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Fisheries Science

, Volume 80, Issue 3, pp 463–474 | Cite as

Analysis of the genetic structure of the European eel Anguilla anguilla using the mtDNA D-loop region molecular marker

  • Adomas Ragauskas
  • Dalius Butkauskas
  • Aniolas Sruoga
  • Vytautas Kesminas
  • Isaak Rashal
  • Wann-Nian Tzeng
Original Article Biology

Abstract

Sequence variation of the mtDNA D-loop region was analyzed in order to investigate the intraspecific evolution and the population genetic structure of the critically endangered European eel Anguilla anguilla. An additional attempt was made to collect information on the genetic characteristics of groups of eels representing naturally recruited eels to Lithuania and Latvia and introduced into Lithuanian lakes. A total of 148 eels were investigated, and 107 different haplotypes attributed to 39 haplogroups were determined during the study. A dataset comprising 229 sequences was created using the data from both this study and from earlier studies (n = 81). Analysis of this dataset revealed that haplotype diversity was 0.99567, the average number of nucleotide differences was 12.50544, there were 145 polymorphic sites and nucleotide diversity was 0.02426. No significant genetic differentiation was detected between different combinations of samples. However, the population genetic structure of this species could be characterized as a genetic mosaic formed due to the existence of reproductively isolated groups. The existence of a genetic mosaic in this species could be explained by the different evolutionary lineages found in the eel population.

Keywords

Anguilla anguilla D-loop Genetic diversity Haplotype Haplogroup Panmixia Restocking 

Notes

Acknowledgments

The authors want to express their gratitude to two anonymous reviewers for their help in improving the quality of the manuscript. The authors also are grateful to the Lithuania–Latvia–Taiwan (Republic of China) mutual fund for financial support for joint research projects between the countries. Sincere gratitude goes to the Lithuanian State Studies Foundation and the Research Council of Lithuania for providing PhD scholarships in support of this study. Special thanks go to Dr. Linas Ložys and fishermen Sigitas and Virgis for kindly providing the eel samples.

