Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-23T05:06:26.910Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular characterization and phylogenetic analysis of ascarid nematodes from twenty-one species of captive wild mammals based on mitochondrial and nuclear sequences

Published online by Cambridge University Press:  01 May 2012

YAN LI ,
LILI NIU ,
QIANG WANG ,
ZHIHE ZHANG ,
ZHIGANG CHEN ,
XIAOBIN GU ,
YUE XIE ,
NING YAN ,
SHUXIAN WANG  and
XUERONG PENG
...Show all authors
YAN LI
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Ya'an 625014, China
LILI NIU
Affiliation:
Veterinary Hospital, Chengdu Zoological Garden, Chengdu, Sichuan 610081, China
QIANG WANG
Affiliation:
Veterinary Hospital, Chengdu Zoological Garden, Chengdu, Sichuan 610081, China
ZHIHE ZHANG
Affiliation:
The Sichuan Key Laboratory for Conservation Biology on Endangered Wildlife – Developing toward a State Key Laboratory for China, Chengdu Research Base of Giant Panda Breeding, Chengdu, Sichuan 610081, China
ZHIGANG CHEN
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Ya'an 625014, China
XIAOBIN GU
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Ya'an 625014, China
YUE XIE
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Ya'an 625014, China
NING YAN
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Ya'an 625014, China
SHUXIAN WANG
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Ya'an 625014, China
XUERONG PENG
Affiliation:
Department of Chemistry, College of Life and Basic Science, Sichuan Agricultural University, Ya'an 625014, China
GUANGYOU YANG*
Affiliation:
Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Ya'an 625014, China
*
*Corresponding author: Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Ya'an 625014, China. Tel: +86 835 2882787. Fax: +86 835 2885302. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Although ascarid nematodes are important parasites of wild animals of public health concern, few species of ascarids from wild animals have been studied at the molecular level so far. Here, the classification and phylogenetic relationships of roundworms from 21 species of captive wild animals have been studied by sequencing and analysis of parts of the ribosomal 18S and 28S genes and the mitochondrial (mt) 12S gene. Phylogenetic relationships were inferred by 3 methods (NJ/MP/ML) based on the data of single gene sequences and concatenated sequences. Homology analysis indicated that the 18S sequences were conserved among roundworms from all 21 species and that 28S showed interspecies variability. Divergence levels displayed in 12S suggested that 12S appears to be either intra- or interspecifically variable. Evolutionary trees indicated that the ascarids split into 2 families, 4 genera and 7 species, with high bootstrap support for each clade. Combined trees suggested that Baylisascaris ailuri is more closely related to B. transfuga than to B. schroederi. This study provides useful molecular markers for the classification, phylogenetic analysis and epidemiological investigation of roundworms from wild animals.

Keywords

giant pandawild mammalsAscarid nematodesmitochondrial genenuclear geneclassificationmolecular phylogeny
Type
Research Article
Information
Parasitology , Volume 139 , Issue 10 , September 2012 , pp. 1329 - 1338
Copyright
Copyright © Cambridge University Press 2012

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

