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Polar Biology

, Volume 39, Issue 6, pp 969–980 | Cite as

Population genetic analysis of Euro-Arctic polar cod Boreogadus saida suggests fjord and oceanic structuring

  • Matias L. MadsenEmail author
  • R. John Nelson
  • Svein-Erik Fevolden
  • Jørgen S. Christiansen
  • Kim Præbel
Original Paper

Abstract

Polar cod, Boreogadus saida, is a key species in Arctic marine ecosystems; however, its genetic population structure is largely undescribed. The population genetic structure of 472 B. saida specimens among nine locations in the north-east Atlantic was revealed using 12 microsatellite loci. Pairwise F ST comparisons showed significant population differentiation between B. saida sampled inside fjords in Svalbard and north-east Greenland, as compared to B. saida from the shelf. The observed genetic variation was not a function of isolation by distance, and it is speculated that B. saida populations inhabiting fjords may have become reproductively isolated from shelf-dwelling B. saida during the last post-glacial recolonization.

Keywords

Gadidae Genetic differentiation Marine barriers Spatial population structure Microsatellite markers Polar cod 

Notes

Acknowledgments

This study forms part of the TUNU Programme, UiT The Arctic University of Norway. The analysed material was collected during the TUNU-Expeditions (Christiansen 2012). The authors would like to thank the crew of RV “Jan Mayen” for their help at sea and Tanja L. Hanebrekke for valuable assistance in the laboratory. We appreciate the constructive comments of three anonymous referees on the submitted manuscript.

