Skip to main content
Log in

Historical and recent genetic bottlenecks in European grayling, Thymallus thymallus

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

Abstract

Sharp declines in population size, known as genetic bottlenecks, increase the level of inbreeding and reduce genetic diversity threatening population sustainability in both short- and long-term. We evaluated the presence, severity and approximate time of bottlenecks in 34 European grayling (Thymallus thymallus) populations covering the majority of the species distribution using microsatellite markers. We identified footprints of population decline in all grayling populations using the M ratio test. In contrast to earlier simulation studies assuming isolated populations, forward simulations allowing low levels of migration demonstrated that bottleneck footprints measured using the M ratio can persist within small populations much longer (up to thousands of generations) than previously anticipated. Using a coalescence approach, the beginning of population reduction was dated back to 1,000–10,000 years ago which suggests that the extremely low M ratio in European grayling is most likely caused by the last glaciation and subsequent post-glacial recolonization processes. In contrast to the M ratio, two alternative methods for bottleneck detection identified more recent bottlenecks in six populations and thus, from a conservation perspective, these populations warrant future monitoring. Based on a single time-point analysis using approximate Bayesian computation methodology, all grayling populations exhibited very small effective population sizes with the majority of N e estimates below 50. Taken together, our results demonstrate the predominate role of genetic drift in European grayling populations in the short term but also emphasize the importance of gene flow counteracting the effects of genetic drift and loss of variation over longer evolutionary timescales.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdelkrim J, Pascal M, Samadi S (2005) Island colonization and founder effects: the invasion of the Guadeloupe islands by ship rats (Rattus rattus). Mol Ecol 14:2923–2931

    Article  CAS  PubMed  Google Scholar 

  • Aspi J, Roininen E, Kiiskila J, Ruokonen M, Kojola I, Bljudnik L, Danilov P, Heikkinen S, Pulliainen E (2009) Genetic structure of the northwestern Russian wolf populations and gene flow between Russia and Finland. Conserv Genet 10:815–826

    Article  CAS  Google Scholar 

  • Balloux F (2001) EASYPOP (Version 1.7): a computer program for population genetics simulations. J Hered 92:301–302

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Beaumont MA (2004) msvar1.3 update. http://www.rubic.rdg.ac.uk/~mab/stuff/

  • Beebee T, Rowe G (2001) Application of genetic bottleneck testing to the investigation of amphibian declines: a case study with natterjack toads. Conserv Biol 15:266–270

    Google Scholar 

  • Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568

    Article  CAS  PubMed  Google Scholar 

  • Bernatchez L, Wilson CC (1998) Comparative phylogeography of nearctic and palearctic fishes. Mol Ecol 7:431–452

    Article  Google Scholar 

  • Bouza C, Castro J, Martinez P, Amaro R, Fernandez C, Ondina P, Outeiro A, Miguel ES (2007) Threatened freshwater pearl mussel Margaritifera margaritifera L. in NW Spain: low and very structured genetic variation in southern peripheral populations assessed using microsatellite markers. Conserv Genet 8:937–948

    Article  CAS  Google Scholar 

  • Briscoe DA, Malpica JM, Robertson A, Smith GJ, Frankham R, Banks RG, Barker JSF (1992) Rapid loss of genetic-variation in large captive populations of Drosophila flies—implications for the genetic management of captive populations. Conserv Biol 6:416–425

    Article  Google Scholar 

  • Busch JD, Waser PM, DeWoody JA (2007) Recent demographic bottlenecks are not accompanied by a genetic signature in banner-tailed kangaroo rats (Dipodomys spectabilis). Mol Ecol 16:2450–2462

    Article  CAS  PubMed  Google Scholar 

  • Chen YH, Opp SB, Berlocher SH, Roderick GK (2006) Are bottlenecks associated with colonization? Genetic diversity and diapause variation of native and introduced Rhagoletis completa populations. Oecologia 149:656–667

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Costello AB, Down TE, Pollard SM, Pacas CJ, Taylor EB (2003) The influence of history and contemporary stream hydrology on the evolution of genetic diversity within species: an examination of microsatellite DNA variation in bull trout, Salvelinus confluentus (Pisces: Salmonidae). Evolution 57:328–344

