Skip to main content
Log in

Analysis of gene associated tandem repeat markers in Atlantic salmon (Salmo salar L.) populations: implications for restoration and conservation in the Baltic Sea

  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Patterns of genetic diversity and differentiation among five wild and four hatchery populations of Atlantic salmon in the Baltic Sea were assessed based on eight assumedly neutral microsatellite loci and six gene-associated markers, including four expressed sequence tag (EST) linked and two major histocompatibility complex (MHC) linked tandem repeat markers (micro- and mini-satellites). The coalescent simulations based on the method of Beaumont and Nichols (1996, Proc. R. Soc. Lond. Ser. B – Biol. Sci., 263, 1619–1626) indicated that two loci (MHCIIα and Ssa171, with the lowest and highest overall FST estimates, respectively) exhibited significant departures (P<0.05) from the neutral expectations. Another coalescent-based test for selective neutrality (Vitalis et al. 2001, Genetics, 158, 1811–1823) further supported the outlier status of the Ssa171 microsatellite locus but not of the MHCIIα linked minisatellite. In addition, actin related protein linked microsatellite locus was identified with this test as an outlier in six pairwise population comparisons. All genetic diversity estimates revealed more genetic variation in hatchery stocks than in the small wild salmon populations from the Gulf of Finland. However, the wild populations possessed alleles at gene-associated markers (e.g. MHCI and IGF) not found in the hatchery stocks, which together with moderate genetic differentiation and distinctive environmental conditions justifies the special conservation measures for the last remaining native salmon populations in the Gulf of Finland.

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.

Similar content being viewed by others

References

  • MD Adkison (1995) ArticleTitlePopulation differentiation in Pacific salmon: local adaptation, genetic drift, or the environment? Can. J. Fish. Aquat. Sci. 52 2762–2777

    Google Scholar 

  • JM Akey G Zhang K Zhang L Jin MD Shriver (2002) ArticleTitleInterrogating a high-density SNP map for signatures of natural selection Genome Res. 12 1805–1814

    Google Scholar 

  • Altukhov YP, Salmenkova EA, Omelchenko VT (2000) Salmonid Fishes. Population Biology, Genetics and Management. Blackwell Science Ltd, Oxford

  • CJ Bayne L Gerwick K Fujiki M Nakao T Yano (2001) ArticleTitleImmune-relevant (including acute phase) genes identified in the livers of rainbow trout, Oncorhynchus mykiss, by means of suppression subtractive hybridization Dev. Comp. Immunol. 25 205–217

    Google Scholar 

  • MA Beaumont RA Nichols (1996) ArticleTitleEvaluating loci for use in the genetic analysis of population structure Proc. R. Soc. Lond. Ser. B – Biol. Sci. 263 1619–1626

    Google Scholar 

  • G Benson (1999) ArticleTitleTandem repeats finder: a program to analyze DNA sequences Nucleic Acids Res. 27 573–580

    Google Scholar 

  • L Bernatchez C Landry (2003) ArticleTitleMHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J. Evolution Biol. 16 363–377

    Google Scholar 

  • K Buchmann JL Larsen B Therkildsen (2001) ArticleTitleImproved recapture rate of vaccinated sea-ranched Atlantic salmon, Salmo salar L J. Fish Dis. 24 245–248

    Google Scholar 

  • SL Clifford P McGinnity A Ferguson (1998) ArticleTitleGenetic changes in an Atlantic salmon population resulting from escaped juvenile farm salmon J. Fish Biol. 52 118–127

    Google Scholar 

  • CC Cockerham BS Weir (1993) ArticleTitleEstimation of gene flow from F-statistics Evolution 47 855–863

    Google Scholar 

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

    Google Scholar 

  • GC Davey NC Caplice SA Martin R Powell (2001) ArticleTitleA survey of genes in the Atlantic salmon (Salmo salar) as identified by expressed sequence tags Gene 263 121–130

    Google Scholar 

  • K Elo (1993) ArticleTitleGene flow and conservation of genetic variation in anadromous Atlantic salmon (Salmo salar) Hereditas 119 149–159

