Skip to main content
SpringerLink
Log in

Contrasting patterns of gene diversity between microsatellites and mitochondrial SNPs in farm and wild Atlantic salmon

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Levels of genetic variability at 12 microsatellite loci and 19 single nucleotide polymorphisms in mitochondrial DNA were studied in four farm strains and four wild populations of Atlantic salmon. Within populations, the farm strains showed significantly lower allelic richness and expected heterozygosity than wild populations at the 12 microsatellite loci, but a significantly higher genetic variability with respect to observed number of haplotypes and haplotype diversity in mtDNA. Significant differences in allele- and haplotype-frequencies were observed between farm strains and wild populations, as well as between different farm strains and between different wild populations. The large genetic differentiation at mitochondrial DNA between wild populations (FST = 0.24), suggests that the farm strains attained a high mitochondrial genetic variability when created from different wild populations seven generations ago. A large proportion of this variability remains despite an expected lower effective population size for mitochondrial than nuclear DNA. This is best explained by the particular mating schemes in the breeding programmes, with 2–4 females per male. Our observations suggest that for some genetic polymorphisms farm populations might currently hold equal or higher genetic variability than wild populations, but lower overall genetic variability. In the short-term, genetic interactions between escaped farm salmon and wild salmon might increase genetic variability in wild populations, for some, but not most, genetic polymorphisms. In the long term, further losses of genetic variability in farm populations are expected for all genetic polymorphisms, and genetic variability in wild populations will be reduced if escapes of farm salmon continue.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Allendorf FW, Ryman N (1987) Genetic management of hatchery stocks. In: Ryman N, Utter F (eds) Population genetics and fishery management. Univ Washington Press, Seattle, USA, pp 141–159

    Google Scholar 

  • Cairney M, Taggart JB, Hoyheim B (2000) Characterization of microsatellite and minisatellite loci in Atlantic salmon (Salmo salar L.) and cross-species amplification in other salmonids. Molec Ecol 9:2175–2178

    Article  CAS  Google Scholar 

  • Ciborowski KL, Conseguera S, García de Leániz C, Wang J, Beaumont MA, Jordan WC (2007) Stocking may increase mitochondrial DNA diversity but fails to halt the decline of endangered Atlantic salmon populations. Conserv Genet 8:1355–1367

    Article  CAS  Google Scholar 

  • Clifford SL, McGinnity P, Ferguson A (1998) Genetic changes in Atlantic salmon (Salmo salar) populations of Northwest Irish rivers resulting from escapes of adult farm salmon. Can J Fish Aquat Sci 55:358–363

    Article  Google Scholar 

  • Consuegra S, Verspoor E, Knox D, García de Leániz C (2005) Asymmetric gene flow and the evolutionary maintenance of genetic diversity in small, peripheral Atlantic salmon populations. Conserv Genet 6:823–842

    Article  CAS  Google Scholar 

  • Dowling TE, Minckley WL, Marsh PC, Goldstein ES (1996) Mitochondrial DNA variability in the endangered Razorback Sucker (Xyrauchen texanus): analysis of Hatchery Stocks and implications for captive propagation. Conserv Biol 10:120–127

    Article  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among population of the argan tree (Argania spinosa (L.) Skeels) endemic to Morocco. Theor Appl Genet 92:832–839

    Article  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Small populations: I. Changes of gene frequency under simplified conditions. In: Falconer (ed) Introduction to quantitative genetics. Longman Group Ltd, Essex, England, pp 48–64

    Google Scholar 

  • Ferguson A, Fleming IA, Hindar K, Skaala Ø, McGinnity P, Cross TF, Prodöhl (2007) Farm escapes. In: Verspoor E, Stradmeyer L, Nielsen JL (eds) The Atlantic salmon; genetics, conservation and management, Blackwell, pp 364–365

  • Fiske P, Lund RA, Østborg GM, Fløystad L (2001) Rømt oppdrettslaks i sjø-og elvefisket i årene 1989–2000 (In Norwegian). NINA Oppdragsmelding 704:1–26

    Google Scholar 

  • Fleming IA, Jonsson B, Gross MR, Lamberg A (1996) An experimental study of the reproductive behaviour and success of farmed and wild Atlantic salmon (Salmo salar). J Appl Ecol 33:893–905

    Article  Google Scholar 

  • Fleming IA, Hindar K, Mjølnerød IB, Jonsson B, Balstad T, Lamberg A (2000) Lifetime success and interactions of farm salmon invading a native population. Proc R Soc Lond B 267:1517–1523

