Genome-wide SNP analysis reveals a genetic basis for sea-age variation in a wild population of Atlantic salmon (Salmo salar)
Susan E. Johnston
Division of Genetics and Physiology, Department of Biology, University of Turku, Itäinen Pitkäkatu 4, Turku, FIN-20520 Finland
Search for more papers by this authorPanu Orell
Finnish Game and Fisheries Research Institute, Utsjoki, FIN-99980 Finland
Search for more papers by this authorVictoria L. Pritchard
Division of Genetics and Physiology, Department of Biology, University of Turku, Itäinen Pitkäkatu 4, Turku, FIN-20520 Finland
Search for more papers by this authorMatthew P. Kent
Centre for Integrative Genetics (CIGENE) and Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Aas, N-1432 Norway
Search for more papers by this authorSigbjørn Lien
Centre for Integrative Genetics (CIGENE) and Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Aas, N-1432 Norway
Search for more papers by this authorEero Niemelä
Finnish Game and Fisheries Research Institute, Utsjoki, FIN-99980 Finland
Search for more papers by this authorJaakko Erkinaro
Finnish Game and Fisheries Research Institute, Utsjoki, FIN-99980 Finland
Search for more papers by this authorCorresponding Author
Craig R. Primmer
Division of Genetics and Physiology, Department of Biology, University of Turku, Itäinen Pitkäkatu 4, Turku, FIN-20520 Finland
Correspondence: Craig R. Primmer, Fax: +358 2 333 6680; E-mail: [email protected]Search for more papers by this authorSusan E. Johnston
Division of Genetics and Physiology, Department of Biology, University of Turku, Itäinen Pitkäkatu 4, Turku, FIN-20520 Finland
Search for more papers by this authorPanu Orell
Finnish Game and Fisheries Research Institute, Utsjoki, FIN-99980 Finland
Search for more papers by this authorVictoria L. Pritchard
Division of Genetics and Physiology, Department of Biology, University of Turku, Itäinen Pitkäkatu 4, Turku, FIN-20520 Finland
Search for more papers by this authorMatthew P. Kent
Centre for Integrative Genetics (CIGENE) and Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Aas, N-1432 Norway
Search for more papers by this authorSigbjørn Lien
Centre for Integrative Genetics (CIGENE) and Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Aas, N-1432 Norway
Search for more papers by this authorEero Niemelä
Finnish Game and Fisheries Research Institute, Utsjoki, FIN-99980 Finland
Search for more papers by this authorJaakko Erkinaro
Finnish Game and Fisheries Research Institute, Utsjoki, FIN-99980 Finland
Search for more papers by this authorCorresponding Author
Craig R. Primmer
Division of Genetics and Physiology, Department of Biology, University of Turku, Itäinen Pitkäkatu 4, Turku, FIN-20520 Finland
Correspondence: Craig R. Primmer, Fax: +358 2 333 6680; E-mail: [email protected]Search for more papers by this authorAbstract
Delaying sexual maturation can lead to larger body size and higher reproductive success, but carries an increased risk of death before reproducing. Classical life history theory predicts that trade-offs between reproductive success and survival should lead to the evolution of an optimal strategy in a given population. However, variation in mating strategies generally persists, and in general, there remains a poor understanding of genetic and physiological mechanisms underlying this variation. One extreme case of this is in the Atlantic salmon (Salmo salar), which can show variation in the age at which they return from their marine migration to spawn (i.e. their ‘sea age’). This results in large size differences between strategies, with direct implications for individual fitness. Here, we used an Illumina Infinium SNP array to identify regions of the genome associated with variation in sea age in a large population of Atlantic salmon in Northern Europe, implementing individual-based genome-wide association studies (GWAS) and population-based FST outlier analyses. We identified several regions of the genome which vary in association with phenotype and/or selection between sea ages, with nearby genes having functions related to muscle development, metabolism, immune response and mate choice. In addition, we found that individuals of different sea ages belong to different, yet sympatric populations in this system, indicating that reproductive isolation may be driven by divergence between stable strategies. Overall, this study demonstrates how genome-wide methodologies can be integrated with samples collected from wild, structured populations to understand their ecology and evolution in a natural context.