Blaxter, M. L., De Ley, P., Garey, J. R., Liu, L. X., Scheldeman, P., Vierstraete, A., Vanfleteren, J. R., Mackey, L. Y., Dorris, M. and Frisse, L. M. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature, London 392, 71–75. doi: 10.1038/32160 CrossRefGoogle ScholarPubMed
Crompton, D. W. T. (2001). Ascaris and ascariasis. Advances in Parasitology 48, 285–375. doi:10.1016/S0065-308X(01)48008-0.CrossRefGoogle ScholarPubMed
Despommier, D. (2003). Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clinical Microbiology Reviews 16, 265–272. doi: 10.1128/CMR.16.2.265-272.2003 CrossRefGoogle ScholarPubMed
Foster, G. W., Cunningham, M. W., Kinsella, J. M. and Forrester, D. J. (2009). Parasitic helminths of black bear cubs (Ursus americanus) from Florida. Journal of Parasitology 90, 173–175. doi: http://dx.doi.org/10·1645/GE-127R CrossRefGoogle Scholar
Gasser, R. B., Chilton, N. B., Hoste, H. and Beveridge, I. (1993) Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21, 2525–2526. doi: 10.1093/nar/21.10.2525 CrossRefGoogle ScholarPubMed
Gibson, D. I. (1983). The systematics of ascaridoid nematodes-a current assessment. In Concepts in Nematode Systematics (ed. Stone, A. R., Platt, H. M. and Khalil, L. F.), pp. 321–338. Academic Press, New York, USA.Google Scholar
González, P., Carbonell, E., Urios, V. and Rozhnov, V. V. (2007). Coprology of Panthera tigris altaica and Felis bengalensis euptilurus from the Russian Far East. Journal of Parasitology 93, 948–950. doi: http://dx.doi.org/10.1645/GE−3519RN.1.CrossRefGoogle ScholarPubMed
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704. doi: 10.1080/10635150390235520.CrossRefGoogle ScholarPubMed
He, G. Z., Niu, L. L., Yang, G. Y., Deng, J. B, Wang, S. X., Yu, X. M., Wang, T., Gu, X. B. and Cheng, W. G. (2008). Sequence analysis of ITS-2 rDNA of roundworms from Ailuropoda melanoleuca and seven rare wild animals. Chinese Veterinary Science 11, 933–938 (in Chinese).Google Scholar
Hu, H. G., Huang, H., Zhao, G. L. and Wu, J. (1993). Name list of parasites in wild animals of Chongqing zoological garden. Journal of China West Normal University (Natural Sciences) 14, 315–325 (in Chinese).Google Scholar
Hu, M., Chilton, N. B. and Gasser, R. B. (2003 a). The mitochondrial genomics of parasitic nematodes of socio-economic importance: recent progress, and implications for population genetics and systematics. Advances in Parasitology 56, 133–212. doi:10.1016/S0065-308X(03)56003-1.CrossRefGoogle Scholar
Hu, M., Chilton, N. B. and Gasser, R. B. (2003 b). The mitochondrial genome of Strongyloides stercoralis (Nematoda) – idiosyncratic gene order and evolutionary implications. International Journal for Parasitology 33, 1393–1408. doi:10.1016/S0020-7519(03)00130-9.CrossRefGoogle ScholarPubMed
Jacobs, D. E., Zhu, X. Q., Gasser, R. B. and Chilton, N. B. (1997). PCR-based methods for identification of potentially zoonotic ascaridoid parasites of the dog, fox and cat. Acta Tropica 68, 191–200. doi:10.1016/S0001-706X(97)00093-4.CrossRefGoogle ScholarPubMed
Li, J., Zhao, G. H., Zou, F. C., Mo, X. H., Yuan, Z. G., Ai, L., Li, H. L., Weng, Y. B., Lin, R. Q. and Zhu, X. Q. (2010). Combined mitochondrial 16S and 12S rDNA sequences: an effective genetic marker for inter-species phylogenetic analysis of zoonotic trematodes. Parasitology Research 107, 561–569. doi: 10.1007/s00436-010-1895-x.CrossRefGoogle ScholarPubMed
