Abstract
Recent technological developments have facilitated an increased focus on identifying genomic regions underlying adaptive trait variation in natural populations, and it has been advocated that this information should be important for designating population units for conservation. In marine fishes, phenotypic studies have suggested adaptation through divergence of life-history traits among natural populations, but the distribution of adaptive genetic variation in these species is still relatively poorly known. In this study, we extract information about the geographical distribution of genetic variation for 33 single nucleotide polymorphisms (SNPs) associated with life-history trait candidate genes, and compare this to variation in 70 putatively neutral SNPs in Atlantic cod (Gadus morhua). We analyse samples covering the major population complexes in the eastern Atlantic and find strong evidence for non-neutral levels and patterns of population structuring for several of the candidate gene-associated markers, including two SNPs in the growth hormone 1 gene. Thus, this study aligns with findings from phenotypic studies, providing molecular data strongly suggesting that these or closely linked genes are under selection in natural populations of Atlantic cod. Furthermore, we find that patterns of variation in outlier markers do not align with those observed at selectively neutral markers, and that outlier markers identify conservation units on finer geographical scales than those revealed when analysing only neutral markers. Accordingly, results also suggest that information about adaptive genetic variation will be useful for targeted conservation and management in this and other marine species.
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Aguirre-Hernandez J, Sargan DR (2005) Evaluation of candidate genes in the absence of positional information: a poor bet on a blind dog! J Hered 96:475–484
Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709
Andersen O, Wetten OF, De Rosa MC, Andre C, Carelli Alinovi C, Colafranceschi M, Brix O, Colosimo A (2009) Haemoglobin polymorphisms affect the oxygen-binding properties in Atlantic cod populations. Proc R Soc B Biol Sci 276:833–841
Anderson TJ, Nair S, Sudimack D, Williams JT, Mayxay M, Newton PN, Guthmann JP, Smithuis FM, Tran TH, van den Broek IV, White NJ, Nosten F (2005) Geographical distribution of selected and putatively neutral SNPs in Southeast Asian malaria parasites. Mol Biol Evol 22:2362–2374
Beaumont MA, Balding DJ (2004) Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13:969–980
Beaumont M, Nichols R (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc B Biol Sci 263:1619–1626
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300
Bierne N, Welch J, Loire E, Bonhomme F, David P (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol Ecol 20:2044–2072
Bradbury IR, Hubert S, Higgins B, Borza T, Bowman S, Paterson IG, Snelgrove PV, Morris CJ, Gregory RS, Hardie DC, Hutchings JA, Ruzzante DE, Taggart CT, Bentzen P (2010) Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature. Proc R Soc B Biol Sci 277:3725–3734
Bradbury IR, Hubert S, Higgins B, Bowman S, Borza T, Paterson IG, Snelgrove PVR, Morris CJ, Gregory RS, Hardie D, Hutchings JA, Ruzzante DE, Taggart CT, Bentzen P (2013) Genomic islands of divergence and their consequences for the resolution of spatial structure in an exploited marine fish. Evol Appl 6:446–450
Case R, Hutchinson W, Hauser L, Van Oosterhout C, Carvalho G (2005) Macro- and micro-geographic variation in pantophysin (PanI) allele frequencies in NE Atlantic cod Gadus morhua. Mar Ecol Prog Ser 301:267–278