Supporting Information
Filename | Description |
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mec12832-sup-0001-TableS1-S6.xlsxMS Excel, 1.8 MB | Table S1 Proportions of the four clusters identified to have different levels of relatedness. Table S2 FST between MDS clusters based on unlinked SNP markers (N = 521). Table S3 Genotyping summary and genome-wide association study (GWAS) and FST outlier results for all SNPs included in the current study. Table S4 Nucleotide BLAST (blastn) results of all Salmo nucleotide sequences (N = 60 140) accessed from NCBI in June 2013. Sequences were aligned to reference contigs containing significant SNPs. Table S5 Protein to nucleotide BLAST (tblastn) results of all Salmo and Oncorhynchus protein sequences (N = 22 766 and 21 401, respectively) accessed from NCBI in June 2013. Table S6 Gene ontology (GO) information for genes spanning or flanking SNPs significantly associated with sea age variation. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.
- Amaral IPG, Johnston IA (2011) Insulin-like growth factor (IGF) signalling and genome-wide transcriptional regulation in fast muscle of zebrafish following a single-satiating meal. Journal of Experimental Biology, 214, 2125–2139.
- Aubin-Horth N, Renn SCP (2009) Genomic reaction norms: using integrative biology to understand molecular mechanisms of phenotypic plasticity. Molecular Ecology, 18, 3763–3780.
- Aulchenko YS, Ripke S, Isaacs A, van Duijn CM (2007) GenABEL: an R library for genome-wide association analysis. Bioinformatics, 23, 1294–1296.
- Balding DJ (2006) A tutorial on statistical methods for population association studies. Nature Reviews Genetics, 7, 781–791.
- Beaumont M, Nichols R (1996) Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society of London, Series B: Biological Sciences, 263, 1619–1626.
- Bierne N, Welch J, Loire E, Bonhomme F, David P (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Molecular Ecology, 20, 2044–2072.
- Bierne N, Roze D, Welch JJ (2013) Pervasive selection or is it…? Why are FST outliers sometimes so frequent? Molecular Ecology, 22, 2061–2064.
- Bourret V, Kent MP, Primmer CR et al. (2013) SNP-array reveals genome-wide patterns of geographical and potential adaptive divergence across the natural range of Atlantic salmon (Salmo salar). Molecular Ecology, 22, 532–551.
- Braceland M, Bickerdike R, Tinsley J et al. (2013) The serum proteome of Atlantic salmon, Salmo salar, during pancreas disease (PD) following infection with salmonid alphavirus subtype 3 (SAV3). Journal of Proteomics, 94, 423–436.
- Bruneaux M, Johnston SE, Herczeg G et al. (2013) Molecular evolutionary and population genomic analysis of the nine-spined stickleback using a modified restriction-site-associated DNA tag approach. Molecular Ecology, 22, 565–582.
- Chadwick EMP, Randall RG, Luger C (1986) Ovarian development of Atlantic salmon (Salmo salar) smolts and age at first maturity. Canadian Special Publication of Fisheries and Aquatic Sciences, 89, 15–23.
- Chaput G (2012) Overview of the status of Atlantic salmon (Salmo salar) in the North Atlantic and trends in marine mortality. ICES Journal of Marine Science, 69, 1538–1548.
- Charlesworth B (1994) Evolution in Age-structured Populations. Cambridge University Press, Cambridge.
10.1017/CBO9780511525711 Google Scholar
- Conover D, Munch S (2002) Sustaining fisheries yields over evolutionary time scales. Science, 297, 94–96.
- Di Rienzo A, Peterson AC, Garza JC et al. (1994) Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences of the USA, 91, 3166–3170.
- Dionne M, Miller KM, Dodson JJ, Caron F, Bernatchez L (2007) Clinal variation in MHC diversity with temperature: evidence for the role of host-pathogen interaction on local adaptation in Atlantic salmon. Evolution, 61, 2154–2164.
- Do C, Waples RS, Peel D et al. (2013) NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Molecular Ecology Resources, 14, 209–214.
- Edward DA, Chapman T (2011) Mechanisms underlying reproductive trade-offs: costs of reproduction. In: Mechanisms of Life History Evolution: The Genetics and Physiology of Life History Traits and Trade-offs(eds T Flatt & A Heyland), pp. 137–152. Oxford University Press, New York.
10.1093/acprof:oso/9780199568765.003.0011 Google Scholar
- Eisbrenner WD, Botwright N, Cook M et al. (2013) Evidence for multiple sex-determining loci in Tasmanian Atlantic salmon (Salmo salar). Heredity, 113, 86–92.