Lim, Y. A. L., Ngui, R., Shukri, J., Rohela, M. and Mat Naim, H. R. (2008). Intestinal parasites in various animals at a zoo in Malaysia. Veterinary Parasitology 157, 154–159. doi:10.1016/j.vetpar.2008.07.015.CrossRefGoogle Scholar
Loytynoja, A. and Milinkovitch, M. C. (2003) A hidden Markov model for progressive multiple alignment. Bioinformatics 19, 1505–1513. doi:10.1093/bioinformatics/ btg193.CrossRefGoogle ScholarPubMed
Nadler, S. A. (1992). Phylogeny of some ascaridoid nematodes, inferred from comparison of 18S and 28S rRNA sequences. Molecular Biology and Evolution 9, 932–944. doi: 0737-4038/92/0905-0013 Google ScholarPubMed
Nadler, S. A. (1995). Advantages and disadvantages of molecular phylogenetics: A case study of ascaridoid nematodes. Journal of Nematology 27, 423–432.Google ScholarPubMed
Nadler, S. A. and Hudspeth, D. S. S. (1998). Ribosomal DNA and phylogeny of the Ascaridoidea (Nemata: Secernentea): implications for morphological evolution and classification. Molecular Phylogenetics and Evolution 10, 221–236. doi:10.1006/mpev.1998.0514.CrossRefGoogle ScholarPubMed
Nadler, S. A. and Hudspeth, D. S. S. (2000). Phylogeny of the Ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: Hypotheses of structural and sequence evolution. Journal of Parasitology 86, 380–393. doi: http://dx.doi.org/ 10.1645/0022-3395(2000) 086[0380:POTANA]2.0.CO;2.CrossRefGoogle ScholarPubMed
Nadler, S. A., Bolotin, E. and Stock, S. P. (2006). Phylogenetic relationships of Steinernema travassos, 1927 (Nematoda: Cephalobina: Steinernematidae) based on nuclear, mitochondrial and morphological data. Systematic Parasitology 63, 159–179. doi: 10.1007/s11230-005-9009-3.CrossRefGoogle ScholarPubMed
Nejsum, P., Parker, E. D. Jr., Frydenberg, J., Roepstorff, A., Boes, J., Haque, R., Astrup, I., Prag, J. and Skov Sorensen, U. B. (2005). Ascariasis is a zoonosis in Denmark. Journal of Clinical Microbiology 43, 1142–1148. doi:10.1128/JCM.43.3.1142-1148.2005.CrossRefGoogle ScholarPubMed
Nejsum, P., Grondahl, C. and Murrell, K. D. (2006). Molecular evidence for the infection of zoo chimpanzees by pig Ascaris . Veterinary Parasitology 139, 203–210. doi:10.1016/j.vetpar.2006.02.025.CrossRefGoogle ScholarPubMed
Nejsum, P., Bertelsen, M. F., Betson, M., Stothard, J. R. and Murrell, K. D. (2010). Molecular evidence for sustained transmission of zoonotic Ascaris suum among zoo chimpanzees (Pan troglodytes). Veterinary Parasitology 171, 273–276. doi:10.1016/j.vetpar.2010.03.030.CrossRefGoogle ScholarPubMed
Okulewicz, A., Lonc, E. and Borgsteede, F. H. (2002). Ascarid nematodes in domestic and wild terrestrial mammals. Polish Journal of Veterinary Sciences 5, 277–281. PMID: 12512563.Google ScholarPubMed
Razo-Mendivil, U., Vázquez-Domínguez, E., Rosas-Valdez, R., de León, G. P. P. and Nadler, S. A. (2010). Phylogenetic analysis of nuclear and mitochondrial DNA reveals a complex of cryptic species in Crassicutis cichlasomae (Digenea: Apocreadiidae), a parasite of Middle-American cichlids. International Journal for Parasitology 40, 471–486. doi:10.1016/j.ijpara.2009.10.004.CrossRefGoogle ScholarPubMed
Roberts, L. S. and Janovy, J. Jr. (2005). Nematodes: Ascaridida, intestinal large roundworms. In Gerald, D. Schmidt & Larry S. Roberts’ Foundations of Parasitology, 7th Edn (ed. Roberts, L. S. and Janovy, J. Jr.), pp. 431–444. McGraw-Hill, New York, USA.Google Scholar
Shi, X. Q. and Zhou, Z. Y. (1993). Notes on some nematodes of the suborder Ascaris data from Shanghai Zoo. Chinese Journal of Veterinary Medicine 19, 19–20 (in Chinese).Google Scholar
