Temporal variation of genetic composition in Atlantic salmon populations from the Western White Sea Basin: influence of anthropogenic factors?

BMC Genetics

Craig R Primmer¹  Jaakko Lumme²  Alexey E Veselov³  Mikhail Yu Ozerov⁴ 

[1] Department of Biology, Division of Genetics and Physiology, University of Turku, 20014 Turku, Finland;Department of Biology, University of Oulu, P.O. Box 3000, 90014 Oulu, Finland;Institute of Biology, Karelian Research Centre RAS, Pushkinskaya 11, 185610 Petrozavodsk, Russia;Kevo Subarctic Research Institute, University of Turku, Turku 20014, Finland

关键词: Fishing pressure;    Genetic structure;    Genetic diversity;    Temporal variation;    Atlantic salmon;   

Others  :  1086645
DOI  :  10.1186/1471-2156-14-88

 received in 2013-05-25, accepted in 2013-09-19,  发布年份 2013

【 摘 要 】

Background

Studies of the temporal patterns of population genetic structure assist in evaluating the consequences of demographic and environmental changes on population stability and persistence. In this study, we evaluated the level of temporal genetic variation in 16 anadromous and 2 freshwater salmon populations from the Western White Sea Basin (Russia) using samples collected between 1995 and 2008. To assess whether the genetic stability was affected by human activity, we also evaluated the effect of fishing pressure on the temporal genetic variation in this region.

Results

We found that the genetic structure of salmon populations in this region was relatively stable over a period of 1.5 to 2.5 generations. However, the level of temporal variation varied among geographical regions: anadromous salmon of the Kola Peninsula exhibited a higher stability compared to that of the anadromous and freshwater salmon from the Karelian White Sea coast. This discrepancy was most likely attributed to the higher census, and therefore effective, population sizes of the populations inhabiting the rivers of the Kola Peninsula compared to salmon of the Karelian White Sea coast. Importantly, changes in the genetic diversity observed in a few anadromous populations were best explained by the increased level of fishing pressure in these populations rather than environmental variation or the negative effects of hatchery escapees. The observed population genetic patterns of isolation by distance remained consistent among earlier and more recent samples, which support the stability of the genetic structure over the period studied.

Conclusions

Given the increasing level of fishing pressure in the Western White Sea Basin and the higher level of temporal variation in populations exhibiting small census and effective population sizes, further genetic monitoring in this region is recommended, particularly on populations from the Karelian rivers.

