Skip to main content

Advertisement

SpringerLink
Log in

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

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337

    Article  PubMed  Google Scholar 

  • Anderson EC, Garza JC (2009) Estimation of population size with molecular genetic data. NOAA Tech. Mem. NMFS-SWFSC-448

  • 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

  • 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 9:323

    Article  Google Scholar 

  • Ashley MV, Wilson MF, Pergams ORW, O’Dowd DJ, Gende SM, Brown JS (2003) Evolutionarily enlightened management. Biol Conserv 111:115–123

    Article  Google Scholar 

  • Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029

    PubMed  CAS  Google Scholar 

  • 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 98:4563–4568

    Article  PubMed  CAS  Google Scholar 

  • 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)

  • 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 18:197–214

    Article  Google Scholar 

  • 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, Sweden

  • Bonhommeau S, Chassot E, Rivot E (2008) Fluctuations in European eel (Anguilla anguilla) recruitment resulting from environmental changes in the Sargasso Sea. Fish Oceanogr 17:32–44

    Article  Google Scholar 

  • 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

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • 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 272:1129–1137

    Article  Google Scholar 

  • Dekker W (2000) A Procrustean assessment of the European eel stock. ICES J Mar Sci 57:938–947

    Article  Google Scholar 

  • Dekker W (2003) Did lack of spawners cause the collapse of the European eel Anguilla anguilla? Fish Manage Ecol 10:365–376

    Article  Google Scholar 

  • 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 91:3166–3170

    Article  PubMed  CAS  Google Scholar 

  • 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, Denmark

  • 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, Denmark

  • Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327

    Article  PubMed  CAS  Google Scholar 

  • Franklin JR (1980) Evolutionary change in small populations. In: Soulé ME, Wilcox BA (eds) Conservation biology: an evolutionary-ecological perspective. Sinuer, Sunderland, pp 135–150

    Google Scholar 

  • 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 16:3866–3889

    Article  PubMed  Google Scholar 

  • 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 64:519–530

    Article  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  PubMed  CAS  Google Scholar 

  • Goudet J (2002) FSTAT version 2.9.3.2. Available from: http://www2.unil.ch/popgen/softwares/fstat.htm

  • 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–S67

    Article  PubMed  Google Scholar 

  • Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362

    Google Scholar 

  • 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 99:11742–11747

    Article  PubMed  CAS  Google Scholar 

  • 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 122–134

    Google Scholar 

  • Hendrick P (2005) Large variance in reproductive success and the N e /N ratio. Evolution 59:1596–1599

    Google Scholar 

  • Hendry AP, Kinnison MT (1999) The pace of modern life: measuring rates of contemporary microevolution. Evolution 53:1637–1653

    Article  Google Scholar 

  • 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 272:497–503

    Article  Google Scholar 

  • 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 270:2125–2132

    Article  Google Scholar 

  • Jorde PE, Ryman N (1995) Temporal allele frequency change and estimation of effective size in populations with overlapping generations. Genetics 139:1077–1090

    PubMed  CAS  Google Scholar 

  • 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 143:1369–1381

    PubMed  CAS  Google Scholar 

  • 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 165:1137–1148

    PubMed  CAS  Google Scholar 

  • 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 310:237–244

    Article  PubMed  CAS  Google Scholar 

  • Kuhner MK (2006) LAMARC 2.0:maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770

    Article  PubMed  CAS  Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460

    Article  PubMed  CAS  Google Scholar 

  • Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol Ecol 7:963–974

    Article  PubMed  CAS  Google Scholar 

  • Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW (2010) Estimating census and effective population sizes: increasing usefulness of genetic methods. Conserv Genet 11:355–373

    Article  CAS  Google Scholar 

  • Lynch M, Lande R (1998) The critical effective population size for a genetically secure population. Anim Conserv 1:70–72

    Article  Google Scholar 

  • Maes GE, Pujolar JM, Hellemans B, Volckaert FAM (2007) Evidence for isolation by time in the European eel (Anguilla anguilla). Mol Ecol 15:2095–2107