Clark AG, Hubisz MJ, Bustamante CD, Williamson SH, Nielsen R (2005) Ascertainment bias in studies of human genome-wide polymorphism. Genome Res 15:1496–1502
Conover DO, Clarke LM, Munch SB, Wagner GN (2006) Spatial and temporal scales of adaptive divergence in marine fishes and the implications for conservation. J Fish Biol 69:21–47
Coop G, Witonsky D, Di Rienzo A, Pritchard JK (2010) Using environmental correlations to identify loci underlying local adaptation. Genetics 185:1411–1423
Cosart T, Beja-Pereira A, Chen S, Ng SB, Shendure J, Luikart G (2011) Exome-wide DNA capture and next generation sequencing in domestic and wild species. BMC Genomics 12:347
Deane EE, Woo NYS (2009) Modulation of fish growth hormone levels by salinity, temperature, pollutants and aquaculture related stress: a review. Rev Fish Biol Fish 19:97–120
De-Santis C, Jerry DR (2007) Candidate growth genes in finfish—where should we be looking? Aquaculture 272:22–38
DeWoody J, Avise J (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol 56:461–473
Edenberg HJ, Liu Y (2009) Laboratory methods for high-throughput genotyping. Cold Spring Harb Protoc 11:pdb.top62
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchically structured population. Heredity 103:285–298
Feder JL, Egan SP, Nosil P (2012) The genomics of speciation-with-gene-flow. Trends Genet 28:342–350
Fevolden SE, Pogson GH (1997) Genetic divergence at the synaptophysin (Syp I) locus among Norwegian coastal and north-east Arctic populations of Atlantic cod. J Fish Biol 51:895–908
Fischer MC, Foll M, Excoffier L, Heckel G (2011) Enhanced AFLP genome scans detect local adaptation in high-altitude populations of a small rodent (Microtus arvalis). Mol Ecol 20:1450–1462
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
Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496
Gienapp P, Teplitsky C, Alho JS, Mills JA, Merila J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Grant W, Bowen B (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426
Hancock AM, Witonsky DB, Gordon AS, Eshel G, Pritchard JK, Coop G, Di Rienzo A (2008) Adaptations to climate in candidate genes for common metabolic disorders. PLoS Genet 4:e32
Harrald M, Neat FC, Wright PJ, Fryer RJ, Huntingford FA (2010a) Population variation in thermal growth responses of juvenile Atlantic cod (Gadus morhua L.). Environ Biol Fishes 87:187–194
Harrald M, Wright PJ, Neat FC (2010b) Substock variation in reproductive traits in North Sea cod (Gadus morhua). Can J Fish Aquat Sci 67:866–876
Hemmer-Hansen J, Nielsen EE, Frydenberg J, Loeschcke V (2007) Adaptive divergence in a high gene flow environment: Hsc70 variation in the European flounder (Platichthys flesus L.). Heredity 99:592–600
Hemmer-Hansen J, Nielsen EE, Meldrup D, Mittelholzer C (2011) Identification of single nucleotide polymorphisms in candidate genes for growth and reproduction in a nonmodel organism; the Atlantic cod, Gadus morhua. Mol Ecol Resour 11:71–80
Hemmer-Hansen J, Nielsen EE, Therkildsen NO, Taylor MI, Ogden R, Geffen AJ, Bekkevold D, Helyar S, Pampoulie C, Johansen T, Carvalho GR, FishPopTrace Consortium (2013) A genomic island linked to ecotype divergence in Atlantic cod. Mol Ecol 22:2653–2667
Hendry A, Day T, Taylor E (2001) Population mixing and the adaptive divergence of quantitative traits in discrete populations: a theoretical framework for empirical tests. Evolution 55:459–466
Hilborn R, Quinn T, Schindler D, Rogers D (2003) Biocomplexity and fisheries sustainability. Proc Natl Acad Sci USA 100:6564–6568
Hutchings JA, Fraser DJ (2008) The nature of fisheries- and farming-induced evolution. Mol Ecol 17:294–313