References

  1. Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693. doi: 10.1093/nar/25.22.4692 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Andersen Ø, Johnsen H, De Rosa MC et al (2015) Evolutionary history and adaptive significance of the polymorphic Pan I in migratory and stationary populations of Atlantic cod (Gadus morhua). Mar Genom 22:45–54. doi: 10.1016/j.margen.2015.03.009 CrossRefGoogle Scholar
  3. Árnason E (2004) Mitochondrial cytochrome b DNA variation in the high-fecundity Atlantic cod. Genet Soc Am 166:1871–1885Google Scholar
  4. Beacham TDEA (2002) Multiple stock structure of Atlantic cod (Gadus morhua) off Newfoundland and Labrador determined from genetic variation. ICES J Mar Sci 59:650–665. doi: 10.1006/jmsc.2002.1253 CrossRefGoogle Scholar
  5. Bentzen P, Taggart CT, Ruzzante DE, Cook D (1996) Microsatellite polymorphism and the population structure of Atlantic cod (Gadus morhua) in the northwest Atlantic. Can J Fish Aquat Sci 53:2706–2721. doi: 10.1139/f96-238 CrossRefGoogle Scholar
  6. Bigg GR, Cunningham CW, Ottersen G et al (2008) Ice-age survival of Atlantic cod: agreement between palaeoecology models and genetics. Proc Biol Sci 275:163–172. doi: 10.1098/rspb.2007.1153 CrossRefPubMedGoogle Scholar
  7. Bouchard C, Fortier L (2011) Circum-arctic comparison of the hatching season of polar cod Boreogadus saida: a test of the freshwater winter refuge hypothesis. Prog Oceanogr 90:105–116CrossRefGoogle Scholar
  8. Bradbury IR, Hubert S, Higgins B et al (2013) Genomic islands of divergence and their consequences for the resolution of spatial structure in an exploited marine fish. Evol Appl 6:450–461. doi: 10.1111/eva.12026 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bradbury IR, Bowman S, Borza T et al (2014) Long distance linkage disequilibrium and limited hybridization suggest cryptic speciation in Atlantic cod. PLoS One 9:e106380. doi: 10.1371/journal.pone.0106380 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631. doi: 10.1093/molbev/msl191 CrossRefPubMedGoogle Scholar
  11. Charrier G, Durand J, Quiniou L, Laroche J (2006) An investigation of the population genetic structure of pollack (Pollachius pollachius) based on microsatellite markers. ICES J Mar Sci 63:1705–1709. doi: 10.1016/j.icesjms.2006.07.006 CrossRefGoogle Scholar
  12. Cheung WWL, Lam VWY, Sarmiento JL et al (2010) Large-scale redistribution of maximum fisheries catch potential in the global ocean under climate change. Glob Change Biol 16:24–35. doi: 10.1111/j.1365-2486.2009.01995.x CrossRefGoogle Scholar
  13. Christiansen JS (2012) The TUNU-Programme: Euro-Arctic Marine fishes—Diversity and adaptation. In: di Prisco G, Verde C (eds) Adapt. Evol. Mar. Environ. Vol 1. Springer, Berlin, Heidelberg, pp 35–50Google Scholar
  14. Christiansen JS, Fevolden S-E (2000) The polar cod of Porsangerfjorden, Norway; revisited. Sarsia 85:189–193. doi: 10.1080/00364827.2000.10414571 CrossRefGoogle Scholar
  15. Christiansen JS, Mecklenburg CW, Karamushko OV (2014) Arctic marine fishes and their fisheries in light of global change. Glob Change Biol 20:352–359. doi: 10.1111/gcb.12395 CrossRefGoogle Scholar
  16. Coulson MW, Marshall HD, Pepin P, Carr SM (2006) Mitochondrial genomics of gadine fishes: implications for taxonomy and biogeographic origins from whole-genome data sets. Genome 49:1115–1130. doi: 10.1139/g06-083 CrossRefPubMedGoogle Scholar
  17. Craig PC, Griffiths WB, Haldorson L et al (1982) Ecological studies of Arctic cod (Boreogadus saida) in Beaufort Sea coastal waters, Alaska. Can J Fish Aquat Sci 39:395–406CrossRefGoogle Scholar
  18. DeWoody J (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol 56:461–473. doi: 10.1006/jfbi.1999.1210 CrossRefGoogle Scholar
  19. Dray S, Dufour A (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20CrossRefGoogle Scholar
  20. Excoffier L, Lischer HEL (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. doi: 10.1111/j.1755-0998.2010.02847.x CrossRefPubMedGoogle Scholar
  21. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  22. Fevolden S, Pogson G (1997) Genetic divergence at the synaptophysin (Syp I) locus among Norwegian coastal and north–east Arctic populations of Atlantic cod. J Fish Biol 51:895–908Google Scholar
  23. Fevolden S, Martinez I, Christiansen J (1999) RAPD and scnDNA analyses of polar cod, Boreogadus saida (Pisces, Gadidae), in the north Atlantic. Sarsia 84:99–103Google Scholar
  24. Fevolden SSE, Westgaard JIJ, Pedersen T, Præbel K (2012) Settling-depth versus genotype and size versus genotype correlations at the Pan I locus in 0-group Atlantic cod Gadus morhua. Mar Ecol Prog Ser 468:267–278. doi: 10.3354/meps09990 CrossRefGoogle Scholar