    Article  CAS  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Molec Ecol 10:305–318

    Article  CAS  Google Scholar 

  • Gjedrem T, Gjøen HM, Gjerde B (1991) Genetic origin of Norwegian farmed Atlantic salmon. Aquaculture 98:41–50

    Article  Google Scholar 

  • Gjøen HM, Bentsen HB (1997) Past, present, and future of genetic improvement in salmon aquaculture. ICES J Mar Sci 54:1009–1014

    Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.chlizea/softwares/fstat.html

  • Hansen MM, Loeschcke V (1996) Temporal variation in mitochondrial DNA haplotype frequencies in a brown trout (Salmo trutta L.) population that shows stability in nuclear allele frequencies. Evolution 50:454–457

    Article  Google Scholar 

  • Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genet Res 38:209–216

    Article  Google Scholar 

  • Hindar K, Ryman N, Utter F (1991) Genetic effects of cultured fish on natural fish populations. Can J Fish Aquat Sci 48:954–957

    Article  Google Scholar 

  • Hindar K, Fleming IA, McGinnity P, Diserud O (2006) Genetic and ecological effects of salmon farming on wild salmon: modelling from experimental results. ICES J Mar Sci 63:1234–1247

    Article  CAS  Google Scholar 

  • Johnsen BO, Jensen AJ (1994) The spread of furunculosis in salmonids in Norwegian rivers. J Fish Biol 45:47–55

    Article  Google Scholar 

  • Jonsson B (ed) (2006) Interaksjoner mellom laksoppdrett og villaks: oppdatering av kunnskapen etter NOU:1999:9 (in Norwegian), Kunnskapsserien for laks og vannmiljø. Namsos, Norway

    Google Scholar 

  • Jorde PE, Ryman N (2007) Unbiased estimator for genetic drift and effective population size. Genetics 177:927–935

    Article  PubMed  Google Scholar 

  • Karlsson S, Moen T, Hindar K (2009) An extended panel of single nucleotide polymorphisms in Atlantic salmon (Salmo salar L.) mitochondrial DNA. Conserv Genet. doi:10.1007/s10592-009-9910-4

  • King TL, Eackles MS, Letcher BH (2005) Microsatellite DNA markers for the study of Atlantic salmon (Salmo salar) kinship, population structure, and mixed-fishery analyses. Molec Ecol Notes 5:130–132

    Article  CAS  Google Scholar 

  • McGinnity P, Stone C, Taggart JB, Cooke D, Cotter D, Hynes R, McCamley C, Cross T, Ferguson A (1997) Genetic impact of escaped farmed Atlantic salmon (Salmo salar L.) on native populations: use of DNA profiling to assess freshwater performance of wild, farmed, and hybrid progeny in natural river environment. ICES J Mar Sci 54:998–1008

    Google Scholar 

  • McGinnity P, Prodöhl P, Ferguson A, Hynes R, Ó Maoiléidigh N, Rogan G, Taggart J, Cross T (2003) Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interaction with escaped farm salmon. Proc R Soc Lond B 270:2443–2520

    Article  Google Scholar 

  • Mjølnerød IB, Refseth UH, Karlsen E, Balstad T, Jakobsen KS, Hindar K (1997) Genetic differences between two wild and one farmed population of Atlantic salmon (Salmo salar) revealed by three classes of genetic markers. Hereditas 127:239–248

    Article  Google Scholar 

  • Mork J, Bentsen HB, Hindar K, Skaala Ø (1999) Genetiske interaksjoner mellom oppdrettslaksog vill laks. In: Rieber-Mohn GF (ed) Til Laks åt alle kan ingen gjera. NOU, Norges Offentlige Utredninger (In Norwegian), pp 232–259

  • Ng SHS, Chang A, Brown GD, Koop BF, Davidson WS (2005) Type I microsatellite markers from Atlantic salmon (Salmo salar) expressed sequence tags. Molec Ecol Notes 5:762–766

    Article  CAS  Google Scholar 

  • Norris AT, Bradley DG, Cunnigham EP (1999) Microsatellite genetic variation between and within farmed and wild Atlantic salmon (Salmo salar) populations. Aquaculture 180:247–264

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Paterson S, Piertney SB, Knox D, Gilbey J, Verspoor E (2004) Characterization and PCR multiplexing of novel highly variable tetranucleotide Atlantic salmon (Salmo salar L.) microsatellites. Molec Ecol Notes 4:160–162