Hutchings JA, Swain DP, Rowe S, Eddington JD, Puvanendran V, Brown JA (2007) Genetic variation in life-history reaction norms in a marine fish. Proc R Soc B Biol Sci 274:1693–1699
Jeffreys H (1961) Theory of probability. Oxford University Press, New York
Johannesson K, Andre C (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol 15:2013–2029
Johnston IA, Andersen O (2008) Number of muscle fibres in adult Atlantic cod varies with temperature during embryonic development and pantophysin (PanI) genotype. Aquat Biol 4:167–173
Johnston IA, Abercromby M, Andersen O (2006) Muscle fibre number varies with haemoglobin phenotype in Atlantic cod as predicted by the optimal fibre number hypothesis. Biol Lett 2:590–592
Karlsson S, Mork J (2003) Selection-induced variation at the pantophysin locus (PanI) in a Norwegian fjord population of cod (Gadus morhua L.). Mol Ecol 12:3265–3274
Karpov AK, Novikov GG (1980) The haemoglobin aloforms in cod (Gadus morhua L.), their functional characteristics and distribution in the populations. J Ichthyol 6:45–50
Kinsella RJ, Kahari A, Haider S, Zamora J, Proctor G, Spudich G, Almeida-King J, Staines D, Derwent P, Kerhornou A, Kersey P, Flicek P (2011) Ensembl BioMarts: a hub for data retrieval across taxonomic space. Database: bar030
Kohn MH, Murphy WJ, Ostrander EA, Wayne RK (2006) Genomics and conservation genetics. Trends Ecol Evol 21:629–637
Kuparinen A, Merila J (2007) Detecting and managing fisheries-induced evolution. Trends Ecol Evol 22:652–659
Kuparinen A, Merila J (2008) The role of fisheries-induced evolution. Science 320:47–50
Lamichhaney S, Barrio AM, Rafati N, Sundstrom G, Rubin C, Gilbert ER, Berglund J, Wetterbom A, Laikre L, Webster MT, Grabherr M, Ryman N, Andersson L (2012) Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring. Proc Natl Acad Sci USA 109:19345–19350
Larmuseau MH, Raeymaekers JA, Ruddick KG, Van Houdt JK, Volckaert FA (2009) To see in different seas: spatial variation in the rhodopsin gene of the sand goby (Pomatoschistus minutus). Mol Ecol 18:4227–4239
Larsen PF, Nielsen EE, Williams TD, Hemmer-Hansen J, Chipman JK, Kruhoffer M, Gronkjaer P, George SG, Dyrskjot L, Loeschcke V (2007) Adaptive differences in gene expression in European flounder (Platichthys flesus). Mol Ecol 16:4674–4683
Limborg MT, Helyar SJ, de Bruyn M, Taylor MI, Nielsen EE, Ogden R, Carvalho GR, Bekkevold D, FPT Consortium (2012) Environmental selection on transcriptome-derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus). Mol Ecol 21:3686–3703
Lingoes JC (1971) Some boundary conditions for a monotone analysis of symmetric matrices. Psychometrika 36:195–203
Luikart G, England P, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994
McCracken KG, Bulgarella M, Johnson KP, Kuhner MK, Trucco J, Valqui TH, Wilson RE, Peters JL (2009) Gene flow in the face of countervailing selection: adaptation to high-altitude hypoxia in the betaA hemoglobin subunit of yellow-billed pintails in the Andes. Mol Biol Evol 26:815–827
Merila J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903
Moen T, Hayes B, Nilsen F, Delghandi M, Fjalestad KT, Fevolden SE, Berg PR, Lien S (2008) Identification and characterisation of novel SNP markers in Atlantic cod: evidence for directional selection. BMC Genet 9:18
Morin PA, Martien KK, Taylor BL (2009) Assessing statistical power of SNPs for population structure and conservation studies. Mol Ecol Resour 9:66–73
Nagylaki T (1975) Conditions for the existence of clines. Genetics 80:595–615
Namroud MC, 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. Mol Ecol 17:3599–3613
Nielsen EE, Hansen MM, Schmidt C, Meldrup D, Gronkjaer P (2001) Fisheries. Population of origin of Atlantic cod. Nature 413:272