  25. Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752CrossRefPubMedGoogle Scholar
  26. Glover KA, Skaala Ø, Limborg M et al (2011) Microsatellite DNA reveals population genetic differentiation among sprat (Sprattus sprattus) sampled throughout the Northeast Atlantic, including Norwegian fjords. ICES J Mar Sci 68:2145–2151CrossRefGoogle Scholar
  27. Gradinger RR, Bluhm BA (2004) In-situ observations on the distribution and behavior of amphipods and Arctic cod (Boreogadus saida) under the sea ice of the high Arctic Canada Basin. Polar Biol 27:595–603. doi: 10.1007/s00300-004-0630-4 CrossRefGoogle Scholar
  28. Graham M, Hop H (1995) Aspects of reproduction and larval biology of Arctic cod (Boreogadus saida). Arctic 48:130–135CrossRefGoogle Scholar
  29. Guo SW, Thompson EA, Carlo M (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372CrossRefPubMedGoogle Scholar
  30. Hardie DC, Gillett RM, Hutchings JA (2006) The effects of isolation and colonization history on the genetic structure of marine-relict populations of Atlantic cod (Gadus morhua) in the Canadian Arctic. Can J Fish Aquat Sci 63:1830–1839. doi: 10.1139/f06-085 CrossRefGoogle Scholar
  31. Hemmer-Hansen J, Therkildsen NO (2014) Population genomics of marine fishes: next-generation prospects and challenges. Biol Bull 227:117–132PubMedGoogle Scholar
  32. Hemmer-Hansen J, Nielsen EE, Therkildsen NO et al (2013) A genomic island linked to ecotype divergence in Atlantic cod. Mol Ecol 22:2653–2667. doi: 10.1111/mec.12284 CrossRefPubMedGoogle Scholar
  33. Hemmer-Hansen J, Therkildsen NO, Meldrup D, Nielsen EE (2014) Conserving marine biodiversity: insights from life-history trait candidate genes in Atlantic cod (Gadus morhua). Conserv Genet 15:213–228. doi: 10.1007/s10592-013-0532-5 CrossRefGoogle Scholar
  34. Hop H, Gjøsæter H (2013) Polar cod (Boreogadus saida) and capelin (Mallotus villosus) as key species in marine food webs of the Arctic and the Barents Sea. Mar Biol Res 9:878–894. doi: 10.1080/17451000.2013.775458 CrossRefGoogle Scholar
  35. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hutchinson W, Carvalho G, Rogers S (2001) Marked genetic structuring in localised spawning populations of cod Gadus morhua in the North Sea and adjoining waters, as revealed by microsatellites. Mar Ecol Prog Ser 223:251–260. doi: 10.3354/meps223251 CrossRefGoogle Scholar
  37. Institute of Marine Research (2009) Polar cod. http://www.imr.no/temasider/fisk/torsk/polartorsk/en. Accessed 25 June 2015
  38. Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics (Oxford England) 24(11):1403–1405. doi: 10.1093/bioinformatics/btn129 CrossRefGoogle Scholar
  39. Jombart T (2013) A tutorial for discriminant analysis of principal components (DAPC) using adegenet 1. 3–4. Rvignette, 1–37Google Scholar
  40. Kalinowski ST (2005) Hp-Rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189. doi: 10.1111/j.1471-8286.2004.00845.x CrossRefGoogle Scholar
  41. Karlsen BO, Klingan K, Emblem Å et al (2013) Genomic divergence between the migratory and stationary ecotypes of Atlantic cod. Mol Ecol 22:5098–5111. doi: 10.1111/mec.12454 CrossRefPubMedGoogle Scholar
  42. Karlsen BO, Emblem Å, Jørgensen TE et al (2014) Mitogenome sequence variation in migratory and stationary ecotypes of North-east Atlantic cod. Mar Genom 15:103–108. doi: 10.1016/j.margen.2014.01.001 CrossRefGoogle Scholar
  43. Kattner G, Hirche HJ (1994) The 1993 Northeast water expedition data report of RV “Polarstern” Arctic cruises ARK IX/2 and 3 (Die Nordostwasser-Polynja-expedition 1993 Datenband der Arktis-Reisen ARK IX/2 und 3 mit FS “Polarstern”). Ber Polarforsch 145:271–272Google Scholar
  44. Keenan K, Mcginnity P, Cross TF et al (2013) DiveRsity: an R package for the estimationand exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788. doi: 10.1111/2041-210X.12067 CrossRefGoogle Scholar
  45. Kettle AJ, Morales-Muñiz A, Roselló-Izquierdo E et al (2011) Refugia of marine fish in the northeast Atlantic during the last glacial maximum: concordant assessment from archaeozoology and palaeotemperature reconstructions. Clim Past 7:181–201. doi: 10.5194/cp-7-181-2011 CrossRefGoogle Scholar
  46. Knutsen H, Jorde PE, Sannaes H et al (2009) Bathymetric barriers promoting genetic structure in the deepwater demersal fish tusk (Brosme brosme). Mol Ecol 18:3151–3162. doi: 10.1111/j.1365-294X.2009.04253.x CrossRefPubMedGoogle Scholar
  47. Lønne OJ, Gulliksen B (1989) Size, age and diet of polar cod, Boreogadus saida (Lepechin 1773), in ice covered waters. Polar Biol 9:187–191CrossRefGoogle Scholar