References

  1. 1.
    Maes GE, Volckaert FAM (2007) Challenges for genetic research in European eel management. ICES J Mar Sci 64:1463–1471CrossRefGoogle Scholar
  2. 2.
    Tsukamoto K, Aoyama J, Miller MJ (2002) Migration, speciation, and the evolution of diadromy in anguillid eels. Can J Fish Aquat Sci 59:1989–1998CrossRefGoogle Scholar
  3. 3.
    McCleave JD (2008) Contrasts between spawning times of Anguilla species estimated from larval sampling at sea and from otolith analysis of recruiting glass eels. Mar Biol 155:249–262CrossRefGoogle Scholar
  4. 4.
    Huertas M, Cerdà J (2006) Stocking density at early developmental stages affects growth and sex ratio in the European eel (Anguilla anguilla). Biol Bull 211:286–296PubMedCrossRefGoogle Scholar
  5. 5.
    Trautner J (2006) Rapid identification of European (Anguilla anguilla) and North American eel (Anguilla rostrata) by polymerase chain reaction. Inf Fischereiforsch 53:49–51Google Scholar
  6. 6.
    Edeline E (2007) Adaptive phenotypic plasticity of eel diadromy. Mar Ecol Prog Ser 341:229–232CrossRefGoogle Scholar
  7. 7.
    Tsukamoto K, Arai T (2001) Facultative catadromy of the eel Anguilla japonica between freshwater and seawater habitats. Mar Ecol Prog Ser 220:265–276CrossRefGoogle Scholar
  8. 8.
    Avise JC, Helfman GS, Saunders NC, Hales LS (1986) Mitochondrial DNA differentiation in North Atlantic eels: population genetic consequences of an unusual life history pattern. Proc Natl Acad Sci USA 83:4350–4354PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Van Ginneken VJT, Maes GE (2005) The European eel (Anguilla anguilla, Linnaeus), its lifecycle, evolution and reproduction: a literature review. Rev Fish Biol Fish 15:367–398CrossRefGoogle Scholar
  10. 10.
    Daemen E, Cross T, Ollevier F, Volckaert FAM (2001) Analysis of the genetic structure of European Eel (Anguilla anguilla) using microsatellite DNA and mtDNR markers. Mar Biol 139:755–764CrossRefGoogle Scholar
  11. 11.
    Butkauskas D, Ragauskas A, Sruoga A, Ložys L, Tzeng W-N (2009) Current knowledge about European eel Anguilla anguilla (L.) mtDNA D-loop region haplotypic variety. Acta Zool Litu 19:253–267CrossRefGoogle Scholar
  12. 12.
    Kettle AJ, Haines K (2006) How does the European eel (Anguilla anguilla) retain its population structure during its larval migration across the North Atlantic Ocean? Can J Fish Aquat Sci 63:90–106CrossRefGoogle Scholar
  13. 13.
    Friedland KD, Miller MJ, Knights B (2007) Oceanic changes in the Sargasso Sea and declines in recruitment of the European eel. ICES J Mar Sci 64:519–530CrossRefGoogle Scholar
  14. 14.
    Bonhommeau S, Chassot E, Rivot E (2008) Fluctuations in European eel (Anguilla anguilla) recruitment resulting from environmental changes in the Sargasso Sea. Fish Oceanogr 17:32–44CrossRefGoogle Scholar
  15. 15.
    Durif C, Dufour S, Elie P (2005) The silvering process of Anguilla anguilla: a new classification from the yellow resident to the silver migrating stage. J Fish Biol 66:1–19CrossRefGoogle Scholar
  16. 16.
    Maes GE, Pujolar JM, Hellemans B, Volckaert FAM (2006) Evidence for isolation by time in the European eel (Anguilla anguilla L.). Mol Ecol 15:2095–2107PubMedCrossRefGoogle Scholar
  17. 17.
    Gagnaire PA, Albert V, Jónsson B, Bernatchez L (2009) Natural selection influences AFLP intraspecific genetic variability and introgression patterns in Atlantic eels. Mol Ecol 18:1678–1691PubMedCrossRefGoogle Scholar
  18. 18.
    Palm S, Dannewitz J, Prestegaard T, Wickström H (2009) Panmixia in European eel revisited: no genetic difference between maturing adults from southern and northern Europe. Heredity 103:82–89PubMedCrossRefGoogle Scholar
  19. 19.
    Daverat F, Limburg KE, Thibault I, Shiao JC, Dodson JJ, Caron F et al (2006) Phenotypic plasticity of habitat use by three temperate eel species, Anguilla anguilla, A. japonica and A. rostrata. Mar Ecol Prog Ser 308:231–241CrossRefGoogle Scholar
  20. 20.
    Westerberg H, Lagenfelt I, Svedäng H (2007) Silver eel migration behaviour in the Baltic. ICES J Mar Sci 64:1457–1462CrossRefGoogle Scholar
