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Microsatellite variation in Bavarian populations of European grayling (Thymallus thymallus): Implications for conservation

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Abstract

European grayling populations in Bavaria have shown steady declines during the last 10–20years. In order to provide guidelines for conservation strategies and future management programs, we investigated the genetic structure of 15 grayling populations originating from three major Central European drainages (the Danube, the Elbe and the Rhine/Main) using 20 microsatellite loci. Genetic divergence between the three drainage systems was substantial as illustrated by highly significant heterogeneity of genotype frequencies, high number of drainage-specific private alleles, high between-drainage F ST values, high assignment success of individuals to their drainage of origin and the high bootstrap support for the genetic distance based drainage-specific population clusters. In agreement with earlier studies, microsatellites revealed relatively low levels of intrapopulational genetic diversity in comparison to the overall level of variation across populations. Maximum likelihood methods using the coalescent approach revealed that the proportion of common ancestors was generally high in native populations and that the estimates of N e were correlated with the genetic diversity parameters in all drainages. The number of effective immigrants per generation (N e m) was less than one for all pairwise comparisons of populations within the drainages, indicating restricted interpopulational gene flow. Based on these findings we recommend a drainage and sub-drainage specific conservation of grayling populations in order to preserve their overall genetic diversity and integrity. For large-scale stocking actions to supplement declining or to restore extinct populations, creation of separate broodstocks for major conservation units (ESUs and MUs) is warranted.

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References

  • Beerli P (2002) MIGRATE: Documentation and Program, part of LAMARC, version 1.6.9. Available at http://evolution.genetics. washington.edu/lamarc.html

  • 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. Nat. Acad. Sci. USA, 98, 8, 4563–4568.

    Article  PubMed  CAS  Google Scholar 

  • Bernatchez L, Wilson CC (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Mol. Ecol., 7, 431–451.

    Article  Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: Models and estimation procedures. Am. J. Hum. Genet., 19, 233–257.

    PubMed  CAS  Google Scholar 

  • Ciofi C, Beaumont MA, Swingland IR, Bruford MW(1999) Genetic divergence and units for conservation in the Komodo dragon Varanus komodoensis. Proc. R. Sco. Lond B., 266, 2269–2274. 2MOD programme available at: http://www.rubic.rdg.ac.uk/~mab/software.Html

    Article  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 

  • Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics, 153, 1989–2000.

    PubMed  CAS  Google Scholar 

  • DeWoody JA, Avise JC (2000). Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J. Fish Biol., 56, 461–473.

    Article  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479–491. ARLEQUIN v. 2.00 available at: http://lgb.unige.ch/arlequin/

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1994) PHYLIP (Phylogeny Inference Package), v. 3.572c. Department of Genetics, University of Washington, Seattle. Available at: http://evolution.genetics.washington.edu/ phylip.html

    Google Scholar 

  • Goudet J (2001) FSTAT, a Program to Estimate and Test Gene Diversities and Fixation Indices (version 2.9.3). Available at http://www.unil.ch/izea/softwares/fstat.html

  • Gross R, Kϋhn 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 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics, 48, 361–372.

    Article  PubMed  CAS  Google Scholar 

  • Hänfling B, Brandl, R (1998) Genetic and morphological variation in a common European cyprinid, Leuciscus cephalus within and across Central European drainages. J. Fish Biol., 52, 706–715.

    Google Scholar 

  • Hänfling B, Hellemans B, Volckaert FA, Carvalho GR (2002) Late glacial history of the cold-adapted freshwater fish Cottus gobio, revealed by microsatellites. Mol. Ecol., 11, 1717–1729.

    Article  PubMed  Google Scholar 

  • Hantke R (1993) Flussgeschichte Mitteleuropas. Ferdinand Enke-Verlag. Stuttgart.

    Google Scholar 

  • Koskinen MT, Primmer CR (1999) Cross-species amplification of salmonid microsatellites which reveal polymorphism in European and Arctic grayling, Salmonidae: Thymallus spp. Hereditas, 131, 171–176.

    Article  PubMed  CAS  Google Scholar 

  • 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, Primmer CR (2001a) High throughput analysis of 17 microsatellite loci grayling (Thymallus spp. Salmonidae). Cons. Genet., 2, 173–177.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Koskinen MT, Nilsson J, Veselov A, Potutkin AG, Ranta E, Primmer CR (2002a) Microsatellite data resolve phylogeographic patterns in European grayling, Thymallus thymallus, Salmonidae. Heredity, 88, 391–402.

    Article  PubMed  CAS  Google Scholar 

  • Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, Berns A (1991) Simplified mammalian DNA isolation procedure. Nucl. Acids Res., 19, 4293.

    PubMed  CAS  Google Scholar 

  • Minch E, Ruiz-Linares A, Goldstein D, Feldman M, Cavalli-Sforza LL (1996). Microsat (v. 1.5): A Computer Program for Calculating Various Statistics on Microsatellite Allele Data. Stanford University Medical Center, Stanford, CA. Available at: http://hpgl.stanford.edu/projects/microsat/microsat.html

  • Moritz C (1994) Defining ‘evolutionary significant units’ for conservation. Trends Ecol. Evol., 9, 373–375.

    Article  Google Scholar 

  • Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.

    Google Scholar 

  • Nesbo CL, Fossheim T, Vollestad LA, Jakobsen KS (1999) Genetic divergence and phylogeographic relationships among European perch (Perca fluviatilis) populations reflect glacial refugia and postglacial colonization. Mol. Ecol., 8, 1387–1404.