- Ellner S, Hairston NG Jr (1994) Role of overlapping generations in maintaining genetic variation in a fluctuating environment. American Naturalist, 143, 403–417.
- Evans ML, Dionne M, Miller KM, Bernatchez L (2012) Mate choice for major histocompatibility complex genetic divergence as a bet-hedging strategy in the Atlantic salmon (Salmo salar). Proceedings of the Royal Society of London, Series B: Biological Sciences, 279, 379–386.
- Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567.
- Falconer DS, Mackay TFC (1996) Threshold characters. In: Introduction to Quantitative Genetics(eds DS Falconer & TFC Mackay), pp. 299–311. Longman, Essex, UK.
- Fleming IA (1998) Pattern and variability in the breeding system of Atlantic salmon (Salmo salar), with comparisons to other salmonids. Canadian Journal of Fisheries and Aquatic Sciences, 55(Suppl.), 59–76.
- Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics, 180, 977–993.
- Fourcade Y, Chaput-Bardy A, Secondi J, Fleurant C, Lemaire C (2013) Is local selection so widespread in river organisms? Fractal geometry of river networks leads to high bias in outlier detection. Molecular Ecology, 22, 2065–2073.
- Fraley C, Raftery AE (2002) Model-Based Clustering, Discriminant Analysis, and Density Estimation. Journal of American Statistical Association, 97, 611–631.
- Friedland K (2000) Linkage between ocean climate, post-smolt growth, and survival of Atlantic salmon (Salmo salar L.) in the North Sea area. ICES Journal of Marine Science, 57, 419–429.
- Friedland KD, Haas RE (1996) Marine post-smolt growth and age at maturity of Atlantic salmon. Journal of Fish Biology, 48, 1–15.
- Friedland KD, MacLean JC, Hansen LP et al. (2009) The recruitment of Atlantic salmon in Europe. ICES Journal of Marine Science, 66, 289–304.
- Garant D, Dodson JJ, Bernatchez L (2003) Differential reproductive success and heritability of alternative reproductive tactics in wild Atlantic salmon (Salmo salar L.). Evolution, 57, 1133–1141.
- Gilad Y, Pritchard JK, Thornton K (2009) Characterizing natural variation using next-generation sequencing technologies. Trends in Genetics, 25, 463–471.
- Gjerde B (1984) Response to individual selection for age at sexual maturity in Atlantic salmon. Aquaculture, 38, 229–240.
- Gjerde B, Gjedrem T (1984) Estimates of phenotypic and genetic parameters for carcass traits in Atlantic salmon and rainbow trout. Aquaculture, 36, 97–110.
- Gjerde B, Simianer H, Refstie T (1994) Estimates of genetic and phenotypic parameters for body weight, growth rate and sexual maturity in Atlantic salmon. Livestock Production Science, 38, 133–143.
- Glover KA, Grimholt U, Bakke HG et al. (2007) Major histocompatibility complex (MHC) variation and susceptibility to the sea louse Lepeophtheirus salmonis in Atlantic salmon Salmo salar. Diseases of Aquatic Organisms, 76, 57–65.
- Gosset CC, Bierne N (2013) Differential introgression from a sister species explains high FST outlier loci within a mussel species. Journal of Evolutionary Biology, 26, 14–26.
- Grimholt U, Larsen S, Nordmo R et al. (2003) MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci. Immunogenetics, 55, 210–219.
- Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends in Ecology & Evolution, 11, 92–98.
- Gurney WSC, Bacon PJ, Speirs DC, McGinnity P, Verspoor E (2012) Sea-age variation in maiden Atlantic salmon spawners: phenotypic plasticity or genetic polymorphism? Bulletin of Mathematical Biology, 74, 615–640.
- Gutierrez AP, Lubieniecki KP, Fukui S et al. (2014) Detection of quantitative trait loci (QTL) related to grilsing and late sexual maturation in Atlantic salmon (Salmo salar). Marine Biotechnology, 16, 103–110.
- Hale MC, Thrower FP, Berntson Ea, Miller MR, Nichols KM (2013) Evaluating adaptive divergence between migratory and nonmigratory ecotypes of a salmonid fish, Oncorhynchus mykiss. G3 (Bethesda), 3, 1273–1285.
