Conservation Genetics

, Volume 12, Issue 3, pp 813–825 | Cite as

No apparent genetic bottleneck in the demographically declining European eel using molecular genetics and forward-time simulations

  • J. M. Pujolar
  • D. Bevacqua
  • F. Capoccioni
  • E. Ciccotti
  • G. A. De Leo
  • L. Zane
Research Article


The stock of the European eel is considered to be outside safe biological limits, following a dramatic demographic decline in recent decades (90–99% drop) that involves a large number of factors including overfishing, contaminants and environmental fluctuations. The aim of the present study is to estimate the effective population size of the European eel and the possible existence of a genetic bottleneck, which is expected during or after a severe demographic crash. Using a panel of 22 EST-derived microsatellite loci, we found no evidence for a genetic bottleneck in the European eel as our data showed moderate to high levels of genetic diversity, no loss of allele size range or rare alleles, and a stationary population with growth values not statistically different from zero, which is confirmed by finding comparable value of short-term and long-term effective population size. Our results suggest that the observed demographic decline in the European eel did not entail a genetic decline of the same magnitude. Forward-time simulations confirmed that large exploited marine fish populations can undergo genetic bottleneck episodes and experience a loss of genetic variability. Simulations indicated that the failure to pick up the signal of a genetic bottleneck in the European eel is not due to lack of power. Although anthropogenic factors lowered the continental stock biomass, the observation of a stable genetic effective population size suggests that the eel crash was not due to a reduction in spawning stock abundance. Alternatively, we propose that overfishing, pollution and/or parasites might have affected individual fitness and fecundity, leading to an impoverished spawning stock that may fail to produce enough good quality eggs. A reduced reproduction success due to poor quality of the spawners may be exacerbated by oceanic processes inducing changes in primary production in the Sargasso Sea and/or pathway of transport across the Atlantic Ocean leading to a higher larval mortality.


Anguilla anguilla Bottleneck Effective population size European eel Forward-time simulations 



This work has been funded by an Italian Research Program grant to LZ and by the University of Padova grant CPDA 085158/08 to LZ. We thank the CNR Lesina, the Parco Nazionale del Circeo and the Tiber fishers for support in sampling.

Supplementary material

10592_2011_188_MOESM1_ESM.doc (84 kb)
Supplementary material 1 (DOC 83 kb)


