Marine Biology

, Volume 151, Issue 2, pp 695–702 | Cite as

Levels of intra-host and temporal sequence variation in a large CO1 sub-units from Anisakis simplex sensu stricto (Rudolphi 1809) (Nematoda: Anisakisdae): implications for fisheries management

  • M. A. Cross
  • C. Collins
  • N. Campbell
  • P. C. Watts
  • J. C. Chubb
  • C. O. Cunningham
  • E. M. C. Hatfield
  • K. MacKenzie
Research Article

Abstract

This paper is the first to address the suitability and potential of the cytochrome oxidase-1 (CO1) region of the parasitic marine nematode Anisakis simplex sensu stricto as a genetic marker. A. simplex s.s. is an ubiquitous parasite of many marine organisms and has been used as a ‘biological tag’ for population studies of pelagic fish stocks. The CO1 marker informs not only about nematode population structure but also about its hosts. The large CO1 sub-unit (∼800 bp) was analysed from third stage larvae of A. simplex s.s. from Atlantic herring, Clupea harengus L. caught off the north-west coast of Scotland. In total 161 A. simplex s.s.CO1 sequences were analysed from 37 herring that represented three spawning periods over 2 years. Overall very high haplotype and low nucleotide diversities were observed (h = 0.997 and π = 0.008, respectively). These results are in keeping with studies investigating parasitic nematodes of ungulates and are symptomatic of the high rate of substitutions accumulated by mtDNA and effective dispersal strategies of the parasite. The Tamura-Nei I + Г (Г = 1.2243) model of nucleotide substitution best suited the present data which were dominated by a high thymine bias and associated transitions. Large within population differences were highlighted by hierarchal AMOVAs with little variation related to spawning events or years which may indicate localised temporal stability. Temporal homogeneity in the CO1 gene coupled with the ubiquitous and widespread nature of the parasite indicates both the potential and limitations for its incorporation in stock-separation studies of its hosts.

References

  1. Abollo E, Paggi L, Pascual S, D’Amelio S (2003) Occurrence of recombinant genotypes of Anisakis simplex s.s. and Anisakis pegreffii (Nematoda: Anisakidae) in an area of sympatry. Infect Genet Evol 3:175–181PubMedCrossRefGoogle Scholar
  2. Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission. CABI, OxonGoogle Scholar
  3. Anderson TJ, Blouin MS, Beech RN (1998) Population biology of parasitic nematodes: applications of genetic markers. Adv Parasitol 41:219–283PubMedGoogle Scholar
  4. Blouin MS (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int J Parasitol 32:527–531PubMedCrossRefGoogle Scholar
  5. Blouin MS, Dame JB, Tarrant CA, Courtney CH (1992) Unusual population genetics of a parasitic nematode: mtDNA variation within and among populations. Evolution 46:470–476CrossRefGoogle Scholar
  6. Blouin MS, Yowell CA, Courtney CH, Dame JB (1995) Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141:1007–1014PubMedGoogle Scholar
  7. Blouin MS, Yowell CA, Courtney CH, Dame JB (1998) Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics. Mol Biol Evol 15:1719–1727PubMedGoogle Scholar
  8. Brown BL, Epifanio JM, Smouse PE, Kobak CJ (1996) Temporal stability of mtDNA haplotype frequencies in American shad stocks: to pool or not to pool across years? Can J Fish Aquat Sci 53:2274–2283CrossRefGoogle Scholar
  9. D’Amelio S, Mathiopoulos KD, Santos CP (2000) Genetic markers in ribosomal DNA for the identification of members of the genus Anisakis (Nematoda: Ascaridoidea) defined by polymerase-chain reaction-based restriction fragment length polymorphisms. Int J Parasitol 30:223–226PubMedCrossRefGoogle Scholar
  10. Derycke S, Remerie T, Vierstraete A, Backeljau T, Vanfleteren J, Vincx M, Moens T (2005) Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Mar Ecol Prog Ser 300:91–103Google Scholar
  11. Donald KM, Kennedy M, Poulin R, Spencer HG (2004) Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae). Int J Parasitol 34:557–568PubMedCrossRefGoogle Scholar
  12. Folmer O, Black M, Hoeh W, Lutz R, Virjenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 5:294–299Google Scholar
  13. Grygiel W (1999) Synoptic survey of pathological symptoms in herring (Clupea harengus) and sprat (Sprattus sprattus) in the Baltic Sea. ICES J Mar Sci 56:169–174CrossRefGoogle Scholar
  14. Hansen H, Bachmann L, Bakke TA (2003) Mitochondrial DNA variation of Gyrodactylus spp. (Monogenea, Gyrodactylidae) populations infecting Atlantic salmon, grayling, and rainbow trout in Norway and Sweden. Int J Parasitol 33:1471–1478PubMedCrossRefGoogle Scholar
  15. Hu M, Chilton NB, Gasser RB (2002) The mitochondrial genomes of the human hookworms, Ancylostoma duodenale and Necator americanus (Nematoda: Secernentea). Int J Parasitol 32:145–158PubMedCrossRefGoogle Scholar
  16. Hu M, Chilton NB, Abs El-Osta YG, Gasser RB (2003) Comparative analysis of mitrochondrial genome data for Necator americanus from two endemic regions reveals substantial genetic variation. Int J Parasitol 33:955–963PubMedCrossRefGoogle Scholar
  17. Hugall A, Stanton J, Moritz C (1997) Evolution of the AT-rich mitochondrial DNA of the root knot nematode, Meloidogyne hapla. Mol Biol Evol 14:40–48PubMedGoogle Scholar
  18. Hyman B, Azevedo J (1996) Similar evolutionary patterning among repeated and single copy nematode mitochondrial genes. Mol Biol Evol 13:221–232PubMedGoogle Scholar
  19. Kim KH, Eom KS (2006) The complete mitochondrial genome of Anisakis simplex (Ascaridida: Nematoda) and phylogenetic implications. Int J Parasitol 36:319–328PubMedCrossRefGoogle Scholar
  20. Klimpel S, Palm HW, Ruckert S, Piatkowski U (2004) The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea). Parasitol Res 94:1–9PubMedCrossRefGoogle Scholar
  21. MacKenzie K (2002) Parasites as biological tags in population studies of marine organisms: an update. Parasitology 124:S153–S163PubMedCrossRefGoogle Scholar
  22. Martin-Sanchez J, Artacho-Reinoso ME, Diaz-Gavilan M, Valero-Lopez A (2005) Structure of Anisakis simplex s.l. populations in a region sympatric for A-pegreffii and A-simplex s.s. Absence of reproductive isolation between both species. Mol Biochem Parasitol 141:155–162PubMedCrossRefGoogle Scholar
  23. Mattiucci S, D’Amelio S, Rokicki J (1989) Electrophoretic identification of Anisakis sp. larvae (Ascaridida: Anisakidae) from Clupea harengus L. in Baltic Sea. Parassitologia 31:45–49PubMedGoogle Scholar
  24. Mattiucci S, Nascetti G, Tortini E, Ramadori L, Abaunza P, Paggi L (2000) Composition and structure of metazoan parasitic communities of European hake (Merluccius merluccius) from Mediterranean and Atlantic waters: stock implications. Parassitologia 42:176–186Google Scholar