    Article  Google Scholar 

  • McCleave JD (1993) Physical and behavioral controls on the oceanic distribution and migration of leptocephali. J Fish Biol 43:243–273

    Article  Google Scholar 

  • Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a genetic population. Genet Res 22:201–204

    Article  Google Scholar 

  • 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 103:82–89

    Article  PubMed  CAS  Google Scholar 

  • 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 17:3428–3447

    Article  PubMed  Google Scholar 

  • Palstra AP, Van Ginneken VJT, Murk AJ, Van den Thillart G (2006) Are dioxin-like contaminants responsible for the eel Anguilla anguilla drama? Naturwissenschaften 93:145–148

    Article  PubMed  CAS  Google Scholar 

  • Peng B, Amos CI (2008) Forward-time simulations and non-random mating using SIMUPOP. Bioinformatics 24:1408–1409

    Article  PubMed  CAS  Google Scholar 

  • 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 90:502–503

    Article  Google Scholar 

  • Pollak E (1983) A new method for estimating the effective population size from allele frequency changes. Genetics 104:531–548

    PubMed  CAS  Google Scholar 

  • Pujolar JM, Maes GE, Volckaert FAM (2006) Genetic patchiness among recruits of the European eel Anguilla anguilla. Mar Ecol Prog Ser 307:209–217

    Article  Google Scholar 

  • Pujolar JM, Maes GE, Volckaert FAM (2007) Genetic and morphometric heterogeneity among recruits of the European eel Anguilla anguilla. Bull Mar Sci 81:297–308

    Google Scholar 

  • 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 74:2034–2046

    Article  PubMed  CAS  Google Scholar 

  • 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 9:233–235

    Article  CAS  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer version 1.4. Available from http://beast.bio.ed.ac.uk/Tracer

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): a population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rice WR (1989) Analyzing tables and statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Robinet TT, Feunteun E (2002) Sublethal effects of exposure to chemical compounds: a cause for the decline in Atlantic eels? Ecotoxicology 11:265–277

    Article  PubMed  CAS  Google Scholar 

  • 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 2:257–269

    Article  CAS  Google Scholar 

  • Schlötterer C (2003) A microsatellite-based multilocus screen for the identification of local selective sweeps. Genetics 160:753–763

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. Freeman and Co, New York

    Google Scholar 

  • Stockwell CA, Ashley MV (2003) Rapid adaptation and conservation. Conserv Biol 18:272–273

    Article  Google Scholar 

  • Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18:94–101

    Article  Google Scholar 

  • 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 3:277–290

    Article  PubMed  CAS  Google Scholar 

  • Van den Thillart G, Rankin JC, Dufour S (2009) Spawning migration of the European eel: reproduction index, a useful tool for conservation management. Springer, Dordecht

    Book  Google Scholar 

  • Van Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol 4:535–538

    Article  Google Scholar 

  • Vøllestad LA (1992) Geographic variation in age and length at metamorphosis of maturing European eel: environmental effects and phenotypic plasticity. J Anim Ecol 61:41–48

    Article  Google Scholar 

  • Wirth T, Bernatchez L (2003) Decline of North Atlantic eels: a fatal synergy? Proc R Soc Lond B 270:681–688

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Dipartimento di Biologia, Università di Padova, Via G. Colombo 3, 35131, Padova, Italy

    J. M. Pujolar & L. Zane

  2. Dipartimento di Scienze Ambientali, Università degli Studi di Parma, Viale Usberti 11A, 43100, Parma, Italy

    D. Bevacqua & G. A. De Leo

  3. Dipartimento di Biologia, Università Roma Tor Vergata, 00133, Rome, Italy

    F. Capoccioni & E. Ciccotti

Authors
  1. J. M. Pujolar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. Bevacqua
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. Capoccioni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Ciccotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. A. De Leo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. L. Zane
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. M. Pujolar.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 83 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pujolar, J.M., Bevacqua, D., Capoccioni, F. et al. No apparent genetic bottleneck in the demographically declining European eel using molecular genetics and forward-time simulations. Conserv Genet 12, 813–825 (2011). https://doi.org/10.1007/s10592-011-0188-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-011-0188-y

Keywords

Search

Navigation