    CAS  PubMed  Google Scholar 

  • Dhuyvetter H, Gaublomme E, Desender K (2005) Bottlenecks, drift and differentiation: the fragmented population structure of the saltmarsh beetle Pogonus chalceus. Genetica 124:167–177

    Article  CAS  PubMed  Google Scholar 

  • Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170

    Article  PubMed  Google Scholar 

  • Dinerstein E, McCracken GF (1990) Endangered greater one-horned rhinoceros carry high-levels of genetic-variation. Conserv Biol 4:417–422

    Article  Google Scholar 

  • Duftner N, Koblmuller S, Weiss S, Medgyesy N, Sturmbauer C (2005) The impact of stocking on the genetic structure of European grayling (Thymallus thymallus, Salmonidae) in two alpine rivers. Hydrobiologia 542:121–129

    Article  CAS  Google Scholar 

  • England PR, Cornuet JM, Berthier P, Tallmon DA, Luikart G (2006) Estimating effective population size from linkage disequilibrium: severe bias in small samples. Conserv Genet 7:303–308

    Article  Google Scholar 

  • Excoffier L, Estoup A, Cornuet JM (2005) Bayesian analysis of an admixture model with mutations and arbitrarily linked markers. Genetics 169:1727–1738

    Article  CAS  PubMed  Google Scholar 

  • Fave MJ, Turgeon J (2008) Patterns of genetic diversity in Great Lakes bloaters (Coregonus hoyi) with a view to future reintroduction in Lake Ontario. Conserv Genet 9:281–293

    Article  Google Scholar 

  • Fernandez-Stolz GP, Stolz JFB, De Freitas TRO (2007) Bottlenecks and dispersal in the tuco-tuco das dunas, Ctenomys Flamarioni (rodentia: Ctenomyidae), in southern Brazil. J Mammal 88:935–945

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508

    Article  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 contrasting population systems. Mol Ecol 16:3866–3889

    Article  PubMed  Google Scholar 

  • Garza JC (2006) Critical M. http://swfsc.noaa.gov/textblock.aspx?Division=FED&id=3298

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

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Gross R, Kuhn R, Baars M, Schroder W, Stein H, Rottmann O (2001) Genetic differentiation of European grayling populations across the Main, Danube and Elbe drainages in Bavaria. J Fish Biol 58:264–280

    Article  CAS  Google Scholar 

  • Gross R, Lulla P, Naver T (2007) Genetic variability and differentiation of rainbow trout (Oncorhynchus mykiss) strains in northern and Eastern Europe. Aquaculture 272:S139–S146

    Article  Google Scholar 

  • 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 

  • Gum B, Gross R, Rottmann O, Schroder W, Kuhn R (2003) Microsatellite variation in Bavarian populations of European grayling (Thymallus thymallus): implications for conservation. Conserv Genet 4:659–672

    Article  CAS  Google Scholar 

  • Gum B, Gross R, Kuehn R (2005) Mitochondrial and nuclear DNA phylogeography of European grayling (Thymallus thymallus): evidence for secondary contact zones in central Europe. Mol Ecol 14:1707–1725

    Article  CAS  PubMed  Google Scholar 

  • Gum B, Gross R, Kuehn R (2006) Discriminating the impact of recent human mediated stock transfer from historical gene flow on genetic structure of European grayling Thymallus thymallus L. J Fish Biol 69:115–135

    Article  CAS  Google Scholar 

  • Gum B, Gross R, Geist J (2009) Conservation genetics and management implications for European grayling, Thymallus thymallus: synthesis of phylogeography and population genetics. Fish Manag Ecol 16:37–51

    Article  Google Scholar 

  • Hale KA, Briskie JV (2007) Decreased immunocompetence in a severely bottlenecked population of an endemic New Zealand bird. Anim Conserv 10:2–10

    Article  Google Scholar 

  • Haugen TO, Vøllestad LA (2001) A century of life-history evolution in grayling. Genetica 112:475–491

    Article  PubMed  Google Scholar 

  • Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112

    Article  Google Scholar 

  • Hill WG (1981) Estimation of effective population-size from data on linkage disequilibrium. Genet Res 38:209–216

    Article  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Statist 6:65–70

    Google Scholar 

  • Hood GM (2006) PopTools 2.7.5. Albany, Western Australia

  • Houlden BA, England PR, Taylor AC, Greville WD, Sherwin WB (1996) Low genetic variability of the koala Phascolarctos cinereus in south-eastern Australia following a severe population bottleneck. Mol Ecol 5:269–281