【 授权许可】

   
2013 Ozerov et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Tessier T, Bernatchez L: Stability of population structure and genetic diversity across generations assessed by microsatellites among sympatric populations of freshwater Atlantic salmon (Salmo salar L.). Mol Ecol 1999, 8:169-179.
• [2]Waples RS: Conservation genetics of Pacific salmon: II: effective population size and the rate of loss of genetic variability. J Hered 1990, 81:267-276.
• [3]Frankham R, Ballou JD, Briscoe DA: Introduction to conservation genetics. Cambridge: Cambridge University Press UK; 2003.
• [4]Reed DH, Frankham R: Correlation between fitness and genetic diversity. Cons Biol 2003, 17:230-237.
• [5]Ebert D, Haag C, Kirkpatrick M, Riek M, Hottinger JW, Pajunen VI: A selective advantage to immigrant genes in a Daphnia metapopulation. Science 2002, 295:485-488.
• [6]Hendry AP, Taylor EB, McPhail JD: Adaptive divergence and the balance between selection and gene flow: lake and stream stickleback in the misty system. Evolution 2002, 56:1199-1216.
• [7]Hansen MM, Ruzzante DE, Nielsen EE, Bekkevold D, Mensberg KLD: Long-term effective population sizes, temporal stability of genetic composition and potential for local adaptation in anadromous brown trout (Salmo trutta) populations. Mol Ecol 2002, 11:2523-2535.
• [8]Hendry AP: Selection against migrants contributes to the rapid evolution of ecologically dependent reproductive isolation. Evol Ecol Res 2004, 6:1219-1236.
• [9]Stabell OB: Homing and olfaction in salmonids–a critical review with special reference to the Atlantic salmon. Biol Rev Camb Philos Soc 1984, 59:333-388.
• [10]Garant D, Dodson JJ, Bernatchez L: Ecological determinants and temporal stability of the within-river population structure in Atlantic salmon (Salmo salar L.). Mol Ecol 2000, 9:615-628.
• [11]Primmer CR, Veselov A, Zubchenko A, Poututkin A, Bakhmet I, Koskinen MT: Isolation by distance within a river system: genetic population structuring of Atlantic salmon, Salmo salar, in tributaries of the Varzuga River in northwest Russia. Mol Ecol 2006, 15:653-666.
• [12]Vähä J-P, Erkinaro J, Niemelä E, Primmer CR: Life-history and habitat features influence the within–river genetic structure of Atlantic salmon. Mol Ecol 2007, 16:2638-2654.
• [13]Hendry AP, Castric V, Kinnison MT, Quinn TP: The evolution of philopatry and dispersal: homing versus straying in salmonids. In Evolution illuminated: salmon and their relatives. Edited by Hendry AP, Stearns SC. New York: Oxford University Press; 2004:52-91.
• [14]Laikre L, Palm S, Ryman N: Genetic population structure of fishes: implications for coastal zone management. Ambio 2005, 34:111-117.
• [15]Fraser DJ, Jones MW, McParland TL, Hutchings JA: Loss of historical immigration and the unsuccessful rehabilitation of extirpated salmon populations. Conserv Genet 2007, 8:527-546.
• [16]Schwartz MK, Luikart G, Waples RS: Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 2007, 22:25-33.
• [17]Yamamoto S, Morita K, Koizumi I, Maekawa K: Genetic differentiation of white-spotted charr (Salvelinus leucomaenis) populations after habitat fragmentation: spatial-temporal changes in gene frequencies. Conserv Genet 2004, 5:529-538.
• [18]Vasemägi A, Gross R, Paaver T, Koljonen ML, Nilsson J: Extensive immigration from compensatory hatchery releases into wild Atlantic salmon population in the Baltic Sea: the analysis of population structure. Evolution 2005, 38:1358-1370.
• [19]Finnegan AK, Stevens JR: Assessing the long-term genetic impact of historical stocking events on contemporary populations of Atlantic salmon, Salmo salar. Fish Manag Ecol 2008, 15:315-326.
• [20]Jordan WC, Youngson AF, Hay DW, Ferguson A: Genetic protein variation in natural populations of Atlantic salmon (Salmo salar) in Scotland: temporal and spatial variation. Can J Fish Aquat Sci 1992, 49:1863-1872.
• [21]Palstra FP, O’Connell MF, Ruzzante DE: Age structure, changing demography and effective population size in Atlantic salmon (Salmo salar). Genetics 2009, 182:1233-1249.
• [22]Vähä JP, Erkinaro J, Niemelä E, Primmer CR: Temporally stable genetic structure and low migration in an Atlantic salmon population complex: implications for conservation and management. Evol Appl 2008, 1:137-154.
• [23]Ozerov M, Veselov A, Lumme J, Primmer C: Genetic structure of freshwater Atlantic salmon (Salmo salar L.) populations from the lakes Onega and Ladoga of northwest Russia and implications for conservation. Conserv Genet 2010, 11:1711-1724.