  48. Lønne OJ, Gulliksen B (1991) Source, density and composition of sympagic fauna in the Barents Sea. Polar Res 10:289–294CrossRefGoogle Scholar
  49. Mach ME, Sbrocco EJ, Hice LA et al (2011) Regional differentiation and post-glacial expansion of the Atlantic silverside, Menidia menidia, an annual fish with high dispersal potential. Mar Biol 158:515–530. doi: 10.1007/s00227-010-1577-3 CrossRefPubMedGoogle Scholar
  50. Madsen ML, Fevolden S-E, Christiansen JS (2009) A simple molecular approach to distinguish between two Arctic gadoid fishes Arctogadus glacialis (Peters, 1874) and Boreogadus saida (Lepechin, 1774). Polar Biol 32:937–939. doi: 10.1007/s00300-009-0616-3 CrossRefGoogle Scholar
  51. Melnikov IA, Chernova NV (2013) Characteristics of under-ice swarming of polar cod Boreogadus saida (Gadidae) in the Central Arctic Ocean. J Ichthyol 53:7–15. doi: 10.1134/S0032945213010086 CrossRefGoogle Scholar
  52. Møller PR, Jordan AD, Gravlund P, Steffensen JF (2002) Phylogenetic position of the cryopelagic codfish genus Arctogadus Drjagin, 1932 based on partial mitochondrial cytochrome b sequences. Polar Biol 25:342–349. doi: 10.1007/s00300-001-0348-5
  53. Mork J, Ryman N, Ståhl G et al (1985) Genetic variation in Atlantic cod (Gadus morhua) throughout its range. Can J Fish Aquat Sci 42:1580–1587. doi: 10.1139/f85-198 CrossRefGoogle Scholar
  54. Nahrgang J, Varpe O, Korshunova E et al (2014) Gender specific reproductive strategies of an arctic key species (Boreogadus saida) and implications of climate change. PLoS One 9:e98452. doi: 10.1371/journal.pone.0098452 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Nelson RJ, Bouchard C, Madsen M et al (2012) Microsatellite loci for genetic analysis of the arctic gadids Boreogadus saida and Arctogadus glacialis. Conserv Genet Resour. doi: 10.1007/s12686-012-9824-1 Google Scholar
  56. Owens HL (2015) Evolution of codfishes (Teleostei: Gadinae) in geographical and ecological space: evidence that physiological limits drove diversification of subarctic fishes. J Biogeogr 42:10911102. doi: 10.1111/jbi.12483 CrossRefGoogle Scholar
  57. Pálsson S, Källman T, Paulsen J, Árnason E (2009) An assessment of mitochondrial variation in Arctic gadoids. Polar Biol 32:471–479. doi: 10.1007/s00300-008-0542-9 CrossRefGoogle Scholar
  58. Pampoulie C, Ruzzante DE, Chosson V et al (2006) The genetic structure of Atlantic cod (Gadus morhua) around Iceland: insight from microsatellites, the Pan I locus, and tagging experiments. Can J Fish Aquat Sci 63:2660–2674. doi: 10.1139/f06-150 CrossRefGoogle Scholar
  59. Pampoulie C, Stefánsson MÖ, Jörundsdóttir TD et al (2008) Recolonization history and large-scale dispersal in the open sea: the case study of the North Atlantic cod, Gadus morhua L. Biol J Linn Soc 94:315–329. doi: 10.1111/j.1095-8312.2008.00995.x CrossRefGoogle Scholar
  60. Pampoulie C, Daníelsdottír AK, Storr-Paulsen M, Hovgård H, Hjörleifsson E, Steinarsson BÆ (2011) Neutral and nonneutral genetic markers revealed the presence of inshore and offshore stocks components of Atlantic cod in Greenland waters. Trans Am Fish Soc 40:307–319CrossRefGoogle Scholar
  61. Pampoulie C, Skirnisdottir S, Star B et al (2015) Rhodopsin gene polymorphism associated with divergent light environments in Atlantic cod. Behav Genet 45:236–244. doi: 10.1007/s10519-014-9701-7 CrossRefPubMedGoogle Scholar
  62. Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi: 10.1111/j.1471-8286.2005.01155.x CrossRefGoogle Scholar
  63. Pérez-Losada M, Guerra A, Carvalho GR et al (2002) Extensive population subdivision of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda) around the Iberian Peninsula indicated by microsatellite DNA variation. Heredity (Edinb) 89:417–424. doi: 10.1038/sj.hdy.6800160 CrossRefGoogle Scholar
  64. Pogson GH, Fevolden S-E (2003) Natural selection and the genetic differentiation of coastal and Arctic populations of the Atlantic cod in northern Norway: a test involving nucleotide sequence variation at the pantophysin (PanI) locus. Mol Ecol 12:63–74CrossRefPubMedGoogle Scholar
  65. Pogson GH, Mesa KA, Boutilier RG (1995) Genetic population structure and gene flow in the Atlantic cod Gadus morhua: a comparison of allozyme and nuclear RFLP loci. Genetics 139:375–385Google Scholar
  66. Ponomarenko V (1968) Some data on the distribution and migrations of polar cod in the seas of the Soviet Arctic. Rapp Process des Réuniuns, Cons Perm Int pour l’Explor la Mer 158:131–135Google Scholar
  67. Præbel K, Westgaard J, Fevolden SE, Christiansen JS (2008) Circumpolar genetic population structure of capelin Mallotus villosus. Mar Ecol Prog Ser 360:189–199. doi: 10.3354/meps07363 CrossRefGoogle Scholar
