Marine Biology

, Volume 162, Issue 5, pp 979–992 | Cite as

Long-term persistence and evolutionary divergence of a marine fish population with a very small effective population size (Kildin cod Gadus morhua kildinensis)

  • Victor Andreev
  • Mikhail Fokin
  • Nikolai Mugue
  • Petr Strelkov
Original Paper

Abstract

The effective population size (Ne) is a crucial characteristic of numerically small populations, positively correlated with their ability to persist in a changing environment and to evolve. Information about the lower bounds of Ne of natural populations is both theoretically interesting and practically important. We studied Kildin cod, an isolated population of Atlantic cod Gadus morhua from an ecologically marginal habitat (marine lake), comparing it with the parental Barents Sea population by a set of 20 microsatellite and protein loci. Overall, the genetic variability in Kildin cod was low (mean allelic richness and heterozygosity: Kildin cod 1.6, 0.26; marine cod 11.6, 0.73). We detected a single locus, the glucose-6-phosphate isomerase-1, which demonstrated a unique variation in the lake. At this locus, about 75 % of the lacustrine fishes carried an allele not found in the sea. The obtained genetic estimates of Ne of Kildin cod (less than a hundred) were much smaller than what is considered as the smallest Ne of a viable population. At the same time, Kildin cod is known to be healthy and productive. Based on the results of bottleneck tests, we hypothesize that Kildin cod has experienced founder-flush dynamics that lead to loss of genetic variation during the founder phase(s) and purging of genetic load and the rise of adaptation during flush phase(s).

Keywords

Brook Trout Approximate Bayesian Computation Allozyme Locus Marine Sample Marine Population 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We extend our sincere gratitude to the following persons and organizations: E. Movchan and other members of the Saint-Petersburg State University (SPbSU) Barents Sea expeditions for their assistance in the field; N. Lentsman for English language editing of the manuscript; T. Moum, P.R. England, D. Roy and anonymous reviewers for helpful comments; Centre for molecular and cell technologies of SPbSU for technical help. This work was funded by SPbSU (Grant no. 1.38.253.2014) and Russian Foundation for Basic Research (Grant nos. 07-04-01734-a and 10-04-90836).

Supplementary material

227_2015_2642_MOESM1_ESM.pdf (514 kb)
Supplementary material 1 (PDF 514 kb)