• [24]Ensing D, Prodöhl PA, McGinnity P, Boylan P, O’Maoiléidigh N, Crozier WW: Complex pattern of genetic structuring in the Atlantic salmon (Salmo salar L.) of the River Foyle system in northwest Ireland: disentangling the evolutionary signal from population stochasticity. Ecol Evol 2011, 1:359-372.
• [25]Glover KA, Quintela M, Wennevik V, Besnier F, Sørvik AGE, Skaala Ø: Three decades of farmed escapees in the wild: a spacio-temporal analysis of Atlantic salmon population genetic structure throughout Norway. PLoS ONE 2012, 7:e43129.
• [26]Palstra FP, Ruzzante DE: A temporal perspective on population structure and gene flow in Atlantic salmon (Salmo salar) in Newfoundland, Canada. Can J Fish Aquat Sci 2010, 67:225-242.
• [27]McElligott EA, Cross TF: Protein variation in wild Atlantic salmon, with particular reference to southern Ireland. J Fish Biol 1991, 39(Suppl A):35-42.
• [28]Moffett IJJ, Crozier WW: A study of temporal genetic variation in a natural population of Atlantic salmon in the River Bush, Northern Ireland. J Fish Biol 1996, 48:302-306.
• [29]Skaala Ø, Wennevik V, Glover KA: Evidence of temporal genetic change in wild Atlantic salmon, Salmo salar L., populations affected by farm escapees. ICES J Mar Sci 2006, 63:1224-1233.
• [30]Parrish DL, Behnke RJ, Gephard SR, McCormick SD, Reeves GH: Why aren’t there more Atlantic salmon (Salmo salar)? Can J Fish Aquat Sci 1998, 55:281-287.
• [31]Veselov AE: Inventory and systematization of spawning rivers of the Atlantic salmon in the Murmansk oblast and Karelia. Doklady Biol Sci 2006, 407:158-162.
• [32]Tonteri A, Veselov AJE, Zubchenko A, Lumme J, Primmer C: Microsatellites reveal clear genetic boundaries among Atlantic salmon (Salmo salar L.) populations from Barents and White seas. Can J Fish Aquat Sci 2009, 66:717-735.
• [33]Schurov IL, Shirokov VA, Gaida RV, Tyrkin IA, Shulman BS: The status of natural reproduction of freshwater salmon (Salmo salar morpha Sebago Girard) populations in Republic of Karelia. In Proceedings of the 1st international conference on reproduction of natural populations of valuable fish species. Sankt-Petersburg, Russia: State Research Institute of Lake and River Fisheries (GosNIORKh), Sankt-Petersburg, Russia; 2010:253-255. in Russian
• [34]Alekseev MYU, Zubchenko AV: Reproduction status and measures for salmon (Salmo salar L.) stock restoration in the River Umba (Kola Peninsula). In Proceedings of the 2nd international conference on reproduction of natural populations of valuable fish species. Sankt-Petersburg, Russia: State Research Institute of Lake and River Fisheries (GosNIORKh), Sankt-Petersburg, Russia; 2013:12-15. in Russian
• [35]Veselov AE, Sysoyeva MI, Potutkin AG: The patern of Atlantic salmon smolt migration in the Varsuga River (White Sea basin). Nordic J Freshw Res 1998, 74:65-78.
• [36]Vorobyova NK, Mitenev VK, Karasev AV: Biology, reproduction and status of the stocks of anadromous and freshwater fishes of the Kola Peninsula. Murmansk: PINRO Press; 2005. (in Russian)
• [37]Zubchenko AV, Veselov AJ, Kalyuzhin SM, Shustov YA, Alikov LV: Reproductive potential of Atlantic salmon reproducing in the rivers of the Kola Peninsula. In Researches on ichthyology and adjacent disciplines of inland water bodies at the beginning of XXI century (for 80-years anniversary of Prof. L.A. Kudersky). 337th edition. : SPb; 2007:375-385. [Proceedings of GosNIOKhR] in Russian
• [38]Zubchenko AV, Loenko AA, Popov NG, Antonova P, Valetov VA: Fishery for and status of Atlantic salmon stocks in north-west Russia in 1994. ICES CM 1994, M:40.
• [39]Ryman N, Palm S: POWSIM: a computer program for assesing statistical power when testing for genetic differentation. Mol Ecol 2006, 6:600-602.
• [40]Ryman N, Palm S, André C, Carvalho GR, Dahlgren TG, Jorde PE, Laikre L, Larsson LC, Palmé A, Ruzzante DE: Power for detecting genetic divergence: differences between statistical methods and marker loci. Mol Ecol 2006, 15:2031-2045.
• [41]Ryman N: CHIFISH: a computer program testing for genetic heterogeneity at multiple loci using chi-square and Fisher’s exact test. Mol Ecol 2006, 6:285-287.
• [42]Ozerov MY, Veselov AE, Lumme J, Primmer CR: “Riverscape” genetics: river characteristics influence the genetic structure and diversity of anadromous and freshwater Atlantic salmon (Salmo salar) populations in northwest Russia. Can J Fish Aquat Sci 2012, 69:1947-1958.
• [43]Nielsen EE, Hansen MM, Loeschcke V: Analysis of DNA from old scale samples: technical aspects, applications and perspectives for conservation. Hereditas 1999, 130:265-276.
• [44]Palstra FP, O’Connell MF, Ruzzante DE: Population structure and gene flow reversals in Atlantic salmon (Salmo salar) over contemporary and long-term temporal scales: effects of population size and life history. Mol Ecol 2007, 16:4504-4522.