- Hansen LP, Quinn TP (1998) The marine phase of the Atlantic salmon (Salmo salar) life cycle, with comparisons to Pacific salmon. Canadian Journal of Fisheries and Aquatic Sciences, 55, 104–118.
- Heinimaa S, Heinimaa P (2004) Effect of the female size on egg quality and fecundity of the wild Atlantic salmon in the sub-arctic River Teno. Boreal Environment Research, 5, 5–62.
- Helyar SJ, Hemmer-Hansen J, Bekkevold D et al. (2010) Application of SNPs for population genetics of nonmodel organisms: new opportunities and challenges. Molecular Ecology Resources, 11(Suppl.), 123–136.
- Hohenlohe PA, Bassham S, Etter PD, et al. (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genetics, 6, e1000862.
- Huizinga TWJ, Pisetsky DS, Kimberly RP (2004) Associations, populations, and the truth: recommendations for genetic association studies in Arthritis & Rheumatism. Arthritis and Rheumatism, 50, 2066–2071.
- Hutchings JA, Jones MEB (1998) Life history variation and growth rate thresholds for maturity in Atlantic salmon, Salmo salar. Canadian Journal of Fisheries and Aquatic Sciences, 55(Suppl.), 22–47.
- ICES (2011) Report of the Workshop on Age Determination of Salmon (WKADS). ICES Document CM 2011/ACOM:44 66 pp.
- ICES (2013) Report of the Working Group on North Atlantic Salmon (WGNAS). ICES Document CM 2013/ACOM:09 380 pp.
- Jennings S, Kaiser MJ (1998) The effects of fishing on marine ecosystems. Advances in Marine Biology, 34, 201–352.
- Johnston SE, McEwan JC, Pickering NK et al. (2011) Genome-wide association mapping identifies the genetic basis of discrete and quantitative variation in sexual weaponry in a wild sheep population. Molecular Ecology, 20, 2555–2566.
- Johnston SE, Lindqvist M, Niemelä E et al. (2013) Fish scales and SNP chips: SNP genotyping and allele frequency estimation in individual and pooled DNA from historical samples of Atlantic salmon (Salmo salar). BMC Genomics, 14, 439.
- Jonsson N, Jonsson B (2007) Sea growth, smolt age and age at sexual maturation in Atlantic salmon. Journal of Fish Biology, 71, 245–252.
- Jonsson B, Jonsson N (2011) Migrations. In: Ecology of Atlantic salmon and Brown Trout: Habitat as a Template for Life Histories (eds. B Jonsson, N Jonsson), pp. 247–326. Springer Verlag, Heidelberg, Germany.
- Kalinowski ST, Wagner AP, Taper ML (2006) ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Molecular Ecology Notes, 6, 576–579.
- Kallio-Nyberg I, Jutila E, Jokikokko E, Saloniemi I (2006) Survival of reared Atlantic salmon and sea trout in relation to marine conditions of smolt year in the Baltic Sea. Fisheries Research, 80, 295–304.
- Karppinen P, Erkinaro J (2009) Using motion-sensitive radio tags to record the activity and behavioural patterns of spawning Atlantic salmon. Ecology of Freshwater Fish, 18, 177–182.
- Kuparinen A, Merilä J (2007) Detecting and managing fisheries-induced evolution. Trends in Ecology & Evolution, 22, 652–659.
- Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics, 121, 185–199.
- Landry C, Bernatchez L (2001) Comparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar). Molecular Ecology, 10, 2525–2539.
- Landry C, Garant D, Duchesne P, Bernatchez L (2001) “Good genes as heterozygosity”: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proceedings of the Royal Society of London, Series B: Biological Sciences, 268, 1279–1285.
- Lewis CM (2002) Genetic association studies: design, analysis and interpretation. Briefings in Bioinformatics, 3, 146–153.
- Li D, Lewinger JP, Gauderman WJ, Murcray CE, Conti D (2011) Using extreme phenotype sampling to identify the rare causal variants of quantitative traits in association studies. Genetic Epidemiology, 35, 790–799.
- Lien S, Gidskehaug L, Moen T et al. (2011) A dense SNP-based linkage map for Atlantic salmon (Salmo salar) reveals extended chromosome homeologies and striking differences in sex-specific recombination patterns. BMC Genomics, 12, 615.