    Google Scholar 

  • D Garant JJ Dodson L Bernatchez (2000) ArticleTitleEcological determinants and temporal stability of the within- river population structure in Atlantic salmon (Salmo salar L.) Mol. Ecol. 9 615–628

    Google Scholar 

  • JC Gower (1971) Statistical methods of comparing different multivariate analyses of the same data F R Hodson DG Kendall P Tautu (Eds) Mathematics in the Archaeological and Historical Sciences Edinburgh University Press Edinburgh 138–149

    Google Scholar 

  • U Grimholt F Drablos SM Jorgensen B Hoyheim RJM Stet (2002) ArticleTitleThe major histocompatibility class I locus in Atlantic salmon (Salmo salar L.): polymorphism, linkage analysis and protein modelling Immunogenetics 54 570–581

    Google Scholar 

  • U Grimholt A Getahun T Hermsen RJM Stet (2000) ArticleTitleThe major histocompatibility class II alpha chain in salmonid fishes Dev. Comp. Immunol. 24 751–763

    Google Scholar 

  • U Grimholt I Hordvik VM Fosse I Olsaker C Endresen O Lie (1993) ArticleTitleMolecular-cloning of major histocompatibilitycomplex class-I cDNAs from Atlantic salmon (Salmo salar) Immunogenetics 37 469–473

    Google Scholar 

  • U Grimholt S Larsen R Nordmo P Midtlyng S Kjoeglum A Storset S Saebo RJM Stet (2003) ArticleTitleMHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci Immunogenetics 4 210–219

    Google Scholar 

  • R Gross J Nilsson (1999) ArticleTitleRestriction fragment length polymorphism at the growth hormone 1 gene in Atlantic salmon (Salmo salar L.) and its association with weight among the offspring of a hatchery stock Aquaculture 173 73–80

    Google Scholar 

  • SW Guo EA Thompson (1992) ArticleTitlePerforming the exact test for Hardy–Weinberg proportion for multiple alleles Biometrics 48 361–372

    Google Scholar 

  • MM Hansen DE Ruzzante EE Nielsen KLD Mensberg (2000) ArticleTitleMicrosatellite and mitochondrial DNA polymorphism reveals life-history dependent interbreeding between hatchery and wild brown trout (Salmo trutta L.) Mol. Ecol. 9 583–594

    Google Scholar 

  • PW Hedrick (2002) ArticleTitlePathogen resistance and genetic variation at MHC loci Evolution 56 1902–1908

    Google Scholar 

  • ICES (2003) Report of the Baltic salmon and trout assessment working group in Karlskrona, Sweden, 2–11 April 2003. ICES CM 2003/ACFM: 20

  • DA Jackson (1993) ArticleTitleMultivariate-analysis of benthic invertebrate communities - the implication of choosing particular data standardizations, measures of association, and ordination methods Hydrobiologia 268 9–26

    Google Scholar 

  • M Kangur M-L Viilmann (2001) Habitat fish and fisheries B Wahlberg M Kangur (Eds) Present and Potential Production of Salmon in Estonian Rivers Estonian Academy Publishers Tallinn 32–69

    Google Scholar 

  • TL King ST Kalinowski WB Schill AP Spidle BA Lubinski (2001) ArticleTitlePopulation structure of Atlantic salmon (Salmo salar L.): a range-wide perspective from microsatellite DNA variation Mol. Ecol. 10 807–821

    Google Scholar 

  • A Klemetsen P-A Amundsen JB Dempson B Jonsson N Jonsson MF O’Connell E Mortensen (2003) ArticleTitleAtlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories Ecol. Freshw. Fish 12 1–59

    Google Scholar 

  • ML Koljonen H Jansson T Paaver O Vasin J Koskiniemi (1999) ArticleTitlePhylogeographic lineages and differentiation pattern of Atlantic salmon (Salmo salar) in the Baltic Sea with management implications Can. J. Fish. Aquat. Sci. 56 1766–1780