    CAS  PubMed  Google Scholar 

  • Johnson JA, Tingay RE, Culver M, Hailer F, Clarke ML, Mindell DP (2009) Long-term survival despite low genetic diversity in the critically endangered Madagascar fish-eagle. Mol Ecol 18:54–63

    PubMed  Google Scholar 

  • Kaukoranta M, Koljonen M-L, Koskiniemi J, Pennanen J, Tammi J (2000) Atlas of Finnish fishes, English summary. Distribution of lamprey, brook lamprey, salmon, trout, Arctic charr, whitefish, vandace, grayling, asp, vimba, spined loach and bullhead, and status of the stocks. Finnish Game and Fisheries Research Institute, Helsinki, Finland, p 40

    Google Scholar 

  • King JP, Kimmel M, Chakraborty R (2000) A power analysis of microsatellite-based statistics for inferring past population growth. Mol Biol Evol 17:1859–1868

    CAS  PubMed  Google Scholar 

  • Kontula T, Vainola R (2001) Postglacial colonization of Northern Europe by distinct phylogeographic lineages of the bullhead, Cottus gobio. Mol Ecol 10:1983–2002

    Article  CAS  PubMed  Google Scholar 

  • Korkea-Aho T (2003) Individual-based population genetic analysis of grayling (Thymallus thymallus) from a single water system. Department of Biological and Environmental Sciences, University of Helsinki, Helsinki, p 80

  • Koskinen MT, Ranta E, Piironen J, Veselov A, Titov S, Haugen TO, Nilsson J, Carlstein M, Primmer CR (2000) Genetic lineages and postglacial colonization of grayling (Thymallus thymallus, Salmonidae) in Europe, as revealed by mitochondrial DNA analyses. Mol Ecol 9:1609–1624

    Article  CAS  PubMed  Google Scholar 

  • Koskinen MT, Piironen J, Primmer CR (2001) Interpopulation genetic divergence in European grayling (Thymallus thymallus, Salmonidae) at a microgeographic scale: implications for conservation. Conserv Genet 2:133–143

    Article  Google Scholar 

  • Koskinen MT, Haugen TO, Primmer CR (2002a) Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:826–830

    Article  CAS  PubMed  Google Scholar 

  • Koskinen MT, Knizhin I, Primmer CR, Schlotterer C, Weiss S (2002b) Mitochondrial and nuclear DNA phylogeography of Thymallus spp. (grayling) provides evidence of ice-age mediated environmental perturbations in the world’s oldest body of fresh water, Lake Baikal. Mol Ecol 11:2599–2611

    Article  CAS  PubMed  Google Scholar 

  • Koskinen MT, Nilsson J, Veselov AJ, Potutkin AG, Ranta E, Primmer CR (2002c) Microsatellite data resolve phylogeographic patterns in European grayling, Thymallus thymallus, Salmonidae. Heredity 88:391–401

    Article  CAS  PubMed  Google Scholar 

  • Koskinen MT, Sundell P, Piironen J, Primmer CR (2002d) Genetic assessment of spatiotemporal evolutionary relationships and stocking effects in grayling (Thymallus thymallus, Salmonidae). Ecol Lett 5:193–205

    Article  Google Scholar 

  • Koyuk A, Bennett A, Tallmon D (2008) ONeSAMP 1.1. http://genomics.jun.alaska.edu/

  • Lambert DM, King T, Shepherd LD, Livingston A, Anderson S, Craig JL (2005) Serial population bottlenecks and genetic variation: translocated populations of the New Zealand Saddleback (Philesturnus carunculatus rufusater). Conserv Genet 6:1–14

    Article  Google Scholar 

  • Lande R (1994) Risk of population extinction from fixation of new deleterious mutations. Evolution 48:1460–1469

    Article  Google Scholar 

  • Le Page SL, Livermore RA, Cooper DW, Taylor AC (2000) Genetic analysis of a documented population bottleneck: introduced Bennett’s wallabies (Macropus rufogriseus rufogriseus) in New Zealand. Mol Ecol 9:753–763

    Article  CAS  PubMed  Google Scholar 

  • Lehtonen PK, Tonteri A, Sendek D, Titov S, Primmer CR (2009) Spatio-temporal genetic structuring of brown trout (Salmo trutta L.) populations within the River Luga, northwest Russia. Conserv Genet 10:281–289

