb haplotypes were also present in four groups of A. cantonensis. There was no observable relationship between the genetic differentiation of gene flow and geographical distance. This low genetic variation and geographical distribution of A. cantonensis in each location indicates a founder effect, which may have resulted from multiple independent origins, and suggests that haplotypes migrated from endemic areas via human-related activities.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 5 , September 2015 , pp. 545 - 551
Copyright
Copyright © Cambridge University Press 2014 

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References

Acedo, J., Dropkin, V. & Luedders, V. (1984) Nematode population attrition and histopathology of Heterodera glycines-soybean associations. Journal of Nematology 16, 48–56.Google ScholarPubMed
Alicata, J. (1965) Biology and distribution of the rat lungworm, Angiostrongylus cantonensis, and its relationship to eosinophilic meningoencephalitis and other neurological disorders of man and animals. Advances in Parasitology 3, 223–248.Google ScholarPubMed
Bhaibulaya, M. (1979) Morphology and taxonomy of major Angiostrongylus species of Eastern Asia and Australia. pp. 4–13. Taipei, US Naval Medical Research Unit.Google Scholar
Blouin, M. (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527–531.CrossRefGoogle ScholarPubMed
Brown, W., George, M. Jr & Wilson, A. (1979) Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Sciences of the United States of America 76, 1967–1971.CrossRefGoogle ScholarPubMed
Chotmongkol, V. & Sawanyawisuth, K. (2002) Clinical manifestations and outcome of patients with severe eosinophilic meningoencephalitis presumably caused by Angiostrongylus cantonensis. The Southeast Asian Journal of Tropical Medicine and Public Health 33, 231–234.Google ScholarPubMed
Clement, M., Posada, D. & Crandall, K. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.CrossRefGoogle ScholarPubMed
Eamsobhana, P. (2006) The rat lungworm Parastrongylus ( = Angiostrongylus) cantonensis: parasitology, immunology, eosinophilic meningitis, epidemiology and laboratory diagnosis. Bangkok: Wankaew (IQ) Book Center.Google Scholar
Eamsobhana, P., Lim, P., Solano, G., Zhang, H., Gan, X. & Yong, H. (2010a) Molecular differentiation of Angiostrongylus taxa (Nematoda: Angiostrongylidae) by cytochrome c oxidase subunit I (COI) gene sequences. Acta Tropica 116, 152–156.CrossRefGoogle ScholarPubMed
Eamsobhana, P., Lim, P., Zhang, H., Gan, X. & Yong, H. (2010b) Molecular differentiation and phylogenetic relationships of three Angiostrongylus species and Angiostrongylus cantonensis geographical isolates based on a 66-kDa protein gene of A. cantonensis (Nematoda: Angiostrongylidae). Experimental Parasitology 126, 564–569.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
Goka, K., Yokoyama, J., Une, Y., Kuroki, T., Suzuki, K., Nakahara, M., Kobayashi, A., Inaba, S., Mizutani, T. & Hyatt, A. (2009) Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan. Molecular Ecology 18, 4757–4774.CrossRefGoogle ScholarPubMed
Kanpittaya, J., Jitpimolmard, S., Tiamkao, S. & Mairiang, E. (2000) MR findings of eosinophilic meningoencephalitis attributed to Angiostrongylus cantonensis. American Journal of Neuroradiology 21, 1090–1094.Google ScholarPubMed
Kliks, M. & Palumbo, N. (1992) Eosinophilic meningitis beyond the Pacific Basin: the global dispersal of a peridomestic zoonosis caused by Angiostrongylus cantonensis, the nematode lungworm of rats. Social Science and Medicine 34, 199–212.CrossRefGoogle ScholarPubMed
Lima, A., Mesquita, S., Santos, S., Aquino, E., Rosa L., , Duarte, F., Teixeira, A., Costa, Z. & Ferreira, M. (2009) Alicata disease: neuroinfestation by Angiostrongylus cantonensis in Recife, Pernambuco, Brazil. Arquivos de Neuro-psiquiatria 67, 1093–1096.CrossRefGoogle ScholarPubMed
Lv, S., Zhang, Y., Steinmann, P. & Zhou, X. (2008) Emerging angiostrongyliasis in Mainland China. Emerging Infectious Diseases 14, 161–164.CrossRefGoogle ScholarPubMed
Matsui, M., Tominaga, A., Hayashi, T., Misawa, Y. & Tanabe, S. (2007) Phylogenetic relationships and phylogeography of Hynobius tokyoensis (Amphibia: Caudata) using complete sequences of cytochrome b and control region genes of mitochondrial DNA. Molecular Phylogenetics and Evolution 44, 204–216.CrossRefGoogle ScholarPubMed
Nei, M. (1996) Phylogenetic analysis in molecular evolutionary genetics. Annual Review of Genetics 30, 371–403.CrossRefGoogle ScholarPubMed
Nieberding, C., Libois, R., Douady, C., Morand, S. & Michaux, J. (2005) Phylogeography of a nematode (Heligmosomoides polygyrus) in the western Palearctic region: persistence of northern cryptic populations during ice ages? Molecular Ecology 14, 765–779.CrossRefGoogle ScholarPubMed
