Population genetic structure and postglacial colonization of Atlantic salmon (Salmo salar) in the Baltic Sea area based on microsatellite DNA variation

Canadian Journal of Fisheries and Aquatic Sciences

Volumn 62, Issue 8, 2005, Pages 1887-1904

  Säisä, Marjatta ^a   Koljonen, Marja Liisa ^b   Gross, Riho ^c   Nilsson, Jan ^d   Tähtinen, Jaana ^a   Koskiniemi, Jarmo ^a   Vasemägi, Anti ^c,d  

^a UNIVERSITY OF HELSINKI   (Finland)

^b FINNISH FOREST RESEARCH INSTITUTE   (Finland)

^c ESTONIAN UNIVERSITY OF LIFE SCIENCES   (Estonia)

^d SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

COLONIZATION; GENETIC STRUCTURE; PHYLOGEOGRAPHY; POPULATION GENETICS; POSTGLACIAL; SALMONID;

ATLANTIC OCEAN; ATLANTIC OCEAN (NORTHEAST); BALTIC SEA; OCEANIC REGIONS; WORLD;

SALMO SALAR;

EID: 27744591506     PISSN: 0706652X     EISSN: None     Source Type: Journal    
DOI: 10.1139/f05-094     Document Type: Article

References (78)

1. Angers, B., and Bernatchez, L. 1998. Combined use of SMM and non-SMM methods to infer fine structure and evolutionary history of closely related brook charr (Salvelinus fontinalis, Salmonidae) populations from microsatellites. Mol. Biol. Evol. 15: 143-159.
2. Asplund, T., Veselov, A., Primmer, C.R., Bakhmet, I., Potutkin, A., Titov, S., Zubchenko, A., Studenov, I., Kaluzchin, S., and Lumme, J. 2004. Geographical structure and postglacial history of mtDNA haplotype variation in Atlantic salmon (Salmo salar L.) among rivers of the White and Barents Sea basins. Ann. Zool. Fenn. 41: 465-475.
3. Bernatchez, L., and Osinov, A. 1995. Genetic diversity of trout (genus Salmo) from its most eastern native range based on mitochondrial DNA and nuclear gene variation. Mol. Ecol. 4: 285-297.
4. Björck, J., Andrén, T., Wastegård, S., Possnert, G., and Schoning, K. 2002. An event stratigraphy for the Last Glacial-Holocene transition in eastern middle Sweden: results from investigations of varved clay and terrestrial sequences. Quat. Sci. Rev. 21: 1489-1501.
5. Bourke, E.A., Coughlan, J., Jansson, H., Galvin, P., and Cross, T.F. 1997. Allozyme variation in populations of Atlantic salmon located throughout Europe: diversity that could be compromised by introductions of reared fish. ICES J. Mar. Sci. 54: 974-985.
6. Bowcock, A.M., Ruiz-Linares, A., Tomfohrde, J., Minch, E., Kidd, J.R., and Cavalli-Sforza, L.L. 1994. High resolution of human evolutionary trees with polymorphic microsatellites. Nature (Lond.), 368: 455-457.
7. Brunner, P.C., Douglas, M.R., and Bernatchez, L. 1998. Microsatellite and mitochondrial DNA assessment of population structure and stocking effects in arctic charr Salvelinus alpinus (Teleostei: Salmonidae) from central alpine lakes. Mol. Ecol. 7: 209-223.
8. Christensen, O., and Larsson, P-O. (Editors). 1979. Review of Baltic salmon research, ICES Coop. Res. Rep. No. 89.
9. Consuegra, S., Garcia de Leániz, C., Serdino, A., González Morales, M., Straus, L.G., Knox, D., and Verspoor, E. 2002. Mitochondrial DNA variation in Pleistocene and modern Atlantic salmon from the Iberian glacial refugium. Mol. Ecol. 11: 2037-2048.
10. Cornuet, J.-M., and Luikart, G. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144: 2001-2014.
11. Crozier, W.W. 1998. Genetic implications of hatchery rearing in Atlantic salmon: effects of rearing environment on genetic composition. J. Fish Biol. 52: 1014-1025.
12. Edwards, S.W., and Beerli, P. 2000. Gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution, 54: 1839-1854.
13. El Mousadik, A., and Petit, R.J. 1996. High level of genetic differentiation from allelic richness among populations of the argan tree (Argania spinosa (L.) Skeels) endemic to Morocco. Theor. Appl. Genet. 92: 832-839.
14. Elo, K., Vuorinen, J., and Niemelä, E. 1994. Genetic resources of Atlantic salmon (Salmo salar L.) in Teno and Näätämö rivers, northernmost Europe. Hereditas, 120: 19-28.
15. Fleming, I.A., and Einum, S. 1997. Experimental tests of genetic divergence of farmed from wild Atlantic salmon due to domestication. ICES J. Mar. Sci. 54: 1051-1063.
16. Forstén, A., and Alhonen, P. 1975. The subfossil seals of Finland and their relations to the history of the Baltic Sea. Boreas, 4: 143-155.