References

  1. Amadon D (1949) The seventy-five per cent rule for subspecies. Condor 51:250–258CrossRefGoogle Scholar
  2. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinform 9:323. doi: 10.1186/1471-2105-9-323 CrossRefGoogle Scholar
  3. Beaumont M, Nichols R (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc B 263:1619–1626. doi: 10.1098/rspb.1996.0237 CrossRefGoogle Scholar
  4. Berthier P, Beaumont MA, Cornuet J-M, Luikart G (2002) Likelihood-based estimation of the effective population size using temporal changes in allele frequencies: a genealogical approach. Genetics 160:741–751Google Scholar
  5. Bijlsma R, Loeschcke V (2012) Genetic erosion impedes adaptive responses to stressful environments. Evol Appl 5:117–129. doi: 10.1111/j.1752-4571.2011.00214.x CrossRefGoogle Scholar
  6. Carr MH, Neigel JE, Estes JA, Andelman S, Warner RR, Largier JL (2003) Comparing marine and terrestrial ecosystems: implications for the design of coastal marine reserves. Ecol Appl 13:90–107CrossRefGoogle Scholar
  7. Carson HL, Templeton AR (1984) Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annu Rev Ecol Evol Syst 15:97–131. doi: 10.1146/annurev.es.15.110184.000525 CrossRefGoogle Scholar
  8. Charlier J, Laikre L, Ryman N (2012) Genetic monitoring reveals temporal stability over 30 years in a small, lake resident brown trout population. Heredity 109:246–253. doi: 10.1038/hdy.2012.36 CrossRefGoogle Scholar
  9. Comps B, Gömöry D, Letouzey J, Thiébaut B, Petit RJ (2001) Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European beech. Genetics 157:389–397Google Scholar
  10. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014Google Scholar
  11. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, SunderlandGoogle Scholar
  12. Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper & Row, New YorkGoogle Scholar
  13. Dawson MN, Hamner WM (2005) Rapid evolutionary radiation of marine zooplankton in peripheral environments. Proc Natl Acad Sci USA 102:9235–9240. doi: 10.1073/pnas.0503635102 CrossRefGoogle Scholar
  14. Dawson MN, Hamner WM (2008) A biophysical perspective on dispersal and the geography of evolution in marine and terrestrial systems. J R Soc Interface 5:135–150. doi: 10.1098/rsif.2007.1089 CrossRefGoogle Scholar
  15. Derjugin KM (1925) Relict Lake Mogilnoe (Island Kildin in the Barents Sea). Glavnauka, Leningrad (in Russian)Google Scholar
  16. Earl D, von Holdt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:1–3. doi: 10.1007/s12686-011-9548-7 CrossRefGoogle Scholar
  17. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x CrossRefGoogle Scholar
  18. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587. doi: 10.1111/j.1471-8286.2007.01758.x Google Scholar
  19. Fox CW, Reed DH (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258. doi: 10.1111/j.1558-5646.2010.01108.x CrossRefGoogle Scholar
  20. Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327. doi: 10.1038/hdy.1997.46 CrossRefGoogle Scholar
  21. Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, red list criteria and population viability analyses. Biol Conserv 170:56–63. doi: 10.1016/j.biocon.2013.12.036 CrossRefGoogle Scholar
  22. Fraser DJ, Debes PV, Bernatchez L, Hutchings JA (2014) Population size, habitat fragmentation, and the nature of adaptive variation in a stream fish. Proc R Soc B. 281:20140370. doi: 10.1098/rspb.2014.0370 CrossRefGoogle Scholar
  23. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318CrossRefGoogle Scholar
  24. Gosset CC, Bierne N (2013) Differential introgression from a sister species explains high F(ST) outlier loci within a mussel species. J Evol Biol 26:14–26. doi: 10.1111/jeb.12046 CrossRefGoogle Scholar
