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Effects of genetic drift in a small population of Atlantic cod (Gadus morhua kildinensis Derjugin) landlocked in a meromictic lake: genetic variation and conservation measures

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Abstract

Landlocked populations of normally salt-water, bottom-dwelling Atlantic cod exist in a few circumpolar meromictic lakes. One such population, the Kildin cod, inhabits Mogilnoe Lake (Kildin Island, the Barents Sea) that is listed among regional nature reserves. The lake has three main strata of water of about 5 m each: an upper level with nearly fresh water, a saline layer, and an anaerobic zone at the bottom. The fish lives in the saline stratum and appears in the fresh layer as well. Available food is poor, the adults heavily prey on cod juveniles. The Kildin cod has distinct morphological features, faster growth rate, earlier age of maturation, and shorter longevity that likely developed in response to the unusual lake environment. Genetic and capture-mark-recapture data show that the Kildin cod greatly differs from its marine counterparts: It has an effective population size of about one hundred and an average adult census size of about half a thousand, reproductively isolated from a parental marine population around 1800 years ago, lost a large portion of microsatellite and mitochondrial DNA variation due to long-term genetic drift, but still maintains variation at allozyme loci. DNA markers of the Kildin cod do not carry novel mutations, but their multilocus genotypes seem to be unique to the lake population. The suggested conservation strategy includes: (1) the lake and its drainage area should be strongly protected from any detrimental human activities; (2) the transplantation of any genetic material into the cod population of Mogilnoe Lake should be strongly prohibited.

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References

  • Allendorf FW, Bayles D, Bottom DL, Currens KP, Frissell ChA, Hankin D, Lichatowich JA, Nehlsen W, Trotter PC, Williams TH (1997) Prioritizing Pacific salmon stocks for conservation. Conserv Biol 11:140–152

    Article  Google Scholar 

  • Allendorf FW, Luikart G, Aitken SN (2012) Conservation and the genetics of populations. Wiley, Hoboken

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Antsiferov MY, Trofimov AG (2002) Hydrological conditions. In: Titov OV (ed) The relict Mogilnoe Lake (studies in 1997–2000). PINRO, Murmansk, pp 20–33 (in Russian)

    Google Scholar 

  • Arnason E (2004) Mitochondrial cytochrome b DNA variation in the high-fecundity Atlantic cod: trans-Atlantic clines and shallow gene genealogy. Genetics 166:1871–1885

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond Ser B 263:1619–1626

    Article  Google Scholar 

  • Brook BW, Traill LW, Bradshaw CJA (2006) Minimum viable population sizes and global extinction risk are unrelated. Ecol Lett 9:375–382

    Article  PubMed  Google Scholar 

  • Cornuet JM, Ravigné V, Estoup A (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v. 1.0). BMC Bioinform 11:401

    Article  Google Scholar 

  • Derjugin KM (1920) Eine neue Kabeljau-oder Dorschform aus dem See Mogilnoje (Insel Kildin). Extrait de: Travaux de la Sociėté des Naturalistes de Pėtrogradé. Petrograd. vol. LI, livr.1, #1-4, pp 1–3

  • Derjugin KM (1925) The Relict Mogilnoe Lake (Kildin Island in the Barents Sea). Glavnauka Press, Leningrad, 112 p (in Russian)

  • Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2013) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour. doi:10.1111/1755-0998.12157

    Google Scholar 

  • Farrall M (2004) Quantitative genetic variation: a post-modern view. Hum Mol Genet 13(Review Issue 1):R1–R7

    Article  PubMed  CAS  Google Scholar 

  • Ferrer M, Negro JJ (2004) The near extinction of two large European predators: super specialists pay a price. Conserv Biol 18:344–349

    Article  Google Scholar 

  • Foll M, Gaggiotti OE (2008) A genome scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Franklin IR (1980) Evolutionary change in small populations. In: Soulé ME, Wilcox BA (eds) Conservation biology: an evolutionary-ecological perspective. Sinauer Press Assoc., Sunderland, pp 135–149

    Google Scholar 

  • Fraser DJ, Weir LK, Bernatchez L, Hansen MM, Taylor EB (2011) Extent and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity 106:404–420

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gavrilets S, Hastings A (1995) Dynamics of polygenic variability under stabilizing selection, recombination, and drift. Genet Res 65:63–74

    Article  PubMed  CAS  Google Scholar 

  • Gurevich VI, Liyva AA (1975) Age of the Mogilnoe Lake. In: Gurevich VI, RYa T (eds) The relict Mogilnoe Lake. Nauka Publ., Leningrad, pp 102–104 (in Russian)

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Hardie DC, Renaud CB, Ponomarenko VP, Mukhina NV, Yaragina NA, Skjæraasen 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kashi Y, King DG (2006) Simple sequence repeats as advantageous mutators in evolution. Trends Genet 22:253–259

    Article  PubMed  CAS  Google Scholar 

  • Kimmel M, Chakraborty R, King JP et al (1998) Signatures of population expansion in microsatellite repeat data. Genetics 148:1921–1930

    PubMed  CAS  PubMed Central  Google Scholar 

  • Knutsen H, Olsen EM, Jorde PE, Espeland SH, André C, Stenseth NC (2011) Are low but statistically significant levels of genetic differentiation in marine fishes ‘biologically meaningful’? A case study of coastal Atlantic cod. Mol Ecol 20:768–783

    Article  PubMed  CAS  Google Scholar 

  • Krebs CJ (1999) Ecological methodology, 2nd edn. Benjamin/Cummings, Menlo Park

    Google Scholar 

  • Le Corre V, Kremer A (2012) The genetic differentiation at quantitative trait loci under local adaptation. Mol Ecol 21:1548–1566

    Article  PubMed  Google Scholar 

  • Lewis PO, Zaykin D (2001) Genetic data analysis. Computer program for the analysis of allelic data. http//lewis.eeb.uconn.lewishome/software.html

  • Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Assocs., Inc., Sunderland

    Google Scholar 

  • MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton, p 203

    Google Scholar 

  • Mitton JB (2000) Selection in natural populations. Oxford University Press, New York, p 256

    Google Scholar 

  • Mityaev MV, Korsun SA, Strelkov PP, Matishov GG (2008) The ancient coast lines of the Eastern Kildin. Proc Russ Acad Sci Earth Sci 423:546–550 (in Russian)

    Google Scholar 

  • Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254

    Article  PubMed  Google Scholar 

  • Moritz C, Lavery S, Slade R (1995) Using allele frequency and phylogeny to define units for conservation and management. In: Nielsen JL, Powers GA (eds) Evolution and the aquatic ecosystem: defining unique units in population conservation. Symposium 17. American Fisheries Society, Bethesda, pp 249–262

  • Mukhina NV, Lepesevich NA, Filina EA (2002) Biological state of Kildin cod. In: Titov OV (ed) The relict Mogilnoe Lake (studies in 1997–2000). PINRO, Murmansk, pp 88–109 (in Russian)

    Google Scholar 

  • Nevo E, Kirzhner V, Beiles A, Korol A (1997) Selection versus random drift: long-term polymorphism persistence in small populations (evidence and modeling). Philos Trans R Soc 352:381–389

    Article  Google Scholar 

  • Nielsen EE, Kenchington E (2001) A new approach to prioritizing marine fish and shellfish populations for conservation. Fish Fish 2:328–343

    Article  Google Scholar 

  • Nielsen EE, Hansen MM, Meldrup D (2006) Evidence of microsatellite hitch-hiking selection in Atlantic cod (Gadus morhua L.): implications for inferring population structure in nonmodel organisms. Mol Ecol 15:3219–3229

    Article  PubMed  CAS  Google Scholar 

  • Nomura T (2008) Estimation of effective number of breeders from molecular coancestry of single cohort sample. Evol Appl 1:462–474

    Article  PubMed  PubMed Central  Google Scholar 

  • Ohta T, Gillespie JH (1995) Development of neutral and nearly neutral theories. Theor Popul Biol 49:128–142

    Article  Google Scholar 

  • Ólafsdóttir GÁ, Westfall KM, Edvardsson R, Pálsson S (2014) Historical DNA reveals the demographic history of Atlantic cod (Gadus morhua) in medieval and early modern Iceland. Proc R Soc Lond B Biol Sci 281(1777):20132976

    Article  Google Scholar 

  • Palstra FP, Fraser DJ (2012) Effective/census population size ratio estimation: a compendium and appraisal. Ecol Evol 2:2357–2365

    Article  PubMed  PubMed Central  Google Scholar 

  • Patriquin DG (1967) The biology of a relict population of Atlantic cod, Gadus morhua L., in Ogac Lake, Baffin Island, N.W.T. A thesis. Faculty of Graduate Studies and Research, Marine Sciences Centre, McGill University, Montreal, Canada

  • Pudovkin A, Zhdanova O, Hedgecock D (2010) Sampling properties of the heterozygote-excess estimator of the effective number of breeders. Conserv Genet 11:759–771

    Article  Google Scholar 

  • Reynolds J, Weir BS, Cockerham CC (1983) Estimation of the coancestry coefficient: basis for a short-term genetic distance. Genetics 105:767–779

    PubMed  CAS  PubMed Central  Google Scholar 

  • Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629

    Article  PubMed  Google Scholar 

  • Serebrov LI, Ignashkin VA (2002) An estimate of the population size of Kildin cod. In: Titov OV (ed) The relict Mogilnoe Lake (studies in 1997–2000). PINRO, Murmansk, pp 110–115 (in Russian)

    Google Scholar 

  • Shaffer ML (1981) Minimum population sizes for species conservation. Bioscience 31:131–134

    Article  Google Scholar 

  • Soulé ME (1980) Thresholds for survival: maintaining fitness and evolutionary potential. In: Soule ME, Wilcox BA (eds) Conservation biology: an evolutionary-ecological perspective. Sinauer Associates, Sunderland, pp 151–169

    Google Scholar 

  • Strelkov P, Shunatova N, Fokin M, Usov N, Fedyuk M, Malavenda S, Lubina O, Poloskin A, Korsun S (2014) Marine Lake Mogilnoe (Kildin Island, the Barents Sea): one hundred years of solitude. Polar Biol 37:297–310

    Article  Google Scholar 

  • Stroganov AN, Afanasiev KI, Rubtsova GA, Rakitskaya TA, Semenova AV (2011) Data on variability of microsattelite loci in Kildin cod Gadus morhua kildinensis (Gadidae). Voprosy Ikhtiologii 51:459–466 (in Russian)

    Google Scholar 

  • Stroganov AN, Mukhina NV, Afanasiev KI, Kotkin KA, Nikiforov AI, Rubtsova GA, Teterina AA, Zhivotovsky LA (2013) On the complex expeditions to Mogilnoe Lake (Kildin Island, the Barents Sea) in 2011 and 2012. Proc Astrakhan State Tech Univ Ser Fish 3:86–90 (in Russian)

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Titov OV, Serebrov LI, Karasev AB (2002) The Introduction. In: Titov OV (ed) The relict Mogilnoe Lake (Studies in 1997–2000). PINRO, Murmansk, pp 3–16 (in Russian)

    Google Scholar 

  • Waples RS (1991) Pacific Salmon, Oncorhynchus spp., and the definition of “species” under the Endangered Species Act. Mar Fish Rev 53:11–22

    Google Scholar 

  • Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262

    Article  PubMed  PubMed Central  Google Scholar 

  • Weir BS (1996) Genetic data analysis ii: methods for discrete population genetic data. Sinauer Associates, Sunderland

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Zaykin D, Zhivotovsky L, Weir BS (1995) Exact tests for association between alleles at arbitrary numbers of loci. Genetica (Netherlands) 96:169–178

    CAS  Google Scholar 

  • Zhivotovsky LA, Bennett L, Bowcock AM, Feldman MW (2000) Human population expansion and microsatellite variation. Mol Biol Evol 17:757–767

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are indebted to the Agency ‘Rosprirodnadzor’ at the Russian Ministry of Natural Resources and Ecology for permissions to obtain genetic samples from Kildin cod. We are thankful to Kirill Kotkin and Andrei Nikiforov for help in sampling from Mogilnoe Lake and Alexander Gvozdev for the White Sea cod sample. The research was supported in part by The Russian Foundation for Basic Research#12-04-00101 and #15-29-02421 (grants to LZh). We are grateful to Dr. Einar Nielsen and all anonymous reviewers for their valuable comments on the manuscript.

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Correspondence to Lev A. Zhivotovsky.

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Lev A. Zhivotovsky and Anastasia A. Teterina have contributed equally to this work.

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Zhivotovsky, L.A., Teterina, A.A., Mukhina, N.V. et al. Effects of genetic drift in a small population of Atlantic cod (Gadus morhua kildinensis Derjugin) landlocked in a meromictic lake: genetic variation and conservation measures. Conserv Genet 17, 229–238 (2016). https://doi.org/10.1007/s10592-015-0774-5

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