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) Genepop (version 2.1): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rexroad CE III, Coleman RL, Hershberger WK, Killefer J (2002) Rapid communication: thirty-eight polymorphic microsatellite markers for mapping in rainbow trout. J Anim Sci 80:541–542

    CAS  PubMed  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DNASP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Sægrov H, Hindar K, Kålås S, Lura H (1997) Escaped farmed Atlantic salmon replaced the original salmon stock in the River Vosso, western Norway. ICES J Mar Sci 54:1166–1172

    Google Scholar 

  • Siemon HSNG, Chang A, Brown GD, Koop BF, Davidson WS (2005) Type I microsatellite markers from Atlantic salmon (Salmo salar) expressed sequence tags. Mole Ecol Notes 5:762–766

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin Ver. 2.0: a software for population genetic data analysis. Genetics and Biometry Laboratory,University of Geneva, Geneva

    Google Scholar 

  • Skaala Ø, Høyheim B, Glover K, Dahle G (2004) Microsatellite analysis in domesticated and wild Atlantic salmon (Salmo salar L.) allelic diversity and identification of individuals. Aquaculture 240:131–143

    Article  CAS  Google Scholar 

  • Skaala Ø, Taggart JB, Gunnes K (2005) Genetic differences between five major domesticated strains of Atlantic salmon and wild salmon. J Fish Biol 67:118–128

    Article  CAS  Google Scholar 

  • Skaala Ø, Wennevik V, Glover KA (2006) Evidence of temporal genetic change in wild Atlantic salmon, Salmo salar L., populations affected by farm escapees. ICES J Mar Sci 63:1224–1233

    Article  CAS  Google Scholar 

  • Tang K, Fu DJ, Julien D, Braun A, Cantor CR, Köster H (1999) Chip-based genotyping by mass spectrometry. Proc Nat Acad Sci USA 96:10016–10020

    Article  CAS  PubMed  Google Scholar 

  • Tufto J, Hindar K (2003) Effective size in management and conservation of subdivided populations. J Theor Biol 222:273–281

    Article  PubMed  Google Scholar 

  • Wang J (2001) A pseudo-likelihood method for estimating effective population size from temporally spaced samples. Genet Res 78:243–257

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Molec Ecol Res 8:753–756

    Article  Google Scholar 

  • Waples RS, Yokota M (2007) Temporal estimates of effective population size in species with overlapping generations. Genetics 175:219–233

    Article  PubMed  Google Scholar 

  • Webb JH, Hay DW, Cunningham PD, Youngson AF (1991) The spawning behavior of escaped farmed and wild adult Atlantic salmon (Salmo salar L.) in a northern Scottish river. Aquaculture 98:97–110

    Article  Google Scholar 

  • Williamson KS, Cordes JF, May B (2002) Characterization of microsatellite loci in Chinook salmon (Oncorhynchus tshawytscha) and cross-species amplification in other salmonids. Mole Ecol Notes 2:17–19

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge SalmoBreed and Aqua Gen for providing samples from farm strains, Gunnel Østborg (NINA), Paul Berg, Arne Roseth (Cigene), and Hege Munck (Nofima) for technical assistance. We also want to thank two anonymous referees for their help in improving this paper. This paper is a contribution from the project “Genomics as a tool for detecting selection in farm Atlantic salmon and interactions between escaped and farm wild salmon” funded by the Research Council of Norway (NFR FUGE grant no. 175130).

Author information

Authors and Affiliations

  1. NOFIMA, Arboretveien 2, 1430, Ås, Norway

    Sten Karlsson

  2. Aqua Gen AS, Postboks 1240, Pirsenteret, 7462, Trondheim

    Thomas Moen

  3. CIGENE, Arboretveien 6, 1432, Ås, Norway

    Thomas Moen

  4. Norwegian Institute for Nature Research (NINA), 7485, Trondheim, Norway

    Kjetil Hindar

Authors
  1. Sten Karlsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas Moen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kjetil Hindar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sten Karlsson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karlsson, S., Moen, T. & Hindar, K. Contrasting patterns of gene diversity between microsatellites and mitochondrial SNPs in farm and wild Atlantic salmon. Conserv Genet 11, 571–582 (2010). https://doi.org/10.1007/s10592-009-0034-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-009-0034-7

Keywords

Search

Navigation