    Article  Google Scholar 

  • Lucchini V, Galov A, Randi E (2004) Evidence of genetic distinction and long-term population decline in wolves (Canis lupus) in the Italian Apennines. Mol Ecol 13:523–536

    Article  CAS  PubMed  Google Scholar 

  • Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Luikart G, Cornuet JM (1999) Estimating the effective number of breeders from heterozygote excess in progeny. Genetics 151:1211–1216

    CAS  PubMed  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998a) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mardulyn P, Vaesen M-A, Milinkovitch MC (2008) Controlling population evolution in the laboratory to evaluate methods of historical inference. PLoS ONE 3:e2960

    Article  PubMed  Google Scholar 

  • Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. 2. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689

    CAS  PubMed  Google Scholar 

  • Meldgaard T, Nielsen EE, Loeschcke V (2003) Fragmentation by weirs in a riverine system: a study of genetic variation in time and space among populations of European grayling (Thymallus thymallus) in a Danish river system. Conserv Genet 4:735–747

    Article  CAS  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  • Nei M, Chakraborty R, Fuerst PA (1976) Infinite allele model with varying mutation-rate. Proc Natl Acad Sci USA 73:4164–4168

    Article  CAS  PubMed  Google Scholar 

  • Nylander E (2004) Kalatalous tilastoina 2004: Finnish fisheries statistic. Finnish Game and Fisheries Research Institute, p 28

  • 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 

  • Peel D, Ovenden J, Peel S (2004) NeEstimator: software for estimating effective population size, version 1.3. Queensland Government, Department of Primary Industries and Fisheries

  • Piry S, 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 

  • Pudovkin AI, Zaykin DV, Hedgecock D (1996) On the potential for estimating the effective number of breeders from heterozygote-excess in progeny. Genetics 144:383–387

    CAS  PubMed  Google Scholar 

  • Queney G, Ferrand N, Marchandeau S, Azevedo M, Mougel F, Branco M, Monnerot M (2000) Absence of a genetic bottleneck in a wild rabbit (Oryctolagus cuniculus) population exposed to a severe viral epizootic. Mol Ecol 9:1253–1264

    Article  CAS  PubMed  Google Scholar 

  • Rand DM (1996) Neutrality tests of molecular markers and the connection between DNA polymorphism, demography, and conservation biology. Conserv Biol 10:665–671

    Article  Google Scholar 

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

    Google Scholar 

  • Russello MA, Brazaitis P, Gratten J, Watkins-Colwell GJ, Caccone A (2007) Molecular assessment of the genetic integrity, distinctiveness and phylogeographic context of the saltwater crocodile (Crocodylus porosus) on Palau. Conserv Genet 8:777–787

    Article  CAS  Google Scholar 

  • Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494

    Article  CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. Ver 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of Geneva

  • Schwartz MK, Tallmon DA, Luikart G (1998) Review of DNA-based census and effective population size estimators. Anim Conserv 1:293–299

    Article  Google Scholar 

  • Shimoda N, Knapik EW, Ziniti J, Sim C, Yamada E, Kaplan S, Jackson D, de Sauvage F, Jacob H, Fishman MC (1999) Zebrafish genetic map with 2000 microsatellite markers. Genomics 58:219–232

    Article  CAS  PubMed  Google Scholar 

  • Spear SF, Peterson CR, Matocq MD, Storfer A (2006) Molecular evidence for historical and recent population size reductions of tiger salamanders (Ambystoma tigrinum) in Yellowstone National Park. Conserv Genet 7:605–611

    Article  Google Scholar 

  • Stamford MD, Taylor EB (2005) Population subdivision and genetic signatures of demographic changes in Arctic grayling (Thymallus arcticus) from an impounded watershed. Can J Fish Aquat Sci 62:2548–2559

    Article  CAS  Google Scholar 

  • Steinfartz S, Glaberman S, Lanterbecq D, Marquez C, Rassmann K, Caccone A (2007) Genetic impact of a severe El Niño event on Galápagos marine Iguanas (Amblyrhynchus cristatus). PloS ONE 2:e1285

    Article  PubMed  Google Scholar 

  • Storz JF, Beaumont MA (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56:154–166