  25. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www2.unil.ch/popgen/softwares/fstat.htm
  26. Gurevich VI (1975) Relief, bathimetry, morphometry. In: Gurevich VI, Zeeb RYA (eds) Relict Lake Mogilnoe. Nauka, Leningrad, pp 18–21 (in Russian)Google Scholar
  27. Gurevich VI, Liiva AA (1975) Age of the lake Mogilnoe. In: Gurevich VI, Zeeb RYA (eds) Relict Lake Mogilnoe. Nauka, Leningrad, pp 102–104 (in Russian)Google Scholar
  28. Hardie DC, Gillett RM, Hutchings JA (2006) The effects of isolation and colonization on the genetic structure of marine relict populations of Atlantic cod (Gadus morhua) in the Canadian Arctic. Can J Fish Aqua Sci 63:1830–1839. doi: 10.1139/F06-085 CrossRefGoogle Scholar
  29. Hardie DC, Renaud CB, Ponomarenko VP, Mukhina NV, Yaragina NA, Skjaeraasen JE, Hutchings JA (2008) The isolation of Atlantic cod Gadus morhua (Gadiformes), populations in northern meromictic lakes—a recurrent Arctic phenomenon. J Ichthyol 48:230–240. doi: 10.1134/S0032945208030053 CrossRefGoogle Scholar
  30. Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362. doi: 10.1111/j.1467-2979.2008.00299.x CrossRefGoogle Scholar
  31. Hedgecock D (1994) Does variance in reproductive success limit effective population sizes of marine organisms? In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman & Hall, London, pp 122–134Google Scholar
  32. Hedgecock D, Pudovkin A (2011) Sweepstakes reproductive success in highly fecund marine fish and shellfish: a review and commentary. Bull Mar Sci 87:971–1002. doi: 10.5343/bms.2010.1051 CrossRefGoogle Scholar
  33. Hutchings JA, Reynolds JD (2004) Marine fish population collapses: consequences for recovery and extinction. Bioscience 54:297–309. doi: 10.1641/0006-3568(2004)054 CrossRefGoogle Scholar
  34. Hutchinson WF, van Oosterhout C, Rogers SI, Carvalho GR (2003) Temporal analysis of archived samples indicates marked genetic changes in declining North Sea cod (Gadus morhua). Proc R Soc B 270:2125–2132. doi: 10.1098/rspb.2003.2493 CrossRefGoogle Scholar
  35. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. doi: 10.1111/j.1471-8286.2007.01769.x CrossRefGoogle Scholar
  36. Jansson E, Ruokonen M, Kojola I, Aspi J (2012) Rise and fall of a wolf population: genetic diversity and structure during recovery, rapid expansion and drastic decline. Mol Ecol 21:5178–5193. doi: 10.1111/mec.12010 CrossRefGoogle Scholar
  37. Johnson JA, Tingay RE, Culver M, Hailer F, Clarke ML, Mindell DP (2009) Long-term survival despite low genetic diversity in the critically endangered Madagascar fish-eagle. Mol Ecol 18:54–63. doi: 10.1111/j.1365-294X.2008.04012.x Google Scholar
  38. Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555. doi: 10.1111/j.1755-0998.2009.02787.x CrossRefGoogle Scholar
  39. Jørstad KE, Nævdal G (1989) Genetic variation and population structure of cod, Gadus morhua L, in some fjords in northern Norway. J Fish Biol 35:245–252. doi: 10.1111/j.1095-8649.1989.tb03067.x CrossRefGoogle Scholar
  40. Jørstad KE, Nævdal G, Paulsen OI, Torkildsen S (1994) Release and recapture of genetically tagged cod fry in a Norwegian fjord system. In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman & Hall, London, pp 519–528Google Scholar
  41. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241. doi: 10.1016/s0169-5347(02)02489-8 CrossRefGoogle Scholar
  42. Koskinen MT, Haugen TO, Primmer CR (2002) Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:826–830. doi: 10.1038/nature01029 CrossRefGoogle Scholar