17. García-Marín, J.-L., Utter, F.M., and Pla, C. 1999. Postglacial colonization of brown trout in Europe based on distribution of allozyme variants. Heredity, 82: 46-56.
18. Goudet, J. 1995. FSTAT (vers. 1.2): a computer program to calculate F-statistics. J. Hered. 86: 4865-486.
19. Goudet, J. 2001. FSTAT, a program to estimate and test gene diversities and fixation indeces (version 2.9.3). Université de Lausanne, Dorigny, Switzerland. Available from http://www2.unil.ch/popgen/softwares/fstat.htm [updated 15 July 2004].
20. Gross, R., Nilsson, J., Kohlmann, K., Lumme, J., Titov, S., and Veselov, A. 2003. Distribution of growth hormone 1 gene haplotypes among Atlantic salmon, Salmo salar L. populations in Europe. In Atlantic salmon: biology, conservation and restoration. Edited by A.J. Veselov, E.P. Ieshko, N.N. Nemova, O.P. Sterligova, and Y.A. Shustov. Pakoni, Petrozavodsk. pp. 32-37.
21. Guo, S.W., and Thompson, E.A. 1992. Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics, 48: 361-372.
22. Hardy, O.J., and Vekemans, X. 2002. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. Notes, 2: 618-620.
23. Hardy, O.J., Charbonnel, N., Freville, H., and Heuertz, M. 2003. Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics, 163: 1467-1482.
24. Hewitt, G.M. 1999. Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 68: 87-112.
25. Hey, J., and Machado, C.A. 2003. The study of structured populations - new hope for a difficult and divided science. Nat. Rev. Genet. 4: 535-543.
26. Hindar, K., Ryman, N., and Utter, F. 1991. Genetic effects of cultured fish on natural fish populations. Can. J. Fish. Aquat. Sci. 48: 945-956.
27. Jordan, W.C., and Youngson, A.F. 1991. Genetic protein variation and natural selection in Atlantic salmon (Salmo salar, L.) parr. J. Fish Biol. 39(Suppl. A): 185-192.
28. Kazakov, R.V., and Titov, S.F. 1991. Geographical patterns in the population genetics of Atlantic salmon, Salmo salar L., on U.S.S.R. territory, as evidence for colonisation routes. J. Fish Biol. 39: 1-6.
29. Kazakov, R.V., and Titov, S.F. 1993. Population genetics of salmon, Salmo salar L., in northern Russia. Aquacult. Fish. Manag. 24: 495-506.
30. King, T.L., Kalinowski, S.T., Schill, W.B., Spidle, A.P., and Lubinski, B.A. 2001. Population structure of Atlantic salmon (Salmo salar L.): a range-wide perspective from microsatellite DNA variation. Mol. Ecol. 10: 807-821.
31. Koljonen, M.-L. 1989. Electrophoretically detectable genetic variation in natural and hatchery stocks of Atlantic salmon in Finland. Hereditas, 10: 23-35.
32. Koljonen, M.-L., Jansson, H., Paaver, T., Vasin, O., and Koskiniemi, J. 1999. Phylogeographic lineages and differentiation pattern of Atlantic salmon (Salmo salar) in the Baltic Sea with management implications. Can. J. Fish. Aquat. Sci. 56: 1766-1780.
33. Koljonen, M.-L., Tähtinen, J., Säisä, M., and Koskiniemi, J. 2002. Maintenance of genetic diversity of Atlantic salmon by captive breeding programmes and the geographic distribution of microsatellite variation. Aquaculture, 212: 69-92.
34. Kontula, T., and Väinölä, R. 2001. Postglacial colonization of northern Europe by distinct phylogeographic lineages of the bullhead, Cottus gobio. Mol. Ecol. 10: 1983-2002.
35. Koskinen, M.T., Ranta, E., Piironen, J., Veselov, A., Titov, S., Haugen, T.O., Nilsson, J., Carlstein, M., and Primmer, C.R. 2000. Genetic lineages and postglacial colonization of grayling (Thymallus thymallus, Salmonidae) in Europe, as revealed by mitochondrial DNA analyses. Mol. Ecol. 9: 1609-1624.
36. Kumar, S., Tamura, K., Jakobsen, I., and Nei, M. 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics, 17: 1244-1245.
37. Mangerud, J., Astakhov, V.I., Murray, A., and Svendsen, J.E. 2001. The chronology of a large ice-dammed lake and the Barents-Kara ice sheet advances, northern Russia. Global Planet. Change, 31: 321-336
38. Mangerud, J., Astakhov, V.I., and Svendsen, J.E. 2002. The extent of the Barents-Kara ice sheet during the Last Glacial Maximum. Quat. Sci. Rev. 21: 111-119.
39. Mangerud, J., Jakobsson, M., Alexanderson, H., Astakhov, V., Clarke, G., Henrikson, M., Hjort, C., Krinner, G., Lunkka, J.-P., Möller, P., Murray, A., Nikolskaya, O., Saarnisto, M., and Svendsen, J. 2004. Ice-dammed lakes and rerouting of the drainage of northern Eurasia during the last glaciation. Quat. Sci. Rev. 23: 1313-1332.