Nielsen E, Hansen M, Ruzzante D, Meldrup D, Gronkjaer P (2003) Evidence of a hybrid-zone in Atlantic cod (Gadus morhua) in the Baltic and the Danish Belt Sea revealed by individual admixture analysis. Mol Ecol 12:1497–1508
Nielsen EE, Hemmer-Hansen J, Larsen PF, Bekkevold D (2009a) Population genomics of marine fishes: identifying adaptive variation in space and time. Mol Ecol 18:3128–3150
Nielsen EE, Hemmer-Hansen J, Poulsen NA, Loeschcke V, Moen T, Johansen T, Mittelholzer C, Taranger G, Ogden R, Carvalho GR (2009b) Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua). BMC Evol Biol 9:276
Nordborg M, Tavare S (2002) Linkage disequilibrium: what history has to tell us. Trends Genet 18:83–90
Nordeide JT, Johansen SD, Jorgensen TE, Karlsen BO, Moum T (2011) Population connectivity among migratory and stationary cod Gadus morhua in the Northeast Atlantic—a review of 80 years of study. Mar Ecol Prog Ser 435:269–283
Olsen EM, Knutsen H, Gjosaeter J, Jorde PE, Knutsen JA, Stenseth NC (2008) Small-scale biocomplexity in coastal Atlantic cod supporting a Darwinian perspective on fisheries management. Evol Appl 1:524–533
Ouborg NJ, Pertoldi C, Loeschcke V, Bijlsma RK, Hedrick PW (2010) Conservation genetics in transition to conservation genomics. Trends Genet 26:177–187
Pespeni MH, Garfield DA, Manier MK, Palumbi SR (2012) Genome-wide polymorphisms show unexpected targets of natural selection. Proc R Soc B Biol Sci 279:1412–1420
Pogson GH (2001) Nucleotide polymorphism and natural selection at the pantophysin (Pan I) locus in the Atlantic cod, Gadus morhua (L.). Genetics 157:317–330
Poulsen N, Nielsen E, Schierup M, Loeschcke V, Gronkjaer P (2006) Long-term stability and effective population size in North Sea and Baltic Sea cod (Gadus morhua). Mol Ecol 15:321–331
Poulsen NA, Hemmer-Hansen J, Loeschcke V, Carvalho GR, Nielsen EE (2011) Microgeographical population structure and adaptation in Atlantic cod Gadus morhua: spatio-temporal insights from gene-associated DNA markers. Mar Ecol Prog Ser 436:231–243
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103
Reiss H, Hoarau G, Dickey-Collas M, Wolff WJ (2009) Genetic population structure of marine fish: mismatch between biological and fisheries management units. Fish Fish 10:361–395
Richter-Boix A, Teplitsky C, Rogell B, Laurila A (2010) Local selection modifies phenotypic divergence among Rana temporaria populations in the presence of gene flow. Mol Ecol 19:716–731
Righton DA, Andersen KH, Neat F, Thorsteinsson V, Steingrund P, Svedang H, Michalsen K, Hinrichsen H, Bendall V, Neuenfeldt S, Wright P, Jonsson P, Huse G, van der Kooij J, Mosegaard H, Hussy K, Metcalfe J (2010) Thermal niche of Atlantic cod Gadus morhua: limits, tolerance and optima. Mar Ecol Prog Ser 420:1–13
Ryynanen HJ, Primmer CR (2004) Distribution of genetic variation in the growth hormone 1 gene in Atlantic salmon (Salmo salar) populations from Europe and North America. Mol Ecol 13:3857–3869
Sarup P, Frydenberg J, Loeschcke V (2009) Local adaptation of stress related traits in Drosophila buzzatii and Drosophila simulans in spite of high gene flow. J Evol Biol 22:1111–1122
Sarvas T, Fevolden S (2005) Pantophysin (Pan I) locus divergence between inshore v. offshore and northern v. southern populations of Atlantic cod in the north-east Atlantic. J Fish Biol 67:444–469
Schindler DE, Hilborn R, Chasco B, Boatright CP, Quinn TP, Rogers LA, Webster MS (2010) Population diversity and the portfolio effect in an exploited species. Nature 465:609–612
Shikano T, Ramadevi J, Merila J (2010a) Identification of local- and habitat-dependent selection: scanning functionally important genes in nine-spined sticklebacks (Pungitius pungitius). Mol Biol Evol 27:2775–2789
