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.
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References
MD Adkison (1995) ArticleTitlePopulation differentiation in Pacific salmon: local adaptation, genetic drift, or the environment? Can. J. Fish. Aquat. Sci. 52 2762–2777
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
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
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
G Benson (1999) ArticleTitleTandem repeats finder: a program to analyze DNA sequences Nucleic Acids Res. 27 573–580
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
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
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
CC Cockerham BS Weir (1993) ArticleTitleEstimation of gene flow from F-statistics Evolution 47 855–863
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
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
K Elo (1993) ArticleTitleGene flow and conservation of genetic variation in anadromous Atlantic salmon (Salmo salar) Hereditas 119 149–159
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
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
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
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
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
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
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
SW Guo EA Thompson (1992) ArticleTitlePerforming the exact test for Hardy–Weinberg proportion for multiple alleles Biometrics 48 361–372
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
PW Hedrick (2002) ArticleTitlePathogen resistance and genetic variation at MHC loci Evolution 56 1902–1908
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
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
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
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
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
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
MT Koskinen TO Haugen CR Primmer (2002) ArticleTitleContemporary fisherian life-history evolution in small salmonid populations Nature 419 826–830
PW Laird A Zijderveld K Linders MA Rudnicki R Jaenisch A Berns (1991) ArticleTitleSimplified mammalian DNA isolation procedure Nucleic Acids Res. 19 4293
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
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
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
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
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
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
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
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
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
RA Nichols MW Bruford JJ Groombridge (2001) ArticleTitleSustaining genetic variation in a small population: evidence from the Mauritius kestrel Mol. Ecol. 10 593–602
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
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
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
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
RDM Page (1996) ArticleTitleTREEVIEW: an application to display phylogenetic trees on personal computers Computer Appl. Biosci. 12 357–358
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
VD Pillar (1999) ArticleTitleThe bootstrapped ordination re-examined J.␣Veg. Sci. 10 895–902
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
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
M Raymond F Rousset (1995a) ArticleTitleGENEPOP (Version 1.2): a population genetics software for exact tests and ecumenism J. Hered. 86 248–249
M Raymond F Rousset (1995b) ArticleTitleAn exact test for population differentiation Evolution 49 1280–1283
WR Rice (1989) ArticleTitleAnalysing tables of statistical tests Evolution 43 223–225
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
A Slettan I Olsaker Ø Lie (1995) ArticleTitleAtlantic salmon, Salmo salar, microsatellites at the SSOSL25, SSOSL85, SSOSL311, SSOSL417 loci Anim. Genet. 26 277–285
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
EB Taylor (1991) ArticleTitleA review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon Aquaculture 98 185–207
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
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
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
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
R Vitalis K Dawson P Boursot (2001) ArticleTitleInterpretation of variation across marker loci as evidence of selection Genetics 158 1811–1823
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
ML Wayne LM McIntyre (2002) ArticleTitleCombining mapping and arraying: an approach to candidate gene identification Proc. Natl. Acad. Sci. USA 99 14903–14906
RS Waples (1989) ArticleTitleA generalised approach for estimating effective population size from temporal changes in allele frequency Genetics 121 379–391
BS Weir CC Cockerham (1984) ArticleTitleEstimating F-statistics for the analysis of population structure Evolution 38 1358–1370
KM Wegner TBH Reusch M Kalbe (2003) ArticleTitleMultiple parasites are driving major histocompatibility complex polymorphism in the wild J. Evol. Biol. 16 224–232
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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
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DOI: https://doi.org/10.1007/s10592-005-4974-2