  25. Mattiucci S, Abaunza P, Ramadori L, Nascetti G (2004) Genetic identification of Anisakis larvae in European hake from Atlantic and Mediterranean waters for stock recognition. J Fish Biol 65:495–510CrossRefGoogle Scholar
  26. Mattiucci S, Nascetti G, Dailey M, Webb SC, Barros NB, Cianchi R, Bullini L (2005) Evidence for a new species of Anisakis Dujardin, 1845: morphological description and genetic relationships between congeners (Nematoda: Anisakidae). Syst Parasitol 61:157–171PubMedCrossRefGoogle Scholar
  27. McCoy KD, Bouliner T, Tirard C (2005) Comparative host-parasite population structures: disentangling prospecting and dispersal in the black-legged kittiwake (Rissa tridactyla). Mol Ecol 14:2825–2838PubMedCrossRefGoogle Scholar
  28. McGladdery SE, Burt MDB (1985) Potential of parasites for use as biological indicators of migration, feeding, and spawning behaviour of Northwestern Atlantic Herring (Clupea harengus). Can J Fish Aquat Sci 42:1957–1985Google Scholar
  29. McQuinn IH (1997) Metapopulations and the Atlantic herring. Rev Fish Biol Fish 7:297–329CrossRefGoogle Scholar
  30. Moser M, Hsieh J (1992) Biological tags for stock separation in Pacific Herring Clupea harengus pallasi in California. J Parasitol 78:54–60PubMedCrossRefGoogle Scholar
  31. Mulvey M, Aho JM, Lydeard C, Lebero PL, Smith MH (1991) Comparative populations genetic structure of a parasite (Fascioloides magna) and its definitive host. Evolution 45:1628–1640CrossRefGoogle Scholar
  32. Nascetti G, Paggi L, Orecchia P, Smith JW, Mattiucci S, Bullini L (1986) Electrophoretic studies on the Anisakis simplex complex (Ascaridida: Anisakidae) from the Mediterranean and North–East Atlantic. Int J Parasitol 16:633–640PubMedCrossRefGoogle Scholar
  33. Nieberding C, Morand S, Libois R, Michaux JR (2004) A parasite reveals cryptic phylogeographic history of its host. Proc Biol Sci 271:2559–2568PubMedCrossRefGoogle Scholar
  34. Papetti C, Zane L, Bortolotto E, Bucklin A, Patarnello T (2005) Genetic differentiation and local temporal stability of population structure in the euphausiid Meganyctiphanes norvegica. Mar Ecol Prog Ser 289:225–235Google Scholar
  35. Peng W, Anderson TJC, Zhou B, Kennedy MW (1998) Genetic variation in sympatric Ascaris populations from humans and pigs in China. Parasitology 117:355–361PubMedCrossRefGoogle Scholar
  36. Posada D, Crandall KD (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  37. Rozen S, Skaletsky HJ (2000) Primer 3 on the WWW for general users and for biologist programmers. In: Misener KS (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, TotowaGoogle Scholar
  38. Sabater EIL, Sabater CJL (2000) Health hazards related to occurrence of parasites of the genera Anisakis and Pseudoterranova in fish. Food Sci Technol Int 6:183–195Google Scholar
  39. Schneider S, Roessli D, Excoffier L (2001) ARLEQUIN, version 2.001: a software for population genetics data analysis. Genetics and Biometry Laboratory, Department of Anthropology. University of Geneva, SwitzerlandGoogle Scholar
  40. Smith JW, Wootten R (1978) Anisakis and Anisakiasis. Adv Parasitol 16:93–163PubMedCrossRefGoogle Scholar
  41. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in Humans and Chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  42. van Thiel PH (1962) Anisakiasis. Parasitology 52:16–17Google Scholar
  43. Tolonen A, Karlsbakk E (2003) The parasite fauna of the Norwegian spring spawning herring (Clupea harengus L.). ICES J Mar Sci 60:77–84CrossRefGoogle Scholar
  44. Walsh SP, Metzger DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513PubMedGoogle Scholar
  45. Zhan B, Li T, Xiao S, Zheng F, Hawdon JM (2001) Species–specific identification of human hookworms by PCR of the mitochondrial cytochrome oxidase I gene. J Parasitol 87:1227–1229PubMedGoogle Scholar
  46. Zhu XQ, Spratt DM, Beveridge I, Haycock P, Gasser RB (2000) Mitochondrial DNA polymorphism within and among species of Capillaria sensu lato from Australian marsupials and rodents. Int J Parasitol 30:933–938PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • M. A. Cross
    • 1
    • 3
  • C. Collins
    • 2
  • N. Campbell
    • 2
    • 4
  • P. C. Watts
    • 3
  • J. C. Chubb
    • 3
  • C. O. Cunningham
    • 2
  • E. M. C. Hatfield
    • 2
  • K. MacKenzie
    • 4
  1. 1.Biological Sciences InstituteUniversity of DundeeDundeeScotland, UK
  2. 2.FRS Marine LaboratoryAberdeenScotland, UK
  3. 3.School of Biological Sciences, Biosciences BuildingLiverpool UniversityLiverpoolUK
  4. 4.School of Biological Sciences (Zoology)University of AberdeenAberdeenScotland, UK

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