    Google Scholar 

  • ML Koljonen J Tahtinen M Saisa J Koskiniemi (2002) ArticleTitleMaintenance of genetic diversity of Atlantic salmon (Salmo salar) by captive breeding programmes and the geographic distribution of microsatellite variation Aquaculture 212 69–92

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • C Landry L Bernatchez (2001) ArticleTitleComparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite␣loci in Atlantic salmon (Salmo salar) Mol. Ecol. 10 2525–2539

    Google Scholar 

  • C Landry D Garant P Duchesne L Bernatchez (2001) ArticleTitle’Good genes as heterozygosity’: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar) Proc. R. Soc. Lond. Ser. B – Biol. Sci. 268 1279–1285

    Google Scholar 

  • A Langefors J Lohm M Grahn O Andersen T Schantz Particlevon (2001) ArticleTitleAssociation between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon Proc. R. Soc. Lond. Ser. B – Biol. Sci. 268 479–485

    Google Scholar 

  • J Lohm M Grahn A Langefors O Andersen A Storset T Schantz Particlevon (2002) ArticleTitleExperimental evidence for major histocompatibility complex- allele-specific resistance to a bacterial infection Proc. R. Soc. Lond. Ser. B – Biol. Sci. 269 2029–2033

    Google Scholar 

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

    Google Scholar 

  • SA Martin NC Caplice GC Davey R Powell (2002) ArticleTitleEST-based identification of genes expressed in the liver of adult Atlantic salmon (Salmo salar) Biochem. Biophys. Res. Commun. 293 578–585

    Google Scholar 

  • KM Miller JR Winton AD Schulze MK Purcell TJ Ming (2004) ArticleTitleMajor histocompatibility complex loci are associated with susceptibility of Atlantic salmon to infectious hematopoietic necrosis virus Environ. Biol. Fish. 69 307–316

    Google Scholar 

  • P Moran (2002) ArticleTitleCurrent conservation genetics: building an ecological approach to the synthesis of molecular and quantitative genetic methods Ecol. Freshw. Fish 11 30–55

    Google Scholar 

  • M Nei F Tajima Y Tateno (1983) ArticleTitleAccuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data J. Mol. Evol. 19 153–170

    Google Scholar 

  • RA Nichols MW Bruford JJ Groombridge (2001) ArticleTitleSustaining genetic variation in a small population: evidence from the Mauritius kestrel Mol. Ecol. 10 593–602

    Google Scholar 

  • EE Nielsen MM Hansen V Loeschcke (1999) ArticleTitleGenetic variation in time and space: microsatellite analysis of extinct and␣extant populations of Atlantic salmon Evolution 53 261–268

    Google Scholar 

  • J Nilsson R Gross T Asplund O Dove H Jansson J Kelloniemi K Kohlmann A Loytynoja EE Nielsen T Paaver CR Primmer S Titov A Vasemagi A Veselov T Ost J Lumme (2001) ArticleTitleMatrilinear phylogeography of Atlantic salmon (Salmo salar L.) in Europe and postglacial colonization of the Baltic Sea area Mol. Ecol. 10 89–102

    Google Scholar 

  • AT Norris DG Bradley EP Cunningham (1999) ArticleTitleMicrosatellite genetic variation between and within farmed and wild Atlantic salmon (Salmo salar) populations Aquaculture 180 247–264

    Google Scholar 

  • PT O’Reilly LC Hamilton SK McConnell JM Wright (1996) ArticleTitleRapid analysis of Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites Can. J. Fish. Aquat. Sci. 53 2292–2298

    Google Scholar 

  • RDM Page (1996) ArticleTitleTREEVIEW: an application to display phylogenetic trees on personal computers Computer Appl. Biosci. 12 357–358

    Google Scholar 

  • PR Peres-Neto DA Jackson (2001) ArticleTitleHow well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test Oecologia 129 169–178

    Google Scholar 

  • VD Pillar (1999) ArticleTitleThe bootstrapped ordination re-examined J.␣Veg. Sci. 10 895–902