  1. Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337PubMedCrossRefGoogle Scholar
  2. Anderson EC, Garza JC (2009) Estimation of population size with molecular genetic data. NOAA Tech. Mem. NMFS-SWFSC-448Google Scholar
  3. Andrello M, Bevacqua D, Maes GE, De Leo GA (2010) An integrated genetic-demographic model to unravel the origin of genetic-structure in European eel (Anguilla anguilla). Evol Appl. doi: 10.1111/j.1752-4571.2010.00167.x
  4. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN—a workbench to detect molecular adaptation based on a FST-outlier method. BMC Bioinform 9:323CrossRefGoogle Scholar
  5. Ashley MV, Wilson MF, Pergams ORW, O’Dowd DJ, Gende SM, Brown JS (2003) Evolutionarily enlightened management. Biol Conserv 111:115–123CrossRefGoogle Scholar
  6. Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029PubMedGoogle Scholar
  7. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and population effective sizes in n subpopulations using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568PubMedCrossRefGoogle Scholar
  8. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France)Google Scholar
  9. Belpaire C, Goemans G, Geeraerts C, Quataert P, Parmentier K, Hagel P, de Boer J (2009) Decreasing eel stocks: survival of the fattest? Ecol Freshw Fish 18:197–214CrossRefGoogle Scholar
  10. Bevacqua D, De Leo GA, Gatto M, Melià M, Crivelli AJ (2009) A long term study on eel population in the Camargue lagoon, Southern France. Presented to “Workshop on Eel in Saline Waters”, 4–7 Sep 2009, University of Göteborg, SwedenGoogle Scholar
  11. 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
  12. Chikhi L, Sousa VC, Luisi P, Goossens B, Beaumont MA (2010) The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics (in press) doi: 10.1534/genetics.110.118661
  13. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  14. Dannewitz J, Maes GE, Johansson L, Wickström H, Volckaert FAM, Jarvi T (2005) Panmixia in the European eel: a matter of time. Proc R Soc Lond B Biol Sci 272:1129–1137CrossRefGoogle Scholar
  15. Dekker W (2000) A Procrustean assessment of the European eel stock. ICES J Mar Sci 57:938–947CrossRefGoogle Scholar
  16. Dekker W (2003) Did lack of spawners cause the collapse of the European eel Anguilla anguilla? Fish Manage Ecol 10:365–376CrossRefGoogle Scholar
  17. Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of single-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170PubMedCrossRefGoogle Scholar
  18. ICES (2008) Report of the Working Group on Eels (WGEEL), 3–9 September 2008, Leuven, Belgium. ICES CM 2008/ACFM:15, International Council for the Exploration of the Seas, Copenhagen, DenmarkGoogle Scholar
  19. ICES (2009) Report of the Working Group on Eels (WGEEL), 7–12 September 2009, Göteborg, Sweden. ICES CM 2009/ACFM:xx, International Council for the Exploration of the Seas, Copenhagen, DenmarkGoogle Scholar
  20. Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327PubMedCrossRefGoogle Scholar
  21. Franklin JR (1980) Evolutionary change in small populations. In: Soulé ME, Wilcox BA (eds) Conservation biology: an evolutionary-ecological perspective. Sinuer, Sunderland, pp 135–150Google Scholar
  22. Fraser DJ, Hansen MM, Ostergaard S, Tessier N, Legault M, Bernatchez L (2007) Comparative estimation of effective population sizes and temporal gene flow in two contracting population systems. Mol Ecol 16:3866–3889PubMedCrossRefGoogle Scholar
  23. Friedland KD, Miller MI, 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
  24. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318PubMedCrossRefGoogle Scholar
  25. Goudet J (2002) FSTAT version Available from:
  26. Guinand B, Scribner KT (2003) Evaluation of methodology for detection of genetic bottlenecks: inferences from temporally replicated lake trout populations. C R Biol 326:S61–S67PubMedCrossRefGoogle Scholar
  27. Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362Google Scholar
  28. Hauser L, Adcock GJ, Smith PJ, Bernal Ramirez JH, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci USA 99:11742–11747PubMedCrossRefGoogle Scholar
  29. Hedgecock D (1994) Does variance in reproductive success limit effective population sizes of marine organisms? In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman and Hall, London, pp 122–134Google Scholar
  30. Hendrick P (2005) Large variance in reproductive success and the N e/N ratio. Evolution 59:1596–1599Google Scholar
  31. Hendry AP, Kinnison MT (1999) The pace of modern life: measuring rates of contemporary microevolution. Evolution 53:1637–1653CrossRefGoogle Scholar
  32. Hoarau G, Boon E, Jongma DN, Ferber S, Rijnsdorp AD, Palsson J, Van der Veer HW, Stam WT, Olsen JL (2005) Low effective population size and evidence for inbreeding in a commercially overexploited flatfish: plaice (Pleuronectes platessa). Proc R Soc Lond B 272:497–503CrossRefGoogle Scholar
  33. Hutchinson WF, Van Oosterhout C, Rogers SI, Carvalho GR (2003) Temporal analysis of archived samples indicates marked genetic changes in declining North Sea cod (Gadus morhua). Proc R Soc Lond B 270:2125–2132CrossRefGoogle Scholar
  34. Jorde PE, Ryman N (1995) Temporal allele frequency change and estimation of effective size in populations with overlapping generations. Genetics 139:1077–1090PubMedGoogle Scholar
  35. Jorde PE, Ryman N (1996) Demographic genetics of brown trout (Salmo trutta) and estimation of effective population size from temporal change of allele frequencies. Genetics 143:1369–1381PubMedGoogle Scholar