- Mank JE, Avise JC (2006) Comparative phylogenetic analysis of male alternative reproductive tactics in ray-finned fishes. Evolution, 60, 1311–1316.
- Manolio TA, Collins FS, Cox NJ et al. (2009) Finding the missing heritability of complex diseases. Nature, 461, 747–753.
- Mather ME (1998) The role of context-specific predation in understanding patterns exhibited by anadromous salmon. Canadian Journal of Fisheries and Aquatic Sciences, 55(Suppl.), 232–246.
- McCarthy MI, Abecasis GR, Cardon LR et al. (2008) Genome-wide association studies for complex traits: consensus, uncertainty and challenges. Nature Reviews Genetics, 9, 356–369.
- Milinski M (2006) The major histocompatibility complex, sexual selection and mate choice. Annual Review of Ecology Evolution and Systematics, 37, 159–186.
- Moskvina V, Schmidt KM (2008) On multiple-testing correction in genome-wide association studies. Genetic Epidemiology, 32, 567–573.
- Namroud M-C, Beaulieu J, Juge N, Laroche J, Bousquet J (2008) Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce. Molecular Ecology, 17, 3599–3613.
- Niemelä E, Mäkinen TS, Moen K et al. (2000) Age, sex ratio and timing of the catch of kelts and ascending Atlantic salmon in the subarctic River Teno. Journal of Fish Biology, 56, 974–985.
- Niemelä E, Erkinaro J, Julkunen M et al. (2006a) Temporal variation in abundance, return rate and life histories of previously spawned Atlantic salmon in a large subarctic river. Journal of Fish Biology, 68, 1222–1240.
- Niemelä E, Orell P, Erkinaro J et al. (2006b) Previously spawned Atlantic salmon ascend a large subarctic river earlier than their maiden counterparts. Journal of Fish Biology, 69, 1151–1163.
- Otero J, Jensen AJ, L'Abée-Lund JH et al. (2011) Quantifying the ocean, freshwater and human effects on year-to-year variability of one-sea-winter Atlantic salmon angled in multiple Norwegian rivers. PLoS ONE, 6, e24005.
- Otero J, Jensen AJ, L'Abée-Lund JH et al. (2012) Contemporary ocean warming and freshwater conditions are related to later sea age at maturity in Atlantic salmon spawning in Norwegian rivers. Ecology and Evolution, 2, 2192–2203.
- Parchman TL, Gompert Z, Mudge J et al. (2012) Genome-wide association genetics of an adaptive trait in lodgepole pine. Molecular Ecology, 21, 2991–3005.
- Pedersen S, Berg PR, Culling M et al. (2013) Quantitative trait loci for precocious parr maturation, early smoltification, and adult maturation in double-backcrossed trans-Atlantic salmon (Salmo salar). Aquaculture, 410–411, 164–171.
- Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity, 90, 502–503.
- Piry S, Alapetite A, Cornuet J-M et al. (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. Journal of Heredity, 95, 536–539.
- Platt A, Vilhjálmsson BJ, Nordborg M (2010) Conditions under which genome-wide association studies will be positively misleading. Genetics, 186, 1045–1052.
- Price AL, Patterson NJ, Plenge RM et al. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics, 38, 904–909.
- Price AL, Zaitlen NA, Reich D, Patterson N (2010) New approaches to population stratification in genome-wide association studies. Nature Reviews Genetics, 11, 459–463.
- Purcell S, Neale B, Todd-Brown K et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81, 559–575.
- R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
- Rajakaruna RS, Brown JA, Kaukinen KH, Miller KM (2006) Major histocompatibility complex and kin discrimination in Atlantic salmon and brook trout. Molecular Ecology, 15, 4569–4575.
- Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences of the USA, 94, 9197–9201.
- Rodger H, Murphy T, Drinan E, Rice D (1991) Acute skeletal myopathy in farmed Atlantic salmon Salmo salar. Diseases of Aquatic Organisms, 12, 17–23.
- Roff DA (1992) The Evolution of Life Histories: Theory and Analysis. Chapman & Hall, New York.
10.1046/j.0962-1083.2001.01425.x Google Scholar
- Roff DA (2011) Genomic insights into life history evolution. In: Mechanisms of Life History Evolution: The Genetics and Physiology of Life History Traits and Trade-offs(eds T Flatt & A Heyland), pp. 11–25. Oxford University Press, New York.