    CAS  PubMed  Google Scholar 

  • Storz JF, Beaumont MA, Alberts SC (2002) Genetic evidence for long-term population decline in a savannah-dwelling primate: inferences from a hierarchical Bayesian model. Mol Biol Evol 19:1981–1990

    CAS  PubMed  Google Scholar 

  • Susnik S, Snoj A, Dovc P (2001) Evolutionary distinctness of grayling (Thymallus thymallus) inhabiting the Adriatic river system, as based on mtDNA variation. Biol J Linn Soc 74:375–385

    Article  Google Scholar 

  • Susnik S, Berrebi P, Dovc P, Hansen MM, Snoj A (2004) Genetic introgression between wild and stocked salmonids and the prospects for using molecular markers in population rehabilitation: the case of the Adriatic grayling (Thymallus thymallus L. 1785). Heredity 93:273–282

    Article  CAS  PubMed  Google Scholar 

  • Swatdipong A, Vasemägi A, Koskinen M, Piironen J, Primmer C (2009) Unanticipated population structure of European grayling in its northern distribution: implications for conservation prioritization. Front Zool 6:6

    Article  PubMed  Google Scholar 

  • Tallmon DA, Luikart G, Beaumont MA (2004) Comparative evaluation of a new effective population size estimator based on approximate Bayesian computation. Genetics 167:977–988

    Article  PubMed  Google Scholar 

  • Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Resour 8:299–301

    Article  Google Scholar 

  • Taylor EB, McPhail JD (2000) Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proc R Soc Lond Ser B: Biol Sci 267:2375–2384

    Google Scholar 

  • Uiblein F, Jagsch A, Honsig-Erlenburg W, Weiss S (2001) Status, habitat use, and vulnerability of the European grayling in Austrian waters. J Fish Biol 59:223–247

    Google Scholar 

  • Vähä JP, Erkinaro J, Niemela E, Primmer CR (2007) Life-history and habitat features influence the within-river genetic structure of Atlantic salmon. Mol Ecol 16:2638–2654

    Article  PubMed  Google Scholar 

  • Vasemägi A, Gross R, Paaver T, Koljonen ML, Säisä M, Nilsson J (2005) Analysis of gene associated tandem repeat markers in Atlantic salmon (Salmo salar L.) populations: implications for restoration and conservation in the Baltic Sea. Conserv Genet 6:385–397

    Article  Google Scholar 

  • Vitalis R, Couvet D (2001) Estimation of effective population size and migration rate from one- and two-locus identity measures. Genetics 157:911–925

    CAS  PubMed  Google Scholar 

  • Wang YQ, Williams DA, Gaines MS (2005) Evidence for a recent genetic bottleneck in the endangered Florida Keys silver rice rat (Oryzomys argentatus) revealed by microsatellite DNA analyses. Conserv Genet 6:575–585

    Article  CAS  Google Scholar 

  • Waples RS (1989) A generalized-approach for estimating effective population-size from temporal changes in allele frequency. Genetics 121:379–391

    CAS  PubMed  Google Scholar 

  • Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184

    Article  Google Scholar 

  • Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562

    Article  Google Scholar 

  • Witzenberger KA, Hochkirch A (2008) Genetic consequences of animal translocations: A case study using the field cricket, Gryllus campestris L. Biol Conserv 141:3059–3068

    Article  Google Scholar 

Download references

Acknowledgements

We acknowledge Einar Eg Nielsen, Jens Carlsson, Jouni Aspi, Daniel Ruzzante and three anonymous reviewers for valuable comments to improve the manuscript. We also acknowledge Juha-Pekka Vähä for useful discussions. Part of the MSVAR 1.3 simulations was carried out using the resources of the computational biology service unit from Cornell University, which is partially funded by the Microsoft Corporation. We also thank François Balloux for providing a modified version of Easypop 1.8. This study was supported by a Royal Thai Scholarship (to AS), the Academy of Finland (to AV, Post-Doctoral Fellowship; to CP, Centre of Excellence in Evolutionary Genetics and Physiology) and the Estonian Science Foundation (to AV, grant no. 6802).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anti Vasemägi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Swatdipong, A., Primmer, C.R. & Vasemägi, A. Historical and recent genetic bottlenecks in European grayling, Thymallus thymallus . Conserv Genet 11, 279–292 (2010). https://doi.org/10.1007/s10592-009-0031-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-009-0031-x

Keywords

Navigation