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Substantial genetic structure among stocked and native populations of the European grayling (Thymallus thymallus, Salmonidae) in the United Kingdom

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Abstract

While currently in a state of recovery in the United Kingdom (UK), the grayling (Thymallus thymallus) remains of conservation interest due to its historical decline, socio-economic value and the potential impact of hatchery-reared stock fish on the genetic structure and diversity of wild populations. However, little is known about the levels and distribution of genetic diversity among UK grayling populations. To this end, 27 UK populations of grayling were genotyped across 10 microsatellite loci and sequenced at the mtDNA D-Loop. All populations clustered into four higher-level groups: Northern England, Southern England, Wales, and group consisting of a mixture of native and introduced populations. Ten populations showed evidence of bottleneck or founder effects, and the effective population size (Ne) was low in all populations. In most cases, historical stocking records agreed with the genetic relationships revealed in the study. A D-Loop haplotype network supported the groupings observed in the nuclear data, while phylogenetic inference places the UK populations amongst Central European samples. The combined datasets demonstrate that many of the UK populations can be treated as separate Management Units and we recommend that to preserve population specific genetic diversity, that stocking should be an intervention of last resort. However, if stocking is deemed essential, brood stock should originate from the river to be stocked.

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References

  • Aljanabi SM, Martinez I (1999) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693

    Article  Google Scholar 

  • Baker CS, Medrano-Gonzalez L, Calambokidis J, Perry A, Pichler F, Rosenbaum H, Straley JM, Urban-Ramirez J, Yamaguchi M, Von Ziegesar O (1998) Population structure of nuclear and mitochondrial DNA variation among humpback whales in the North Pacific. Mol Ecol 7:695–707

    Article  PubMed  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Bergerot B, Lasne E, Vigneron T, Laffaille P (2008) Prioritization of fish assemblages with a view to conservation and restoration on a large scale European basin, the Loire (France). Biodivers Conserv 9:2247–2262

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Dawnay N, McEwing R, Thorpe RS, Ogden R (2008) Preliminary data suggests genetic distinctiveness of gyr and saker falcons. Conserv Genet 9:703–707

    Article  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. P Natl Acad Sci-Biol 91:3166–3170

    Google Scholar 

  • Duchesne P, Turgeon J (2009) FLOCK: a method for quick mapping of admixture without source samples. Mol Ecol Resour 9:1333–1344

    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 542:121–1297

    Article  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (2004) PHYLIP (phylogeny inference package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Franklin IA (1980) Evolutionary changes in small populations. In: Soule M, Wilcox BA (eds) Conservation biology: an evolutionary and ecological perspective. Sinauer Associates, Sunderland, Massachusett, pp 135–150

    Google Scholar 

  • Freyhof J, Kottelat M (2008) Thymallus thymallus. In: IUCN 2009. IUCN red list of threatened species, Version 2009.1. www.iucnredlist.org. Accessed 10 Oct 2009

  • Gardiner (1989) The distribution of grayling. In: Broughton R (ed) Grayling: the fourth game fish. The Crowood Press, Wiltshire

    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, Kühn R, Baars M, Schröder 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 

  • Gum B, Gross R, Rottmann O, Schröder, Kühn (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  PubMed  CAS  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(Suppl C):115–135

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Ibbotson AT, Cove RJ, Ingraham A, Gallagher M, Hornby DD, Furse M, Williams C (2001) A review of grayling ecology, status and management practice: recommendations for future management in England and Wales. R&D Technical Report W245. Environment Agency and Centre for Ecology and Hydrology

  • IUCN Red List of Threatened Species (2008) (http://www.iucnredlist.org/). Accessed on 26th Sept 2008

  • 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Koskinen MT, Knizhin I, Primmer CR, Schlötterer 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  PubMed  CAS  Google Scholar 

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

  • Lelek A (1984) Threatened fishes of Europe. In: European committee for the conservation of nature and natural resources. Council of Europe. The Freshwater Fishes of Europe 9 AULA-Verlag, Weisbaden

  • Mayr E (1954) Change of genetic environment and evolution. In: Huxley JS, Hardy AC, Ford EB (eds) Evolution as a process. Allen and Unwin, London

    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 14:735–747

    Article  Google Scholar 

  • Moritz C (1994) Defining ‘evolutionary significant units’ for conservation. TREE 9:373–375

    PubMed  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 

  • Olsen JB, Bentzen P, Seeb JE (1998) Characterization of seven microsatellite loci derived from pink salmon. Mol Ecol 7:1087–1089

    PubMed  CAS  Google Scholar 

  • 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 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudoin L, Estoup A (2004) GeneClass2: a software for the genetic assignment and first generation migrant detection. J Hered 95:536–539

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure from multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  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 

  • Regan CT (1911) The freshwater fishes of the British Isles. Methuen, London

    Google Scholar 

  • Reiman BE, Allendorf FW (2001) Effective population size and genetic conservation criteria for bull trout. North Am J Fish Manag 21:756–764

    Article  Google Scholar 

  • Rosenburg NA (2004) Distruct: a program for the graphical display of population structure. Centre of Computational Medicine and Biology, Department of Human Genetics, University of Michigan, MI, USA

    Google Scholar 

  • Saiki RK, Scharf S, Faloona F, Mullis KB, Horn GT, Erlich HA, Arnheim N (1985) Enzymatic amplification of beta-globin genomic sequences and restriction site analyses for diagnosis of sickle-cell anemia. Science 230:1350–1354

    Article  PubMed  CAS  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labelling of PCR fragments. Nat Biotechnol 18:233–234

    Article  PubMed  CAS  Google Scholar 

  • Scribner KT, Gust JR, Fields RL (1996) Isolation and characterization of novel microsatellite loci: cross-species amplification and population genetic applications. Can J Fish Aquat Sci 53:833–841

    Article  CAS  Google Scholar 

  • Sušnik S, Snoj A, Dovc P (1999a) Microsatellites in grayling (Thymallus thymallus): comparison of two geographically remote populations from the Danubian and Adriatic river basin in Slovenia. Mol Ecol 8:1756–1758

    Article  PubMed  Google Scholar 

  • Sušnik S, Snoj A, Dovc P (1999b) A new set of microsatellite markers for grayling: BFRO014, BFRO015, BFRO016, BFRO017 and BFRO018. Anim Genet 30:478

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Swatdipong A, Primmer CR, Vasemag A (2010) Historical and recent genetic bottlenecks in European grayling, Thymallus thymallus. Conserv Genet 11:279–292. doi:10.1007/s10592-009-0031-x

    Article  Google Scholar 

  • Taberlet P, Bouvet J (1994) Mitochondrial DNA polymorphism, phylogeography, and conservation genetics of the brown bear Ursus arctos in Europe. Proc R Soc Lond B 255:195–200

    Article  CAS  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 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. 111. Cladogram estimation. Genetics 132:619–633

    PubMed  CAS  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(supp A):223–247

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-Statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Weiss S, Persat H, Eppe R, Schlötterer C, Uiblein F (2002) Complex patterns of colonization and refugia revealed for European Grayling Thymallus thymallus, based on complete sequencing of the mitochondrial DNA control region. Mol Ecol 11:1393–1407

    Article  PubMed  CAS  Google Scholar 

  • Werle E, Schneider CS, Renner M, Volker M, Fiehn W (1994) Convenient single-step, one tube purification of PCR product for direct sequencing. Nucleic Acids Res 22:4354–4355

    Article  PubMed  CAS  Google Scholar 

  • Wheeler A (1977) The origin and distribution of the freshwater fishes of the British Isles. J Biogeogr 4:1–24

    Article  Google Scholar 

  • Wilson TK (1963) How our rivers got their grayling. Fishing, June, 9–10

  • Wilson TK (1966) Trout by all means. Angling Times, Peterborough

  • Youngson AF, Jordan WC, Verspoor E, McGinnity P, Cross T, Ferguson A (2003) Management of salmonid fisheries in the British Isles: towards a practical approach based on population genetics. Fish Res 62:193–209

    Article  Google Scholar 

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Acknowledgements

The authors would wish to thank The Grayling Society and the Environment Agency for funding MIT and ND, and coordinating sample collection. We would also like to thank the anglers who caught samples for the project.

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  1. Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, Bangor University, ECW Building, Bangor, Gwynedd, LL57 2UW, UK

    Nick Dawnay, Louise Dawnay, Roger N. Hughes & Martin I. Taylor

  2. Environment Agency, Chester Road Buckley, Flintshire, CH7 3AJ, UK

    Richard Cove

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  1. Nick Dawnay
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Correspondence to Martin I. Taylor.

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Dawnay, N., Dawnay, L., Hughes, R.N. et al. Substantial genetic structure among stocked and native populations of the European grayling (Thymallus thymallus, Salmonidae) in the United Kingdom. Conserv Genet 12, 731–744 (2011). https://doi.org/10.1007/s10592-010-0179-4

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