• [45]Veselov AE, Pavlov DS, Primmer CR, Kalyuzhin SM, Lumme JI, Sysoeva MI, Ozerov MYU: Salmon spawning rivers of East Fennoscandia. In Proceedings of the XXVIII international conference on biological resources of the White Sea and inland waters of European North. Petrozavodsk, Russia: Institute of Biology, Karelian Research Center of RAS, Petrozavodsk, Russia; 2009:111-116. in Russian
• [46]Artamonova VS, Makhrov AA, Krylova SS, Lazareva LV, Prischepa BF: Releases of young salmon in “alien” rivers and an efficacy of fish hatchery work. Questions of fisheries 2002, 3:463-473. (in Russian)
• [47]Waples RS, Teel DJ: Conservation genetics of pacific salmon: I: temporal changes in allele frequency. Cons Biol 1990, 4:144-156.
• [48]Miller LM, Kapuscinski AR: Historical analysis of genetic variation reveals low effective population size in a northern pike (Esox lucius) population. Genetics 1997, 147:1249-1258.
• [49]Einum S, Fleming IA, Côté IM, Reynolds JD: Population stability in salmon species: effects of population size and female reproductive allocation. J Anim Ecol 2003, 72:811-821.
• [50]Nilsson J, Gross R, Asplund T, Dove O, Jansson H, Kelloniemi J, Kohlmann K, Löytynoja A, Nielsen EE, Paaver T, Primmer CR, Titov S, Vasemägi A, Veselov A, Öst T, Lumme J: Matrilinear phylogeography of Atlantic salmon (Salmo salar L.) in Europe and postglacial colonization of the Baltic Sea area. Mol Ecol 2001, 10:89-102.
• [51]Tonteri A, Titov S, Veselov A, Zubchenko A, Koskinen MT, Lesbarreres D, Kalyuzhin S, Bakhmet I, Lumme J, Primmer CR: Phylogeography of anadromous and non-anadromous Atlantic salmon (Salmo salar) from northern Europe. Ann Zool Fennici 2005, 42:1-22.
• [52]Tonteri A, Veselov AJE, Titov SI, Lumme J, Primmer CR: The effect of migratory behaviour on genetic diversity and population divergence: a comparison of anadromous and freshwater Atlantic salmon Salmo salar. J Fish Biol 2007, 70:381-398.
• [53]Hutchison DW, Templeton AR: Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 1999, 53:1898-1914.
• [54]Moran P, Pendas AM, Garsia-Vasquez E, Izquierdo JI, Lobon-Cervia J: Estimates of gene flow among neighbouring populations of brown trout. J Fish Biol 1995, 46:593-602.
• [55]Hansen MM, Mensberg KLD: Genetic differentiation and relationship between genetic and geographical distance in Danish sea trout (Salmo trutta L.) populations. Heredity 1998, 81:493-504.
• [56]Knutsen H, Knutsen JA, Jorde PE: Genetic evidence for mixed origin of recolonized sea trout populations. Heredity 2001, 87:207-214.
• [57]King TL, Kalinovski ST, Schill WB, Spidle AP, Lubinski BA: Population structure of Atlantic salmon (Salmo salar L.): a range-wide perspective from microsatellite DNA variation. Mol Ecol 2001, 10:807-821.
• [58]Koljonen ML: Conservation goals and fisheries management units for Atlantic salmon in the Baltic Sea area. J Fish Biol 2001, 59(Suppl A):269-288.
• [59]Goudet J: FSTAT (version 1.2): a computer program to calculate F-statistics. J Heredity 1995, 86:485-486.
• [60]Weir BS, Cockerham CC: Estimating F-statistics for the analysis of population structure. Evolution 1984, 38:1358-1370.
• [61]Guo SW, Thompson EA: Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 1992, 48:361-372.
• [62]Raymond M, Rousset F: GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 1995, 86:248-249.
• [63]Brookfield JFY: A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 1996, 5:453-455.
• [64]Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P: MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 2004, 4:535-538.
• [65]Goudet J: PCA-GEN for windows V. 1.2. Lausanne: Institute of Ecology; University of Lausanne; 1999.
• [66]Nei M, Tajima F, Tateno Y: Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 1983, 19:153-170.
• [67]Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4:406-425.
• [68]Langella O: Populations 1.2.28 (12/5/2002): a population genetic software. Montpellier: Laboratoire Populations, génétique et evolution; 1999. CNRS UPR9034. Available at http://bioinformatics.org/ webcite~tryphon/populations/
• [69]Excoffier L, Laval G, Schneider S: Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 2005, 1:47-50.
• [70]Power G: Estimates of age, growth, standing crop and production of salmonids in some North Norwegian rivers and streams. Rep Ins Freshw Res Drotningholm 1973, 53:78-111.
• [71]Peakall R, Smouse PE: GENALEX 6: genetic analysis in Excel: population genetic software for teaching and research. Mol Ecol Notes 2006, 6:288-295.