  43. Kuo C-H, Janzen FJ (2003) BOTTLESIM: a bottleneck simulation program for long-lived species with overlapping generations. Mol Ecol Notes 3:669–673. doi: 10.1046/j.1471-8286.2003.00532.x CrossRefGoogle Scholar
  44. Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460. doi: 10.1126/science.3420403 CrossRefGoogle Scholar
  45. Linschoten Van JH (1601) Voyagie ofte Schip-vaert, van Ian Hvyghen van Linschoten, van by Noorden om langes Noorvvegen de Noortcaep, Laplant, Vinlant, Russlandt, de VVitte Zee, de Custen van Candenoes, Svvetenoes, Pitzora, &c. door de Strate ofte Engte van Nassau tot voorby de Revier Oby. Gerard Ketel, Ghedruct tot Franeker (in Dutch)Google Scholar
  46. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247. doi: 10.1093/jhered/89.3.238 CrossRefGoogle Scholar
  47. Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW (2010) Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv Genet 11:355–373. doi: 10.1007/s10592-010-0050-7 CrossRefGoogle Scholar
  48. Mayr E (1954) Change of genetic environment and evolution. In: Huxley J, Hardy AC, Ford EB (eds) Evolution as a process. Allen & Unwin, London, pp 157–180Google Scholar
  49. Miller KM, Le KD, Beacham TD (2000) Development of tri- and tetranucleotide repeat microsatellite loci in Atlantic cod (Gadus morhua). Mol Ecol 9:238–239. doi: 10.1046/j.1365-294x.2000.00804-2.x CrossRefGoogle Scholar
  50. Mityaev MV, Korsun SA, Strelkov PP, Matishov GG (2008) Ancient coastlines of Eastern Kildin. Dokl Earth Sci 423:1455–1458. doi: 10.1134/S1028334X08090298 CrossRefGoogle Scholar
  51. Mork J, Reuterwall C, Ryman N, Stahl G (1982) Genetic variation in Atlantic cod (Gadus morhua L.): a quantitative estimate from a Norwegian coastal population. Hereditas 96:55–61CrossRefGoogle Scholar
  52. Mukhina NV, Lepesevich NA, Filina EA (2002) Biological state of Kilidinskaya Cod. In: Titov OV (ed) Relict Lake Mogilnoe (studies of 1997–2000). PINRO, Murmank, pp 88–109 (in Russian)Google Scholar
  53. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10. doi: 10.2307/2407137 CrossRefGoogle Scholar
  54. Norris RD, Hull PM (2012) The temporal dimension of marine speciation. Evol Ecol 26:393–415. doi: 10.1007/s10682-011-9488-4 CrossRefGoogle Scholar
  55. Novikov G, Afanas’ev K, Rubtsova G, Stroganov A (2006) Some genetic parameters of Kildin cod Gadus morhua kildinensis (Gadidae, Gadiformes). J Ichthyol 46:674–676CrossRefGoogle Scholar
  56. O’Reilly PT, McPherson AA, Kenchington E, Taggart C, Jones MW, Bentzen P (2002) Isolation and characterization of tetranucleotide microsatellites from Atlantic haddock (Melanogrammus aeglefinus). Mar Biotechnol 4:418–422. doi: 10.1007/s10126-002-0010-4 CrossRefGoogle Scholar
  57. O’Reilly PT, Canino MF, Bailey KM, Bentzen P (2000) Isolation of twenty low stutter di- and tetranucleotide microsatellites for population analyses of walleye pollock and other gadoids. J Fish Biol 56:1074–1086. doi: 10.1111/j.1095-8649.2000.tb02124.x CrossRefGoogle Scholar
  58. Ottersen G, Hjermann D, Stenseth NC (2006) Changes in spawning stock structure strengthens the link between climate and recruitment in a heavily fished cod stock. Fish Oceanogr 15:230–243. doi: 10.1111/j.1365-2419.2006.00404.x CrossRefGoogle Scholar
  59. Ozeretskovsky N (1804) Opisanie Koli i Astrakhani [Description of Kola and Astrakhan]. Emperor Academy of Sciences, St. Petersburg (in Russian)Google Scholar
  60. Palo JU, Hyvärinen H, Helle E, Mäkinen HS, Väinölä R (2003) Postglacial loss of microsatellite variation in the landlocked Lake Saimaa ringed seal. Conserv Genet 4:117–128. doi: 10.1023/A:1023303109701 CrossRefGoogle Scholar
  61. Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447. doi: 10.1111/j.1365-294X.2008.03842.x CrossRefGoogle Scholar
  62. Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Bëer E, Robinson S, Vasquez-Carrillo C, Pauli JN, Palsbøll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418. doi: 10.1111/j.1365-294X.2012.05635.x CrossRefGoogle Scholar
  63. Pinsky ML, Palumbi SR (2014) Meta-analysis reveals lower genetic diversity in overfished populations. Mol Ecol 23:29–39. doi: 10.1111/mec.12509 CrossRefGoogle Scholar
  64. Poulsen NA, Nielsen EE, Schierup MH, Loeschcke V, Grønkjaer P (2006) Long-term stability and effective population size in North Sea and Baltic Sea cod (Gadus morhua). Mol Ecol 15:321–331. doi: 10.1111/j.1365-294X.2005.02777.x CrossRefGoogle Scholar
  65. Raymond M, Rousset F (1995) Genepop, version 1.2: population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  66. Reed DH (2010) Albatrosses, eagles and newts, Oh My!: exceptions to the prevailing paradigm concerning genetic diversity and population viability? Anim Conserv 13:448–457. doi: 10.1111/j.1469-1795.2010.00353.x CrossRefGoogle Scholar
  67. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225. doi: 10.2307/2409177 CrossRefGoogle Scholar
  68. Robichaud D, Rose GA (2004) Migratory behaviour and range in Atlantic cod: inference from a century of tagging. Fish Fish 5:185–214. doi: 10.1111/j.1467-2679.2004.00141.x CrossRefGoogle Scholar
  69. Robinson JD, Moyer GR (2013) Linkage disequilibrium and effective population size when generations overlap. Evol Appl 6:290–302. doi: 10.1111/j.1752-4571.2012.00289.x CrossRefGoogle Scholar
  70. Ryman N, Allendorf FW, Jorde PE, Laikre L, Hössjer O (2014) Samples from subdivided populations yield biased estimates of effective size that overestimate the rate of loss of genetic variation. Mol Ecol Resour 14:87–99. doi: 10.1111/1755-0998.12154 CrossRefGoogle Scholar
  71. Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annu Rev Mar Sci 3:509–535. doi: 10.1146/annurev-marine-120709-142756 CrossRefGoogle Scholar
  72. Serebrov LI, Ignashkin VA (2002) An estimate of the population size of Kildin cod. In: Relict Lake Mogilnoe (studies of 1997–2000). PINRO, Murmank, pp 110–116 (in Russian)Google Scholar
  73. Shaffer ML (1981) Minimum population sizes for species conservation. Bioscience 31:131–134. doi: 10.2307/1308256 CrossRefGoogle Scholar
  74. Skirnisdottir S, Pampoulie C, Hauksdottir S, Schulte I, Olafsson K, Hreggvidsson GO, Hjörleifsdóttir S (2008) Characterization of 18 new microsatellite loci in Atlantic cod (Gadus morhua L.). Mol Ecol Resour 18:1503–1505. doi: 10.1111/j.1755-0998.2008.02327.x CrossRefGoogle Scholar
  75. Skrbinšek T, Jelenčič M, Waits L, Kos I, Jerina K, Trontelj P (2012) Monitoring the effective population size of a brown bear (Ursus arctos) population using new single-sample approaches. Mol Ecol 21:862–875. doi: 10.1111/j.1365-294X.2011.05423.x CrossRefGoogle Scholar
  76. Strelkov P, Shunatova N, Fokin M, Usov N, Fedyuk M, Malavenda S, Lubina O, Poloskin A, Korsun S (2014) Marine Lake Mogilnoe (Kildin Island, Barents Sea): one hundred years of solitude. Polar Biol 37:297–310. doi: 10.1007/s00300-013-1431-4 CrossRefGoogle Scholar
  77. Stroganov AN, Afanasiev KI, Rubtsova GA, Rakitskaya TA, Semenova AV (2011) Data on variation of microsatellite loci in Kildin cod Gadus morhua kildinensis (Gadidae). J Ichthyol 51:500–507. doi: 10.1134/S0032945211040187 CrossRefGoogle Scholar
  78. Svetovidov AN (1962) Fauna of the U.S.S.R. (Fauna SSSR). Fishes (Ryby). Gadiformes (Treskoobraznye). Israel Program for Scientific Translations, JerusalemGoogle Scholar
  79. Swatdipong A, Primmer CR, Vasemägi A (2010) Historical and recent genetic bottlenecks in European grayling, Thymallus thymallus. Conserv Genet 11:279–292. doi: 10.1007/s10592-009-0031-x CrossRefGoogle Scholar
  80. Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496. doi: 10.1016/j.tree.2004.07.003 CrossRefGoogle Scholar
  81. Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Resour 8:299–301. doi: 10.1111/j.1471-8286.2007.01997.x CrossRefGoogle Scholar
  82. 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. doi: 10.1139/F10-084 CrossRefGoogle Scholar
  83. Titov OV (2002) Conclusions. In: Titov OV (ed) Relict Lake Mogilnoe (studies of 1997–2000). PINRO, Murmank, pp 141–156 (in Russian)Google Scholar
  84. Traill LW, Brook BW, Frankham RR, Bradshaw CJA (2010) Pragmatic population viability targets in a rapidly changing world. Biol Conserv 143:28–34. doi: 10.1016/j.biocon.2009.09.001 CrossRefGoogle Scholar
  85. Tseeb RYA, Astafeva AV (1975) Morphology of Kildin cod. In: Gurevich VI, Zeeb RYA (eds) Relict Lake Mogilnoe. Nauka, Leningrad, pp 259–276 (in Russian)Google Scholar
  86. Tseeb RY, Pozdnyakov YF (1975) Reproduction. In: Gurevich VI, Zeeb RYA (eds) Relict Lake Mogilnoe. Nauka, Leningrad, pp 227–247 (in Russian)Google Scholar
  87. Vasemagi A, Primmer CR (2005) Challenges for identifying functionally important genetic variation: the promise of combining complementary research strategies. Mol Ecol 14:3623–3642. doi: 10.1111/j.1365-294X.2005.02690.x CrossRefGoogle Scholar
  88. Vitalis R (2012) DetSel: an R-package to detect marker loci responding to selection. Methods Mol Biol 888:277–293. doi: 10.1007/978-1-61779-870-2_16 CrossRefGoogle Scholar
  89. Vitalis R, Dawson K, Boursot P (2001) Interpretation of variation across marker loci as evidence of selection. Genetics 158:1811–1823. doi: 10.1093/jhered/esg083 Google Scholar
  90. Wang J (2009) A new method for estimating effective population sizes from a single sample of multilocus genotypes. Mol Ecol 18:2148–2164. doi: 10.1111/j.1365-294X.2009.04175.x CrossRefGoogle Scholar
  91. Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756. doi: 10.1111/j.1755-0998.2007.02061.x CrossRefGoogle Scholar
  92. Ward RD, Woodwark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44:213–232. doi: 10.1111/j.1095-8649.1994.tb01200.x CrossRefGoogle Scholar
  93. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. doi: 10.2307/2408641 CrossRefGoogle Scholar
  94. Wesmajervi M-S, Tafese T, Stenvik J, Fjalestad K-T, Damsgard B, Delghandi M (2007) Eight new microsatellite markers in Atlantic cod (Gadus morhua L.) derived from an enriched genomic library. Mol Ecol Notes 7:138–140. doi: 10.1111/j.1471-8286.2006.01555.x CrossRefGoogle Scholar
  95. Whiteley AR, Hastings K, Wenburg JK, Frissell CA, Martin JC, Allendorf FW (2010) Genetic variation and effective population size in isolated populations of coastal cutthroat trout. Conserv Genet 11:1929–1943. doi: 10.1007/s10592-010-0083-y CrossRefGoogle Scholar
  96. Willi Y, Van Buskirk J, Hoffmann AA (2006) Limits to the adaptive potential of small populations. Annu Rev Ecol Evol Syst 37:433–458. doi: 10.1146/annurev.ecolsys.37.091305 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Victor Andreev
    • 1
    • 2
  • Mikhail Fokin
    • 3
  • Nikolai Mugue
    • 4
    • 5
  • Petr Strelkov
    • 1
  1. 1.St. Petersburg State UniversitySt. PetersburgRussia
  2. 2.Research Institute of Lake and River FisheriesSt. PetersburgRussia
  3. 3.Zoological InstituteRussian Academy of ScienceSt. PetersburgRussia
  4. 4.Russian Federal Research Institute of Fisheries and OceanographyMoscowRussia
  5. 5.N.K. Koltzov Institute of Developmental BiologyRussian Academy of ScienceMoscowRussia

Personalised recommendations