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.
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
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
Balloux F (2001) EASYPOP (Version 1.7): a computer program for population genetics simulations. J Hered 92:301–302
Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029
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
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
Bernatchez L, Wilson CC (1998) Comparative phylogeography of nearctic and palearctic fishes. Mol Ecol 7:431–452
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
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
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
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
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
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
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
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
Dinerstein E, McCracken GF (1990) Endangered greater one-horned rhinoceros carry high-levels of genetic-variation. Conserv Biol 4:417–422
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
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
Excoffier L, Estoup A, Cornuet JM (2005) Bayesian analysis of an admixture model with mutations and arbitrarily linked markers. Genetics 169:1727–1738
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
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
Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327
Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508
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
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
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
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
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
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
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
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
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
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
Hale KA, Briskie JV (2007) Decreased immunocompetence in a severely bottlenecked population of an endemic New Zealand bird. Anim Conserv 10:2–10
Haugen TO, Vøllestad LA (2001) A century of life-history evolution in grayling. Genetica 112:475–491
Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112
Hill WG (1981) Estimation of effective population-size from data on linkage disequilibrium. Genet Res 38:209–216
Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Statist 6:65–70
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
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
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
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
Kontula T, Vainola R (2001) Postglacial colonization of Northern Europe by distinct phylogeographic lineages of the bullhead, Cottus gobio. Mol Ecol 10:1983–2002
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
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
Koskinen MT, Haugen TO, Primmer CR (2002a) Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:826–830
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
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
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
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
Lande R (1994) Risk of population extinction from fixation of new deleterious mutations. Evolution 48:1460–1469
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
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
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
Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237
Luikart G, Cornuet JM (1999) Estimating the effective number of breeders from heterozygote excess in progeny. Genetics 151:1211–1216
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
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
Mardulyn P, Vaesen M-A, Milinkovitch MC (2008) Controlling population evolution in the laboratory to evaluate methods of historical inference. PLoS ONE 3:e2960
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
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
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Nei M, Chakraborty R, Fuerst PA (1976) Infinite allele model with varying mutation-rate. Proc Natl Acad Sci USA 73:4164–4168
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
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
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
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
Rand DM (1996) Neutrality tests of molecular markers and the connection between DNA polymorphism, demography, and conservation biology. Conserv Biol 10:665–671
Raymond M, Rousset F (1995) Genepop (version 1.2)—population genetics software for exact tests and ecumenicism. J Hered 86:248–249
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
Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Vitalis R, Couvet D (2001) Estimation of effective population size and migration rate from one- and two-locus identity measures. Genetics 157:911–925
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
Waples RS (1989) A generalized-approach for estimating effective population-size from temporal changes in allele frequency. Genetics 121:379–391
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
Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562
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
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
Corresponding author
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-009-0031-x