  21. 21.
    Avise JC (2011) Catadromous eels continue to be slippery research subjects. Mol Ecol 20:1317–1319PubMedCrossRefGoogle Scholar
  22. 22.
    Bark A, Williams B, Knights B (2007) Current status and temporal trends in stocks of European eel in England and Wales. ICES J Mar Sci 64:1368–1378CrossRefGoogle Scholar
  23. 23.
    Winter HV, Jansen HM, Breukelaar AW (2007) Silver eel mortality during downstream migration in the River Meuse, from a population perspective. ICES J Mar Sci 64:1444–1449CrossRefGoogle Scholar
  24. 24.
    Bevacqua D, Melià P, Crivelli AJ, Gatto M, De Leo GA (2007) Multi-objective assessment of conservation measures for the European eel (Anguilla anguilla): an application to the Camargue lagoons. ICES J Mar Sci 64:1483–1490CrossRefGoogle Scholar
  25. 25.
    Åström M, Dekker W (2007) When will the eel recover? A full life-cycle model. ICES J Mar Sci 64:1491–1498CrossRefGoogle Scholar
  26. 26.
    Jonsson B, Waples RS, Friedland KD (1999) Extinction considerations for diadromous fishes. ICES J Mar Sci 56:405–409CrossRefGoogle Scholar
  27. 27.
    Cucherousset J, Paillisson J-M, Carpentier A, Thoby V, Damien J-P, Eybert M-C et al (2007) Freshwater protected areas: an effective measure to reconcile conservation and exploitation of the threatened European eels (Anguilla anguilla)? Ecol Freshw Fish 16:528–538CrossRefGoogle Scholar
  28. 28.
    Simon J, Dörner H, Richter C (2009) Growth and mortality of European glass eel Anguilla anguilla marked with oxytetracycline and alizarin red. J Fish Biol 74:289–295PubMedCrossRefGoogle Scholar
  29. 29.
    Limburg KE, Wickström H, Svedäng H, Elfman M, Kristiansson P (2003) Do stocked freshwater eels migrate? Evidence from the Baltic suggest “yes”. Am Fish Soc Symp 33:275–284Google Scholar
  30. 30.
    Westin L (2003) Migration failure in stocked eels Anguilla anguilla. Mar Ecol Prog Ser 254:307–311CrossRefGoogle Scholar
  31. 31.
    Samuilovienė A, Kontautas A (2012) Population genetics of Atlantic salmon and brown trout and its revelance for management of genetic resources. Ekologija 58:427–441Google Scholar
  32. 32.
    Wirth T, Bernatchez L (2001) Genetic evidence against panmixia in the European eel. Nature 409:1037–1040PubMedCrossRefGoogle Scholar
  33. 33.
    Vasemägi A (2009) Eel mystery: time makes a difference. Heredity 103:3–4. doi: 10.1038/hdy.2009.38 Google Scholar
  34. 34.
    Dannewitz J, Maes GE, Johansson L, Wickström H, Volckaert FAM, Järvi T (2005) Panmixia in the European eel: a matter of time. Proc R Soc 272:1129–1137CrossRefGoogle Scholar
  35. 35.
    Als TD, Hansen MM, Maes GE, Castonguay M, Riemann L, Aarestrup K et al (2011) All roads lead to home: panmixia of European eel in the Sargasso Sea. Mol Ecol 20:1333–1346. doi: 10.1111/j.1365-294X.2011.05011.x Google Scholar
  36. 36.
    Cagnon C, Lauga B, Karama S, Mouches C (2011) Temporal genetic variation in European eel Anguilla anguilla (Linnaeus, 1758): a fine scale investigation in the Adour estuary. Mar Biol Res 7:515–519CrossRefGoogle Scholar
  37. 37.
    Pujolar JM, Bevacqua D, Andrello M, Capoccioni F, Ciccotti E, De Leo GA et al (2011) Genetic patchiness in European eel adults evidenced by molecular genetics and population dynamics modelling. Mol Phylogenet Evol 58:198–206PubMedCrossRefGoogle Scholar
  38. 38.
    Lintas C, Hirano J, Archer S (1998) Genetic variation of the European eel (Anguilla anguilla). Mol Mar Biol Biotechnol 7:263–269PubMedGoogle Scholar
  39. 39.
    Shiao J-C, Ložys L, Iizuka Y, Tzeng W-N (2006) Migratory patterns and contribution of stocking to the population of European eel in Lithuanian waters as indicated by otolith Sr:Ca ratios. J Fish Biol 69:749–769CrossRefGoogle Scholar
  40. 40.
    Lin Y-J, Ložys L, Shiao J-C, Iizuka Y, Tzeng W-N (2007) Growth differences between naturally recruited and stocked European eel Anguilla anguilla from different habitats in Lithuania. J Fish Biol 71:1773–1787CrossRefGoogle Scholar
  41. 41.
    Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  44. 44.
    Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  45. 45.
    Lynch M, Crease TJ (1990) The analysis of population survey data on DNA sequence variation. Mol Biol Evol 7:377–394PubMedGoogle Scholar
  46. 46.
    Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460PubMedCentralPubMedGoogle Scholar
  47. 47.
    Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589PubMedCentralPubMedGoogle Scholar
  48. 48.
    Hudson RR, Boos DD, Kaplan NL (1992) A statistical test for detecting population subdivision. Mol Biol Evol 9:138–151PubMedGoogle Scholar
  49. 49.
    Rozas J, Sánchez-Delbarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  50. 50.
    Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  51. 51.
    Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedCrossRefGoogle Scholar
  52. 52.
    Polzin T, Daneshmand SV (2003) On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 31:12–20CrossRefGoogle Scholar
  53. 53.
    Kettle AJ, Vøllestad LA, Wibig J (2011) Where once the eel and the elephant were together: decline of the European eel because of changing hydrology in southwest Europe and northwest Africa? Fish Fish 12:380–411. doi: 10.1111/j.1467-2979.2010.00400.x Google Scholar
  54. 54.
    Minegishi Y, Aoyama J, Inoue JG, Miya M, Nishida M, Tsukamoto K (2005) Molecular phylogeny and evolution of the freshwater eels genus Anguilla based on the whole mitochondrial genome sequences. Mol Phylogenet Evol 34:134–146PubMedCrossRefGoogle Scholar
  55. 55.
    Ishikawa S, Aoyama J, Tsukamoto K, Nishida M (2001) Population structure of the Japanese eel Anguilla japonica as examined by mitochondrial DNA sequencing. Fish Sci 67:246–253CrossRefGoogle Scholar
  56. 56.
    Donovan S, Pezold F, Chen Y, Lynch B (2012) Phylogeography of Anguilla marmorata (Teleostei: Anguilliformes) from the eastern Caroline Islands. Ichthyol Res 59:70–76CrossRefGoogle Scholar
  57. 57.
    Tseng MC, Kao HW, Hung YH, Lee TL (2012) A study of genetic variations, population size, and population dynamics of the catadromous Japanese eel Anguilla japonica (Pisces) in northern Taiwan. Hydrobiologia 683:203–216CrossRefGoogle Scholar
  58. 58.
    Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362CrossRefGoogle Scholar
  59. 59.
    Andrello M, Bevacqua D, Maes GE, De Leo GA (2011) An integrated genetic-demographic model to unravel the origin of genetic structure in European eel (Anguilla anguilla L.). Evol Appl 4:517–533PubMedCentralCrossRefGoogle Scholar
  60. 60.
    Selkoe KA, Watson JR, White C, Horin TB, Iacchei M, Mitarai S et al (2010) Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Mol Ecol 19:3708–3726PubMedCrossRefGoogle Scholar
  61. 61.
    Hedgecock D, Pudovkin AI (2011) Sweepstakes reproductive success in highly fecund marine fish and shellfish: a review and commentary. Bull Mar Sci 87:971–1002CrossRefGoogle Scholar
  62. 62.
    Kettle AJ, Heinrich D, Barrett JH, Benecke N, Locker A (2008) Past distributions of the European freshwater eel from archaeological and palaeontological evidence. Quat Sci Rev 27:1309–1334CrossRefGoogle Scholar
  63. 63.
    Smedbol RK, McPherson A, Hansen MM, Kenchington E (2002) Myths and moderation in marine “metapopulations”? Fish Fish 3:20–35CrossRefGoogle Scholar
  64. 64.
    Dekker W (2000) A Procrustean assessment of the European eel stock. ICES J Mar Sci 57:938–947CrossRefGoogle Scholar

Copyright information

© The Japanese Society of Fisheries Science 2014

Authors and Affiliations

  • Adomas Ragauskas
    • 1
  • Dalius Butkauskas
    • 1
  • Aniolas Sruoga
    • 1
    • 2
  • Vytautas Kesminas
    • 1
  • Isaak Rashal
    • 3
  • Wann-Nian Tzeng
    • 4
  1. 1.Nature Research CentreVilniusLithuania
  2. 2.Vytautas Magnus UniversityKaunasLithuania
  3. 3.Institute of BiologyUniversity of LatviaSalaspilsLatvia
  4. 4.Department of Life Science and Institute of Fisheries ScienceNational Taiwan UniversityTaipeiTaiwan, ROC

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