Sorvillo, F., Ash, L. R., Berlin, O. G. W., Yatabe, J. A., Degiorgio, C. and Morse, S. A. (2002). Baylisascaris procyonis: an emerging helminthic zoonosis. Emerging Infectious Diseases 8, 355–359. doi: 10.3201/eid0804.010273.CrossRefGoogle ScholarPubMed
Sprent, J. F. (1968). Notes on Ascaris and Toxascaris, with a definition of Baylisascaris gen. nov. Parasitology 58, 185–198. doi: 10.1017/S0031182000073534.CrossRefGoogle ScholarPubMed
Sprent, J. F. A. (1983). Observations on the systematics of ascaridoid nematodes. In Concepts in Nematode Systematics (ed. Stone, A. R., Platt, H. M. and Khalil, L. F.), pp. 303–319. Academic Press, New York, USA.Google Scholar
Swofford, D. L. (2002). PAUP: Phylogenetic Analysis using Parsimony, Version 4.0 b10. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599. doi: 10.1093/molbev/msm092.CrossRefGoogle ScholarPubMed
Tang, Z. Z. and Tang, C. T. (1987). Ascaridida. In Nematology of Human and Domestic Animals (ed. Tang, Z. Z. and Tang, C. T.), pp. 91–122. Scientific Publisher, Beijing, China. (in Chinese).Google Scholar
Testini, G., Papini, R., Lia, R. P., Parisi, A., Dantas-Torres, F., Traversa, D. and Otranto, D. (2011). New insights into the morphology, molecular characterization and identification of Baylisascaris transfuga (Ascaridida; Ascarididae). Veterinary Parasitology 175, 97–102. doi:10.1016/j.vetpar.2010.09.017.CrossRefGoogle ScholarPubMed
Wickramasinghe, S., Yatawara, L., Rajapakse, R. P. V. J. and Agatsuma, T. (2009). Toxocara canis and Toxocara vitulorum: molecular characterization, discrimination, and phylogenetic analysis based on mitochondrial (ATP synthase subunit 6 and 12S) and nuclear ribosomal (ITS-2 and 28S) genes. Parasitology Research 104, 1425–1430. doi: 10.1007/s00436-009-1345-9.CrossRefGoogle ScholarPubMed
Wu, J., He, G. Z. and Hu, H. G. (1987). Study on a new species of Toxascaris ailuri from Ailurus fulgens . Sichuan Journal of Zoology 2, 1–3 (in Chinese).Google Scholar
Wyngaard, G. A., Holynska, M. and Schulte, J. A. II (2010). Phylogeny of the freshwater copepod Mesocyclops (Crustacea: Cyclopidae) based on combined molecular and morphological data, with notes on biogeography. Molecular Phylogenetics and Evolution 55, 753–764. doi:10.1016/j.ympev.2010.02.029.CrossRefGoogle ScholarPubMed
Xie, Y., Zhang, Z. H., Wang, C. D., Lan, J. C., Li, Y., Chen, Z. G., Fu, Y., Nie, H. M., Yan, N., Gu, X. B., Wang, S. H., Peng, X. R. and Yang, G. Y. (2011). Complete mitochondrial genomes of Baylisascaris schroederi, B. ailuri and B. transfuga from Giant Panda, Red Panda and Polar Bear. Gene 482, 59–67. doi:10.1016/j.gene.2011.05.004.CrossRefGoogle Scholar
Yang, G. Y. and Wang, C. D. (2000), Advances on parasites and parasitic diseases of Ailurus fulgens . Chinese Journal of Veterinary Medicine 26, 36–38 (in Chinese).Google Scholar
Yatawara, L., Wickramasinghe, S., Nagataki, M., Rajapakse, R. and Agatsuma, T. (2007). Molecular characterization and phylogenetic analysis of Setaria digitata of Sri Lanka based on CO1 and 12S rDNA genes. Veterinary Parasitology 148, 161–165. doi:10.1016/j.vetpar.2007.06.005.CrossRefGoogle ScholarPubMed
Zhang, J. S., Daszak, P., Huang, H. L., Yang, G. Y., Kilpatrick, A. M. and Zhang, S. Y. (2008). Parasite threat to panda conservation. EcoHealth 5, 6–9. doi: 10.1007/s10393-007-0139-8.CrossRefGoogle ScholarPubMed