  68. Prisco G (2012) Adaptation and evolution in Marine environments. In: di Prisco G, Verde C (eds.) Vol 1. Springer, Berlin, Heidelberg. http://doi.org/10.1007/978-3-642-27352-0
  69. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  70. Provan J (2013) The effects of past, present and future climate change on range-wide genetic diversity in northern North Atlantic marine species. Front Biogeogr 5:60–66Google Scholar
  71. Renaud PE, Berge J, Varpe Ø et al (2012) Is the poleward expansion by Atlantic cod and haddock threatening native polar cod, Boreogadus saida? Polar Biol 35:401–412. doi: 10.1007/s00300-011-1085-z CrossRefGoogle Scholar
  72. Rice W (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  73. Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. doi: 10.1111/j.1471-8286.2007.01931.x CrossRefPubMedGoogle Scholar
  74. Rudels B, Friedrich HJ, Quadfasel D (1999) The Arctic circumpolar boundary current. Deep Sea Res Part II Top Stud Oceanogr 46:1023–1062. doi: 10.1016/S0967-0645(99)00015-6 CrossRefGoogle Scholar
  75. Rudels B, Fahrbach E, Meincke J et al (2002) The East Greenland current and its contribution to the Denmark strait overflow. ICES J Mar Sci 59:1133–1154. doi: 10.1006/jmsc.2002.1284 CrossRefGoogle Scholar
  76. Rudels B, Bjørk G, Nilsson J et al (2005) The interaction between waters from the Arctic Ocean and the Nordic Seas north of Fram Strait and along the East Greenland Current: results from the Arctic Ocean-02 Oden expedition. J Mar Syst 55:1–30CrossRefGoogle Scholar
  77. Ruzzante DE, Taggart CT, Cook D, Goddard S (1996) Genetic differentiation between inshore and offshore Atlantic cod (Gadus morhua) off Newfoundland: microsatellite DNA variation and antifreeze level. Can J Fish Aquat Sci 53:634–645. doi: 10.1139/f95-228 CrossRefGoogle Scholar
  78. Ruzzante DE, Taggart CT, Cook D (1999) A review of the evidence for genetic structure of cod (Gadus morhua) populations in the NW Atlantic and population affinities of larval cod off Newfoundland and the Gulf of St. Lawrence. Fish Res 43:79–97. doi: 10.1016/S0165-7836(99)00067-3 CrossRefGoogle Scholar
  79. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  80. R Core Team (2015) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.R-project.org/
  81. Sarnthein M, Pflaumann U, Weinelt M (2003) Past extent of sea ice in the northern North Atlantic inferred from foraminiferal paleotemperature estimates. Paleoceanography 18(2):1047. doi: 10.1029/2002PA000771 Google Scholar
  82. 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. doi: 10.1111/j.1095-8649.2005.00738.x Google Scholar
  83. Takezaki N, Nei M, Tamura K (2010) POPTREE2: software for constructing population trees from allele frequency data and computing other population statistics with Windows interface. Mol Biol Evol 27:747–752. doi: 10.1093/molbev/msp312 CrossRefPubMedGoogle Scholar
  84. Therkildsen NO, Hemmer-Hansen J, Als TD et al (2013a) Microevolution in time and space: SNP analysis of historical DNA reveals dynamic signatures of selection in Atlantic cod. Mol Ecol 22:2424–2440. doi: 10.1111/mec.12260 CrossRefPubMedGoogle Scholar
  85. Therkildsen NO, Hemmer-Hansen J, Hedeholm RB et al (2013b) Spatiotemporal SNP analysis reveals pronounced biocomplexity at the northern range margin of Atlantic cod Gadus morhua. Evol Appl 6:690–705. doi: 10.1111/eva.12055
  86. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. doi: 10.1111/j.1471-8286.2004.00684.x CrossRefGoogle Scholar
  87. Von Dorrien CF (1993) Ökologi und respiration ausgewählte arktischer Bodenfischarten (ecology and respiration of selected Arctic benthic fish species). Ber Polarforsch 125:1–99Google Scholar
  88. Von Dorrien CF, Piepenburg D, Schmid MK (1991) On the abundance of Arctic cod Arctogadus glacialis in Northeast water. Polar Rec (Gr Brit) 27:362–364CrossRefGoogle Scholar
  89. Was A, Gosling E, McCrann K, Mork J (2008) Evidence for population structuring of blue whiting (Micromesistius poutassou) in the Northeast Atlantic. ICES J Mar Sci 65:216–225. doi: 10.1093/icesjms/fsm187 CrossRefGoogle Scholar
  90. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Matias L. Madsen
    • 1
    Email author
  • R. John Nelson
    • 2
  • Svein-Erik Fevolden
    • 1
  • Jørgen S. Christiansen
    • 1
  • Kim Præbel
    • 1
  1. 1.Faculty of Biosciences, Fisheries and EconomicsUiT The Arctic University of NorwayTromsøNorway
  2. 2.Department of BiologyUniversity of VictoriaVictoriaCanada

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