    Google Scholar 

  • S Piry G Luikart JM Cornuet (1999) ArticleTitleBOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data J.␣Hered. 90 502–503

    Google Scholar 

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

    Google Scholar 

  • M Raymond F Rousset (1995a) ArticleTitleGENEPOP (Version 1.2): a population genetics software for exact tests and ecumenism J. Hered. 86 248–249

    Google Scholar 

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

    Google Scholar 

  • WR Rice (1989) ArticleTitleAnalysing tables of statistical tests Evolution 43 223–225

    Google Scholar 

  • S Rozen HJ Skaletsky (2000) Primer3 on the WWW for general users and for biologist programmers S Krawetz S Misener (Eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology Humana Press Totowa NJ 365–386

    Google Scholar 

  • A Slettan I Olsaker Ø Lie (1995) ArticleTitleAtlantic salmon, Salmo salar, microsatellites at the SSOSL25, SSOSL85, SSOSL311, SSOSL417 loci Anim. Genet. 26 277–285

    Google Scholar 

  • Schneider S, Kueffer J-M, Roessli D, Excoffie L (1997) Arlequin. Version 1.1. Genetics and Biometry Laboratory, Department of Anthropology, University of Geneva, Switzerland

  • WJ Tao EG Boulding (2003) ArticleTitleAssociations between single nucleotide polymorphisms in candidate genes and growth rate in Arctic charr (Salvelinus alpinus L.) Heredity 1 60–69

    Google Scholar 

  • EB Taylor (1991) ArticleTitleA review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon Aquaculture 98 185–207

    Google Scholar 

  • N Tessier L Bernatchez JM Wright (1997) ArticleTitlePopulation structure and impact of supportive breeding inferred from mitochondrial and microsatellite DNA analyses in land-locked Atlantic salmon Salmo salar L Mol. Ecol. 6 735–750

    Google Scholar 

  • PH Tienderen Particlevan AA Haan Particlede CG Linden Particlevan der B Vosman (2002) ArticleTitleBiodiversity assessment using markers for ecologically important traits Trends Ecol. Evol. 17 577–582

    Google Scholar 

  • A Vasemägi R Gross T Paaver M Kangur J Nilsson LO Eriksson (2001) ArticleTitleIdentification of the origin of Atlantic salmon (Salmo salar L.) population in a recently recolonized river in the Baltic Sea Mol. Ecol. 10 2877–2882

    Google Scholar 

  • A Vasemägi J Nilsson CR Primmer (2005) ArticleTitleExpressed sequence tag (EST) linked microsatellites as a source of gene associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Mol. Biol. Evol. 22 1067–1076

    Google Scholar 

  • R Vitalis K Dawson P Boursot (2001) ArticleTitleInterpretation of variation across marker loci as evidence of selection Genetics 158 1811–1823

    Google Scholar 

  • R Vitalis K Dawson P Boursot K Belkhir (2003) ArticleTitleDetSel 1.0: a computer program to detect markers responding to selection J. Hered. 94 429–431

    Google Scholar 

  • ML Wayne LM McIntyre (2002) ArticleTitleCombining mapping and arraying: an approach to candidate gene identification Proc. Natl. Acad. Sci. USA 99 14903–14906

    Google Scholar 

  • RS Waples (1989) ArticleTitleA generalised approach for estimating effective population size from temporal changes in allele frequency Genetics 121 379–391

    Google Scholar 

  • BS Weir CC Cockerham (1984) ArticleTitleEstimating F-statistics for the analysis of population structure Evolution 38 1358–1370

    Google Scholar 

  • KM Wegner TBH Reusch M Kalbe (2003) ArticleTitleMultiple parasites are driving major histocompatibility complex polymorphism in the wild J. Evol. Biol. 16 224–232

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anti Vasemägi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vasemägi, A., Gross, R., Paaver, T. et al. 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 (2005). https://doi.org/10.1007/s10592-005-4974-2

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-005-4974-2

Key words:

Navigation