Pasi, K., Lakra, W., Bhatt, J., Goswami, M. & Malakar, A. (2013) Population structure of Tor tor inferred from mitochondrial gene cytochrome b. Mitochondrial DNA 24, 290–296.CrossRefGoogle ScholarPubMed
Pawson, P. & Chase, R. (1984) The life-cycle and reproductive activity of Achatina fulica (Bowdich) in laboratory culture. Journal of Molluscan Studies 50, 85–91.CrossRefGoogle Scholar
Rawlings, T., Hayes, K., Cowie, R. & Collins, T. (2007) The identity, distribution, and impacts of non-native apple snails in the continental United States. Evolutionary Biology 7, 97.Google ScholarPubMed
Rozas, J., Sanchez-DelBarrio, J., Messeguer, X. & Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.CrossRefGoogle ScholarPubMed
Russell, J., Gleeson, D. & Le Corre, M. (2011) The origin of Rattus rattus on the Îles Éparses, Western Indian Ocean. Biogeography 38, 1834–1836.Google Scholar
Salzburger, W., Martens, J., Nazarenko, A., Sun, Y., Dallinger, R. & Sturmbauer, C. (2002) Phylogeography of the Eurasian Willow Tit (Parus montanus) based on DNA sequences of the mitochondrial cytochrome b gene. Molecular Phylogenetics and Evolution 24, 26–34.CrossRefGoogle ScholarPubMed
Schmutzhard, E., Boongird, P. & Vejjajiva, A. (1988) Eosinophilic meningitis and radiculomyelitis in Thailand, caused by CNS invasion of Gnathostoma spinigerum and Angiostrongylus cantonensis. Journal of Neurology, Neurosurgery, and Psychiatry 51, 80–87.CrossRefGoogle ScholarPubMed
Slatkin, M. & Barton, N. (1989) A comparison of three indirect methods for estimating average levels of gene flow. Evolution 43, 1349–1368.CrossRefGoogle ScholarPubMed
Solignac, M., Cornuet, J., Vautrin, D., Le Conte, Y., Anderson, D., Evans, J., Cros-Arteil, S. & Navajas, M. (2005) The invasive Korea and Japan types of Varroa destructor, ectoparasitic mites of the Western honeybee (Apis mellifera), are two partly isolated clones. Proceedings of the Royal Society, Biological Sciences 272, 411–419.CrossRefGoogle ScholarPubMed
Stone, G., Challis, R., Atkinson, R., Csoka, G., Hayward, A., Melika, G., Mutun, S., Preuss, S., Rokas, A., Sadeghi, E. & Schonrogge, K. (2007) The phylogeographical clade trade: tracing the impact of human-mediated dispersal on the colonization of northern Europe by the oak gallwasp Andricus kollari. Molecular Ecology 16, 2768–2781.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Templeton, A., Crandall, K. & Sing, C. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619–633.Google ScholarPubMed
Thaenkham, U., Pakdee, W., Nuamtanong, S., Maipanich, W., Pubampen, S., Sa-Nguankiat, S. & Komalamisra, C. (2012) Population structure of Angiostrongylus cantonensis (Nematoda: Metastrongylidae) in Thailand based on PCR-RAPD markers. The Southeast Asian Journal of Tropical Medicine and Public Health 43, 567–573.Google ScholarPubMed
Thiengo, S., Fernandez, M., Torres, E., Coelho, P. & Lanfredi, R. (2008) First record of a nematode Metastrongyloidea (Aelurostrongylus abstrusus larvae) in Achatina (Lissachatina) fulica (Mollusca, Achatinidae) in Brazil. Journal of Invertebrate Pathology 98, 34–39.CrossRefGoogle ScholarPubMed
Thompson, J., Gibson, T., Plewniak, F., Jeanmougin, F. & Higgins, D. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle ScholarPubMed
Tokiwa, T., Harunari, T., Tanikawa, T., Komatsu, N., Koizumi, N., Tung, K., Suzuki, J., Kadosaka, T., Takada, N., Kumagai, T., Akao, N. & Ohta, N. (2012) Phylogenetic relationships of rat lungworm, Angiostrongylus cantonensis, isolated from different geographical regions revealed widespread multiple lineages. Parasitology International 61, 431–436.Google ScholarPubMed
Tollenaere, C., Brouat, C., Duplantier, J., Rahalison, L., Rahelinirina, S., Pascal, M., Moné, H., Mouahid, G., Leirs, H. & Cosson, J. (2009) Phylogeography of the introduced species Rattus rattus in the western Indian Ocean, with special emphasis on the colonization history of Madagascar. Biogeography 37, 398–410.CrossRefGoogle Scholar
Vitta, A., Polseela, R., Nateeworanart, S. & Tattiyapong, M. (2011) Survey of Angiostrongylus cantonensis in rats and giant African land snails in Phitsanulok province, Thailand. Asian Pacific Journal of Tropical Medicine 4, 597–599.CrossRefGoogle ScholarPubMed
Vogler, A., Chan, F., Wagner, D., Roumagnac, P., Lee, J., Nera, R., Eppinger, M., Ravel, J., Rahalison, L., Rasoamanana, B., Beckstrom-Sternberg, S., Achtman, M., Chanteau, S. & Keim, P. (2011) Phylogeography and molecular epidemiology of Yersinia pestis in Madagascar. PLoS Neglected Tropical Diseases 5, e1319.CrossRefGoogle ScholarPubMed
Wang, Q., Lai, D., Zhu, X., Chen, X. & Lun, Z. (2008) Human angiostrongyliasis. The Lancet Infectious Diseases 8, 621–630.CrossRefGoogle ScholarPubMed
Wright, S. (1978) Evolution and genetics of natural populations. Vol. 4. Variability within and among natural populations. 590 pp. Chicago, University of Chicago Press.Google Scholar