  36. Kauer MO, Dieringer D, Schlötterer C (2003) A microsatellite variability screen for positive selection associated with the “out of Africa” habitat expansion of Drosophila melanogaster. Genetics 165:1137–1148PubMedGoogle Scholar
  37. Knights B (2003) A review of the possible impacts of long-term oceanic and climate changes and fishing mortality on recruitment of anguillid eels of the Northern hemisphere. Sci Total Environ 310:237–244PubMedCrossRefGoogle Scholar
  38. Kuhner MK (2006) LAMARC 2.0:maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770PubMedCrossRefGoogle Scholar
  39. Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460PubMedCrossRefGoogle Scholar
  40. Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol Ecol 7:963–974PubMedCrossRefGoogle Scholar
  41. Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW (2010) Estimating census and effective population sizes: increasing usefulness of genetic methods. Conserv Genet 11:355–373CrossRefGoogle Scholar
  42. Lynch M, Lande R (1998) The critical effective population size for a genetically secure population. Anim Conserv 1:70–72CrossRefGoogle Scholar
  43. Maes GE, Pujolar JM, Hellemans B, Volckaert FAM (2007) Evidence for isolation by time in the European eel (Anguilla anguilla). Mol Ecol 15:2095–2107CrossRefGoogle Scholar
  44. McCleave JD (1993) Physical and behavioral controls on the oceanic distribution and migration of leptocephali. J Fish Biol 43:243–273CrossRefGoogle Scholar
  45. Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a genetic population. Genet Res 22:201–204CrossRefGoogle Scholar
  46. Palm S, Dannewitz J, Prestegaard T, Wickström H (2009) Panmixia in the European eel revisited: no genetic difference between maturing adults from southern and northern Europe. Heredity 103:82–89PubMedCrossRefGoogle Scholar
  47. Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447PubMedCrossRefGoogle Scholar
  48. Palstra AP, Van Ginneken VJT, Murk AJ, Van den Thillart G (2006) Are dioxin-like contaminants responsible for the eel Anguilla anguilla drama? Naturwissenschaften 93:145–148PubMedCrossRefGoogle Scholar
  49. Peng B, Amos CI (2008) Forward-time simulations and non-random mating using SIMUPOP. Bioinformatics 24:1408–1409PubMedCrossRefGoogle Scholar
  50. Piry SG, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  51. Pollak E (1983) A new method for estimating the effective population size from allele frequency changes. Genetics 104:531–548PubMedGoogle Scholar
  52. Pujolar JM, Maes GE, Volckaert FAM (2006) Genetic patchiness among recruits of the European eel Anguilla anguilla. Mar Ecol Prog Ser 307:209–217CrossRefGoogle Scholar
  53. Pujolar JM, Maes GE, Volckaert FAM (2007) Genetic and morphometric heterogeneity among recruits of the European eel Anguilla anguilla. Bull Mar Sci 81:297–308Google Scholar
  54. Pujolar JM, Ciccotti E, De Leo GA, Zane L (2009a) Genetic composition of Atlantic and Mediterranean recruits of the European eel (Anguilla anguilla) based on EST-linked microsatellite. J Fish Biol 74:2034–2046PubMedCrossRefGoogle Scholar
  55. Pujolar JM, Maes GE, Van Hoedt JKJ, Zane L (2009b) Isolation and characterization of EST-linked microsatellite loci for the European eel, Anguilla anguilla. Mol Ecol Res 9:233–235CrossRefGoogle Scholar
  56. Rambaut A, Drummond AJ (2007) Tracer version 1.4. Available from
  57. Raymond M, Rousset F (1995) GENEPOP (version 1.2): a population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  58. Rice WR (1989) Analyzing tables and statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  59. Robinet TT, Feunteun E (2002) Sublethal effects of exposure to chemical compounds: a cause for the decline in Atlantic eels? Ecotoxicology 11:265–277PubMedCrossRefGoogle Scholar
  60. Ruzzante DE, Taggart CT, Doyle RW, Cook D (2001) Stability in the historical pattern of genetic structure of Newfoundland cod (Gadus morhua) despite the catastrophic decline in population size from 1964 to 1994. Conserv Genet 2:257–269CrossRefGoogle Scholar
  61. Schlötterer C (2003) A microsatellite-based multilocus screen for the identification of local selective sweeps. Genetics 160:753–763Google Scholar
  62. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. Freeman and Co, New YorkGoogle Scholar
  63. Stockwell CA, Ashley MV (2003) Rapid adaptation and conservation. Conserv Biol 18:272–273CrossRefGoogle Scholar
  64. Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18:94–101CrossRefGoogle Scholar
  65. Taylor AC, Sherwin WB, Wayne RK (1994) Genetic variation of microsatellite loci in a bottlenecked species: the northern hairy-nosed wombat, Lasiorhinus krefftii. Mol Ecol 3:277–290PubMedCrossRefGoogle Scholar
  66. Van den Thillart G, Rankin JC, Dufour S (2009) Spawning migration of the European eel: reproduction index, a useful tool for conservation management. Springer, DordechtCrossRefGoogle Scholar
  67. Van Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol 4:535–538CrossRefGoogle Scholar
  68. Vøllestad LA (1992) Geographic variation in age and length at metamorphosis of maturing European eel: environmental effects and phenotypic plasticity. J Anim Ecol 61:41–48CrossRefGoogle Scholar
  69. Wirth T, Bernatchez L (2003) Decline of North Atlantic eels: a fatal synergy? Proc R Soc Lond B 270:681–688CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • J. M. Pujolar
    • 1
  • D. Bevacqua
    • 2
  • F. Capoccioni
    • 3
  • E. Ciccotti
    • 3
  • G. A. De Leo
    • 2
  • L. Zane
    • 1
  1. 1.Dipartimento di BiologiaUniversità di PadovaPadovaItaly
  2. 2.Dipartimento di Scienze AmbientaliUniversità degli Studi di ParmaParmaItaly
  3. 3.Dipartimento di BiologiaUniversità Roma Tor VergataRomeItaly

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