    Article  PubMed  CAS  Google Scholar 

  • Northcote TG (1995) Comparative biology and management of Arctic and European grayling (Salmonidae, Thymallus). Rev. Fish Biol., 5, 141–194.

    Article  Google Scholar 

  • Ohta T (1982) Population genetics of multigene families. Adv. Biophys., 15, 173–179.

    Article  PubMed  CAS  Google Scholar 

  • Persat H (1996) Threatened populations and conservation of European grayling, Thymallus thymallus (L., 1758). In: Conservation of Endangered Freshwater Fish in Europe (eds. Kirchhofer A, Hefti D), pp. 233–247. Birkhäuser Verlag, Basel.

    Google Scholar 

  • Piry S, Cornuet JM (1999) GeneClass. A Program for Assignation and Exclusion Using Molecular Markers. URLB/INRA, France. Available at: http://www.ensam.inra.fr/URLB/geneclass/ geneclass.html

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: A computer programme for detecting recent reductions in the effective population size using allele frequency data. J. Heredity, 90, 502–503. Available at: http://www.ensam.inra.fr/URLB/bottleneck/ bottleneck.html

    Article  Google Scholar 

  • Raymond M, Rousset F (1995a) GENEPOP: Population genetics software for exact tests and ecumenicism. J. Heredity, 86, 248–249. Available at: ftp://ftp.cefe.cnrs-mop.fr/pub/pc/msdos/ genepop

    Google Scholar 

  • Raymond M, Rousset F (1995b) An exact test for population differentiation. Evolution, 49, 1280–1283.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ryder OA (1986) Species conservation and systematics: The dilemma of subspecies. Trends Ecol. Evol., 1, 9–10.

    Article  Google Scholar 

  • Schug MD, Mackay TFC, Aquadro CF (1997) Low mutation rates of microsatellite loci in Drosophila melangogaster. Nat. Gen., 15, 99–102.

    Article  CAS  Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical Taxonomy. Freeman, San Francisco, CA.

    Google Scholar 

  • Snoj A, Susnik S, Pohar J, Dovc P (1999) The first microsatellite marker (BFRO004) for grayling, informative for its Adriatic population. Anim. Genet., 30, 74–75.

    Article  PubMed  CAS  Google Scholar 

  • Stein H, Born O (1999) Grϋnes Licht fϋr das Artenhilfsprogramm Äsche. Erstes Artenhilfsprogramm in Bayern für eine gefährdete Fischart initiiert. Fischer und Teichwirt, 50, 179–182.

    Google Scholar 

  • Stein H, Baars M, Mathes E, SteinhÖrster U (2001) Die Äsche: Thymallus thymallus. 1. Aufl. Die Neue Brehm-Bücherei Bd. 640, Westarp Wissenschaften, Hohenwarsleben, Germany.

  • Susnik 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  CAS  Google Scholar 

  • Susnik S, Snoj A, Dovc P (1999b) A new set of microsatellite markers for grayling: BFRO014, BFRO015, BFRO016, BFRO017 and BFRO018. Anim. Genet., 30, 462–478.

    Article  Google Scholar 

  • Susnik S, Snoj A, Jesensek D, Dovc P (2000) Microsatellite DNA markers (BFRO010 and BFRO011) for grayling. J. Anim. Sci., 78, 488–489.

    PubMed  CAS  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. Linnean Soc., 74, 375–385.

    Article  Google Scholar 

  • Takezaki N, Nei M (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics, 144, 389–399.

    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(Supplement A), 223–247.

    Google Scholar 

  • Vrijenhoek RC (1994) Genetic diversity and fitness in small populations. In: Conservation Genetics (eds Loeschke V, Tomiuk J, Jain SK), pp. 37–53. Birkhäuser Verlag, Basel.

    Google Scholar 

  • Wang J, Ryman N (2001) Genetic effects of multiple generations of supportive breeding. Conserv. Biol., 15, 1619–1631.

    Article  Google Scholar 

  • Waples RS (1991) Pacific Salmon, Oncorhynchus spp. and the definition of ‘species’ under the endangered species act. Mar. Fish. Rev., 53, 11–22.

    Google Scholar 

  • Weber JL, Wong C (1993) Mutation of human short tandem repeats. Hum. Mol. Gen., 2, 1123–1128.

    PubMed  CAS  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 

  • Wright S (1969) Evolution and the Genetics of Populations, Vol. 2, The Theory of Gene Frequencies. University of Chicago Press, Chicago and London.

    Google Scholar 

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Authors and Affiliations

  1. Wildlife Biology and Management Unit, Department for Ecosystem and Landscape Management, Technical University Munich-Weihenstephan, 85354, Freising, Germany

    Bernhard Gum, Wolf Schröder & Ralph Kühn

  2. Institute of Animal Science, Estonian Agricultural University, EE-51014, Tartu, Estonia

    Riho Gross

  3. Department for Animal Sciences, Technical University Munich-Weihenstephan, 85354, Freising, Germany

    Oswald Rottmann

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  1. Bernhard Gum
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  2. Riho Gross
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  4. Wolf Schröder
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  5. Ralph Kühn
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Correspondence to Ralph Kühn.

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Gum, B., Gross, R., Rottmann, O. et al. Microsatellite variation in Bavarian populations of European grayling (Thymallus thymallus): Implications for conservation. Conservation Genetics 4, 659–672 (2003). https://doi.org/10.1023/B:COGE.0000006106.64243.e6

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