10.1093/acprof:oso/9780199568765.003.0002 Google Scholar
- Roff DA, Fairbairn DJ (2007) The evolution of trade-offs: where are we? Journal of Evolutionary Biology, 20, 433–447.
- Salminen M (1997) Relationships between smolt size, postsmolt growth and sea age at maturity in Atlantic salmon ranched in the Baltic Sea. Journal of Applied Ichthyology, 13, 121–130.
- Salminen M, Kuikka S, Erkamo E (1995) Annual variability in survival of sea-ranched Baltic salmon, Salmo salar L: significance of smolt size and marine conditions. Fisheries Management and Ecology, 2, 171–184.
10.1111/j.1365-2400.1995.tb00110.x Google Scholar
- Santure AW, De Cauwer I, Robinson MR et al. (2013) Genomic dissection of variation in clutch size and egg mass in a wild great tit (Parus major) population. Molecular Ecology, 22, 3949–3962.
- Saunders RL, Schom CB (1985) Importance of the variation in life history parameters of Atlantic Salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences, 42, 615–618.
- Schindler DE, Hilborn R, Chasco B et al. (2010) Population diversity and the portfolio effect in an exploited species. Nature, 465, 609–612.
- Skilbrei OT (1989) Relationships between smolt length and growth and maturation in the sea of individually tagged Atlantic salmon (Salmo salar). Aquaculture, 83, 95–108.
- Slate J, Santure AW, Feulner PGD et al. (2010) Genome mapping in intensively studied wild vertebrate populations. Trends in Genetics, 26, 275–284.
- Spencer CCA, Su Z, Donnelly P, Marchini J (2009) Designing genome-wide association studies: sample size, power, imputation, and the choice of genotyping chip. PLoS Genetics, 5, e1000477.
- Stearns SC (1992) The Evolution of Life Histories. Oxford University Press, Oxford.
- Stearns SC (2000) Life history evolution: successes, limitations, and prospects. Die Naturwissenschaften, 87, 476–486.
- Stinchcombe JR, Hoekstra HE (2007) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity, 100, 158–170.
- Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Molecular Ecology, 14, 671–688.
- Taborsky M (1994) Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Advances in the Study of Behavior, 23, 1–100.
- Tonteri A, Vasemägi A, Lumme J, Primmer CR (2010) Beyond MHC: signals of elevated selection pressure on Atlantic salmon (Salmo salar) immune-relevant loci. Molecular Ecology, 19, 1273–1282.
- Vähä J-P, Erkinaro J, Niemelä E, Primmer CR (2007) Life-history and habitat features influence the within-river genetic structure of Atlantic salmon. Molecular Ecology, 16, 2638–2654.
- Vähä J-P, Erkinaro J, Niemelä E et al. (2008) Temporally stable genetic structure and low migration in an Atlantic salmon population complex: implications for conservation and management. Evolutionary Applications, 4, 137–154.
- Vasemägi A, Primmer CR (2005) Challenges for identifying functionally important genetic variation: the promise of combining complementary research strategies. Molecular Ecology, 14, 3623–3642.
- Visscher PM, Brown MA, McCarthy MI, Yang J (2012) Five years of GWAS discovery. American Journal of Human Genetics, 90, 7–24.
- Warnes G, Gorjanc G, Leisch F, Man M (2012) genetics: Population Genetics. R package version 1.3.8. http://CRAN.R-project.org/package=genetics.
- Wild V, Simianer H, Gjøen H-M, Gjerde B (1994) Genetic parameters and genotype X environment interaction for early sexual maturity in Atlantic salmon (Salmo salar). Aquaculture, 128, 51–65.
- Wu C-L, Lin T-H, Chang T-L et al. (2011) Zebrafish HSC70 promoter to express carp muscle-specific creatine kinase for acclimation under cold condition. Transgenic Research, 20, 1217–1226.
- Yano A, Nicol B, Jouanno E et al. (2013) The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male-specific Y-chromosome sequence in many salmonids. Evolutionary Applications, 6, 486–496.
- Yousaf MN, Powell MD (2012) The effects of heart and skeletal muscle inflammation and cardiomyopathy syndrome on creatine kinase and lactate dehydrogenase levels in Atlantic salmon (Salmo salar L.). ScientificWorldJournal, 2012, 741302.