40. Marks, L. 2002. Last glacial maximum in Poland. Quat. Sci. Rev. 21: 103-110.
41. McConnell, S.K., O'Reilly, P., Hamilton, L., Wright, J.M., and Bentzen, P. 1995. Polymorphic microsatellite loci from Atlantic salmon (Salmo salar): genetic differentiation of North American and European populations. Can. J. Fish. Aquat. Sci. 52: 1863-1872.
42. Nei, M. 1973. Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. U.S.A. 70: 3321-3323.
43. Nei, M. 1977. F-statistics and analysis of gene diversity in subdivided populations. Ann. Hum. Genet. 41: 225-233.
44. Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89: 583-590.
45. Nei, M., Tajima, F., and Tateno, Y. 1983. Accuracy of estimated phylogenetic trees from molecular data. J. Mol. Evol. 19: 153-170.
46. Nesbø, C.L., Fossheim, T., Vøllestad, L.A., and Jakobsen, K.S. 1999. Genetic divergence and phylogeographic relationships among European perch (Perca fluviatilis) populations reflect glacial refugia and postglacial colonization. Mol. Ecol. 8: 1387-1404.
47. Nilsson, J. 1997. MtDNA and microsatellite variation in Baltic Atlantic salmon. ICES J. Mar. Sci. 54: 1173-1176.
48. Nilsson, J., Gross, R., Asplund, T., Dove, O., Jansson, H., Kelloniemi, J., Kohlmann, K., Löytynoja, A., Nielsen, E.E., Paaver, T., Primmer, C.R., Titov, S., Vasemägi, A., Veselov, A., Ost, T., and Lumme, J. 2001. Matrilinear phylogeography of Atlantic salmon (Salmo salar L.) in Europe and postglacial colonization of the Baltic Sea area. Mol. Ecol. 10: 89-102.
49. Norris, A.T., Bradley, D.G., and Cunningham, E.P. 1999. Microsatellite variation between and within farmed and wild Atlantic salmon (Salmo salar) populations. Aquaculture, 180: 247-264.
50. O'Reilly, P.T., Hamilton, L.C., McConnell, S.K., and Wright, J.M. 1996. Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Can. J. Fish. Aquat. Sci. 53: 2292-2298.
51. Ota, T. 1993. DISPAN: genetic distance and phylogenetic analysis software. Pennsylvania State University, University Park, Pa.
52. Petit, R.J., El Mousadik, A., and Pons, O. 1998. Identifying populations for conservation on the basis of genetic markers. Conserv. Biol. 12: 844-855.
53. Piry, S., Luikart, G., and Cornuet, J.-M. 1999. BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J. Hered. 90: 502-503.
54. Raymond, M., and Rousset, F. 1995. GENEPOP (version 1.2): population genetics software for exact test and ecumenicism. J. Hered. 86: 248-249.
55. Rice, W.R. 1989. Analyzing tables of statistical tests. Evolution, 43: 223-225.
56. Ring, O., and Hanell, L. 1987. Genetisk bakgrund till avelsstammarna av Gullspångslax och Gullspångsöring. Information från Sötvattenslaboratoriet Drottningholm [Genetic background of brood stocks of Gullspång salmon and brown trout at the Fisheries Boards Kälarne hatchery]. Information from Institute of Freshwater Research of the Swedish National Board of Fisheries No. 6, Drottningholm, Sweden. [In Swedish with English summary.]
57. Rousset, F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics, 145: 1219-1228.
58. Ryman, N. 1991. Conservation genetics considerations in fishery management. J. Fish Biol. 39(Suppl. A): 211-224.
59. Saarnisto, M., Grönlund, T., and Ekman, I. 1995. Late glacial of Lake Onega - contribution to the history of the eastern Baltic basin. Quat. Int. 27: 111-120.
60. Saarnisto, S., and Saarinen, T. 2001. Deglaciation chronology of the Scandinavian ice sheet from the Lake Onega Basin to the Salpausselkä end moraines. Global Planet. Change, 31: 387-405.
61. Säisä, M., Koljonen, M.-L., and Tähtinen, J. 2003. Genetic changes in Atlantic salmon stocks since historical times and the effective population size of a long-term captive breeding programme. Conserv. Genet. 4: 613-627.
62. Saitou, N., and Nei, M. 1987. The neighborjoining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
63. Sanchez, J.A., Clabby, C., Ramos, D., Blanco, G., Ravin, F., Vazquez, E., and Powell, R. 1996. Protein and microsatellite single locus variability in Salmo salar L. (Atlantic salmon). Heredity, 77: 423-432.
64. Slettan, A., Olsaker, I., and Lie, O. 1995. Atlantic salmon, Salmo salar, microsatellites at the SSOSL25, SSOSL85, SSOSL311, SSOSL417 loci. Anim. