Advertisement

Parasitology Research

, Volume 113, Issue 7, pp 2455–2466 | Cite as

Phylogenetic relationships between pinworms (Nematoda: Enterobiinae) parasitising the critically endangered orang-utan, according to the characterisation of molecular genomic and mitochondrial markers

  • Ivona FoitováEmail author
  • Kristína Civáňová
  • Vlastimil Baruš
  • Wisnu Nurcahyo
Original Paper

Abstract

Pinworms (Nematoda: Enterobiinae) include 52 species parasitising primates throughout the world. In the present study, we performed the first ever molecular analysis to investigate the phylogenetic position of recently described pinworms parasitising the Sumatran orang-utan. The phylogenetic analysis of mitochondrial CO1 and chromosomal 18S rDNA and ITS1 regions could support the independent status of several Nematoda species. Our molecular data clearly suggest that Enterobius (Colobenterobius) buckleyi and Lemuricola (Protenterobius) pongoi together with Pongobius hugoti form separate clades among other studied species, which significantly supports the hypothesis of recently described new species parasitising the orang-utan (Pongo abelii and Pongo pygmaeus). The phylogenetic tree based on cytochrome oxidase 1 (CO1) gene variability showed possible close relationships between L. (Protenterobius) pongoi and P. hugoti; thus, we can assume that these species could have initially diverged in sympatry from a common ancestor.

Keywords

Molecular phylogeny Cytochromoxidase 1 18S rDNA ITS1 Orang-utan pinworms Pongo abelii 

Notes

Acknowledgements

The authors would like to thank the State Ministry of Research and Technology (RISTEK) and the Directorate for General for Natural Conservation (PHKA) for their cooperation and for their permission to conduct research in the Gunung Leuser National Park. The study was financially supported by the UMI—Saving of Pongidae Foundation project “Parasites and Natural Antiparasitics in the Orang-utan” and by the Czech Academy of Sciences, grant no. P505/11/1163. We thank Dr. Mrkvicová Martina for help with molecular analysis and Dr. Tóthová Andrea for providing the Bayesian analysis and phylogenetic consultations. We are grateful to Matthew Nicholls for English correction of the draft.