Shikano T, Ramadevi J, Shimada Y, Merila J (2010b) Utility of sequenced genomes for microsatellite marker development in non-model organisms: a case study of functionally important genes in nine-spined sticklebacks (Pungitius pungitius). BMC Genomics 11:334
Shimada Y, Shikano T, Merila J (2011) A high incidence of selection on physiologically important genes in the three-spined stickleback, Gasterosteus aculeatus. Mol Biol Evol 28:181–193
Sick K (1961) Haemoglobin polymorphism in fishes. Nature 192:894–896
Slatkin M (2008) Linkage disequilibrium—understanding the evolutionary past and mapping the medical future. Nat Rev Genet 9:477–485
Star B, Nederbragt AJ, Jentoft S, Grimholt U, Malmstrom M, Gregers TF, Rounge TB, Paulsen J, Solbakken MH, Sharma A, Wetten OF, Lanzen A, Winer R, Knight J, Vogel JH, Aken B, Andersen O, Lagesen K, Tooming-Klunderud A, Edvardsen RB, Tina KG, Espelund M, Nepal C, Previti C, Karlsen BO, Moum T, Skage M, Berg PR, Gjoen T, Kuhl H, Thorsen J, Malde K, Reinhardt R, Du L, Johansen SD, Searle S, Lien S, Nilsen F, Jonassen I, Omholt SW, Stenseth NC, Jakobsen KS (2011) The genome sequence of Atlantic cod reveals a unique immune system. Nature 477:207–210
Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688
Therkildsen NO, Nielsen EE, Swain DP, Pedersen JS (2010) Large effective population size and temporal genetic stability in Atlantic cod (Gadus morhua) in the southern Gulf of St. Lawrence. Can J Fish Aquat Sci 67:1585–1595
Therkildsen NO, Hemmer-Hansen J, Als TD, Swain DP, Morgan MJ, Trippel EA, Palumbi SR, Meldrup D, Nielsen EE (2013a) Microevolution in time and space: SNP analysis of historical DNA reveals dynamic signatures of selection in Atlantic cod. Mol Ecol 22:2424–2440
Therkildsen NO, Hemmer-Hansen J, Hedeholm RB, Wisz MS, Pampoulie C, Meldrup D, Bonanomi S, Retzel A, Olsen SM, Nielsen EE (2013b) Spatiotemporal SNP analysis reveals pronounced biocomplexity at the northern range margin of Atlantic cod Gadus morhua. Evol Appl 6:690–705
Tonteri A, Vasemagi A, Lumme J, Primmer CR (2010) Beyond MHC: signals of elevated selection pressure on Atlantic salmon (Salmo salar) immune-relevant loci. Mol Ecol 19:1273–1282
van Tienderen P, de Haan A, van der Linden C, Vosman B (2002) Biodiversity assessment using markers for ecologically important traits. Trends Ecol Evol 17:577–582
Via S (2012) Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow. Philos Trans R Soc Lond B Biol Sci 367:451–460
Waples R (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38:1358–1370
Acknowledgments
We are grateful to Christophe Pampoulie, Torild Johansen and Gary R. Carvalho for the provision of samples, and to Dorte Bekkevold, Thomas Damm Als and members of the EU projects “FinE” and “FishPopTrace” for discussions improving the manuscript. This work was carried out under the EU projects ‘FinE’ (Grant Number: 044276) and FishPopTrace (Grant Agreement Number: KBBE212399), the Greenland Climate Research Centre financed by the Danish Agency for Science, Technology and Innovation, and also received support through the project “Improved management through stock identification of eastern and western Baltic Sea cod” financed by the The Danish Ministry of Food, Agriculture and Fisheries and the European Fisheries Fund.
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Hemmer-Hansen, J., Therkildsen, N.O., Meldrup, D. et al. Conserving marine biodiversity: insights from life-history trait candidate genes in Atlantic cod (Gadus morhua). Conserv Genet 15, 213–228 (2014). https://doi.org/10.1007/s10592-013-0532-5
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DOI: https://doi.org/10.1007/s10592-013-0532-5