References

  1. Baruš V, Foitová I, Koubková B, Hodová I, Šimková A, Nurcahyo W (2007) A new nematode, Pongobius hugoti gen. et sp. n. from the orangutan Pongo abelii (Primates: Hominidae). Helminthologia 44:162–169CrossRefGoogle Scholar
  2. Blouin MS (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int J Parasitol 32:527–531PubMedCrossRefGoogle Scholar
  3. Brooks D (1982) Pinworms and primates: a case study of coevolution. Proc Helminthol Soc Wash 49:76–85Google Scholar
  4. Cameron TWM (1929) The species of Enterobius Leach in primates. J Helminthol 7:161–182CrossRefGoogle Scholar
  5. Chabaud AG, Petter AJ (1959) Les Nématodes parasites de Lémuriens Malgaches II. Un nouvel Oxyure: Lemuricola contagiosus. Mém Institut Sci Madagascar 13:127–132Google Scholar
  6. Chabaud AG, Petter AJ, Golvan Y (1961) Les Nématodes parasites de Lémuriens Malgaches III. Collection récoltée par M. et Mme Francis Petter. Ann Parasitol Hum Comp 36:113–126PubMedGoogle Scholar
  7. Floyd RMA, Rogers D, Lambshead JD, Smith CR (2005) Nematode-specific PCR primers for the 18S small subunit rRNA gene. Mol Ecol Notes 5:611–612CrossRefGoogle Scholar
  8. Foitová I, Baruš V, Hodová I, Koubková B, Nurcahyo W (2008) Two remarkable pinworms (Nematoda: Enterobiinae) parasitizing orangutan (Pongo abelii) in Sumatra (Indonesia). Helminthologia 45:162–168CrossRefGoogle Scholar
  9. Foitová I, Baruš V, Koubková B, Mašová Š, Nurcahyo W (2010) Description of Lemuricola (Lemuricola) pongoi–male (Nematoda: Enterobiinae) parasitizing orangutan (Pongo abelii). Parasitol Res 106:817–820PubMedCrossRefGoogle Scholar
  10. Glen DR, Brooks DR (1986) Parasitological evidence pertaining to the phylogeny of the hominoid primates. Biol J Linn Soc Lond 27:331–354CrossRefGoogle Scholar
  11. Gonzáles-Moreno O, Domingo L, Teixidor J, Gracenae M (2011) Prevalence and associated factors of intestinal parasitisation: a cross-sectional study among outpatients with gastrointestinal symptoms in Catalonia, Spain. Parasitol Res 108:87–93CrossRefGoogle Scholar
  12. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41:95–98Google Scholar
  13. Hasegawa H (1999) Phylogeny, host–parasite relationship and zoogeography. Korean J Parasitol 37:197–213PubMedCentralPubMedCrossRefGoogle Scholar
  14. Hasegawa H, Matsuo K, Onuma M (2003) Enterobius (Colobenterobius) serratus sp. nov. (Nematoda: Oxyuridae) from the Proboscis Monkey, Nasalis larvatus (Wurmb, 1787) (Primates: Cercopithecidae: Colobinae), in Sarawak, Borneo, Malaysia. Comp Parasitol 70:128–131CrossRefGoogle Scholar
  15. Hasegawa H, Ikeda Y, Diaz-Aquino DJJ, Fukui D (2004) Redescription of two pinworms from the black-handed spider monkey, Ateles geoffroyi, with reestablishment of Oxyuronema and Buckleyenterobius (Nematoda: Oxyuroidea). Comp Parasitol 71:166–174CrossRefGoogle Scholar
  16. Hasegawa H, Ikeda Y, Fujisaki A, Moscovice LR, Petrželková KJ, Kaur T, Huffman MA (2005) Morphology of chimpanzee pinworms, Enterobius (Enterobius) anthropopitheci (Gedoelst, 1916) (Nematoda: Oxyuridae), collected from Chimpanzees, Pan troglodytes, on Rubondo Island, Tanzania. J Parasitol 91:1314–1317PubMedCrossRefGoogle Scholar
  17. Huelsenbeck JP, Ronquist FR (2001) MrBayes: Bayesian inference of phylogeny. Biometrics 17:754–755Google Scholar
  18. Hugot JP (1984a) Sur le genre Trypanoxyuris (Oxyuridae, Nematoda): I. Parasites de Sciuridés: sous-genre Rodentoxyuris. Bull Mus Natl Hist Nat Sér A Zool 6:711–720Google Scholar
  19. Hugot JP (1984b) Sur le genre Trypanoxyuris (Oxyuridae, Nematoda) II. Sous-genre Hapaloxyuris parasites de Primates Callitrichidae. Bull Mus Natl Hist Nat Sér A Zool 6:1007–1019Google Scholar
  20. Hugot JP (1987) Sur le genre Enterobius (Oxyuridae, Nematoda): s.g. Colobenterobius I. Parasites de Primates Colobinae en region Éthiopienne. Bull Mus Natl Hist Nat Sér A Zool 9:341–352Google Scholar
  21. Hugot JP (1999) Primates and their pinworm parasites: Cameron hypothesis revisited. Syst Biol 48:523–546PubMedCrossRefGoogle Scholar
  22. Hugot JP, Baylac M (2007) Shape patterns of genital papillae in pinworms (Enterobiinae, Oxyurida, Nematoda) parasite of primates: a landmark analysis. Inf Gen Evol 7:168–179CrossRefGoogle Scholar
  23. Hugot JP, Morand S, Gardner SL (1995) Morphology and morphometrics of three oxyurids parasitic in primates with a description of Lemuricola microcebi n. sp. Int J Parasitol 25:1065–1075PubMedCrossRefGoogle Scholar
  24. Hugot JP, Gardner SL, Morand S (1996) The Enterobiinae subfam. nov. (Nematoda, Oxyurida) pinworm parasites of primates and rodents. Int J Parasitol 26:147–159PubMedCrossRefGoogle Scholar
  25. Inglis WG (1961) The oxyurids parasites (Nematoda) of primates. P Zool Soc Lond 136:103–122CrossRefGoogle Scholar
  26. Inglis WG, Dunn FL (1963) The occurrence of Lemuricola (Nematoda: Oxyurida) in Malaya: with the description of a new species. Z Parasitenk 23:354–359PubMedCrossRefGoogle Scholar
  27. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  28. Kuze N, Kanamori T, Malim TP, Bernard H, Zamma K, Kooriyma T, Morimoto A, Hasegawa H (2010) Parasites found from the feces of Bornean Orangutans in Danum Valley, Sabah, Malaysia, with a redescription of Pongobius hugoti and the description of a new species of Pongobius (Nematoda: Oxyuridae). J Parasitol 96:954–960PubMedCrossRefGoogle Scholar
  29. Nakano T, Okamoto M, Ikeda Y, Hasegawa H (2006) Mitochondrial cytochrome c oxidase subunit 1 gene and nuclear rDNA regions of Enterobius vermicularis parasitic in captive chimpanzees with special reference to its relationship with pinworms in humans. Parasitol Res 100:51–57PubMedCrossRefGoogle Scholar
  30. Nylander JAA (2004) MrModeltest 2.2. Program distributed by the author. Evolutionary Biology Centre Uppsala UniversityGoogle Scholar
  31. Petter AJ, Chabaud AG, Delavenay R, Brygoo ER (1972) Une nouvelle espéce de Nématode du genre Lemuricola, parasite de Daubentonia madagascariensis Gmelin, et considérations sur le genre Lemuricola. Ann Parasitol Hum Comp 47:391–398PubMedGoogle Scholar
  32. Quentin JC, Tenora F (1975) Morphologie et position systématique de Lemuricola (Rodentoxyuris) sciuri (Cameron, 1933) nov. comb., nov. subg., et Syphacia (Syphatineria) funambuli Johnson, 1967. Oxyures (Nematoda) parasites de Rongeurs Sciurides. Bull Mus Natl Hist Natl Ser A Zool 178:1525–1535Google Scholar
  33. Quentin JC, Betterton C, Krishnasamy M (1979) Oxyures nouveaux ou peu connus, parasites, de Primates, de Rongeurs et de Dermoptères en Malaisie. Création du sous-genre Colobenterobius n. subgen. Bull Mus Natl Hist Nat Sér A Zool 1:1031–1050Google Scholar
  34. Remm M (2006) Distribution of enterobiasis among nursery school children in SE Estonia and of other helminthiases in Estonia. Parasitol Res 99:729–736PubMedCrossRefGoogle Scholar
  35. Rim HJ, Chai JY, Min DY, Cho SY, Eom KS, Hong SJ, Sohn WM, Yong TS, Deodato G, Standgaard H, Phommasack B, Yun CH, Hoang EH (2003) Prevalence of intestinal parasite infections on a national scale among primary schoolchildren in Laos. Parasitol Res 91:267–272PubMedCrossRefGoogle Scholar
  36. Sandosham AA (1950) On Enterobius vermicularis (Linnaeus, 1758) and some related species from primates and rodents. J Helminthol 24:171–204CrossRefGoogle Scholar
  37. Song HJ, Cho CH, Kim JS, Choi MH, Hong ST (2003) Prevalence and risk factors for enterobiasis among preschool children in a metropolitan city in Korea. Parasitol Res 91:46–50PubMedCrossRefGoogle Scholar
  38. Sorci G, Morand S, Hugot JP (1997) Host parasites coevolution: comparative evidence for covariation of life history traits in primates and oxyurid parasites. P Zool Soc Lond 264:285–289Google Scholar
  39. 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. Mol Biol Evol 28(10):2731–2739PubMedCentralPubMedCrossRefGoogle Scholar
  40. Wägele JW, Mayer C (2007) Visualizing differences in phylogenetic information content of alignments and distinction of three classes of long-branch effects. BMC Evol Biol 7:147PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Ivona Foitová
    • 1
    Email author
  • Kristína Civáňová
    • 1
  • Vlastimil Baruš
    • 2
  • Wisnu Nurcahyo
    • 3
  1. 1.Department of Botany and ZoologyMasaryk UniversityBrnoCzech Republic
  2. 2.Institute of Vertebrate BiologyCzech Academy of SciencesBrnoCzech Republic
  3. 3.Department of Parasitology, Faculty of Veterinary MedicineGadjah Mada UniversityYogyakartaIndonesia

Personalised recommendations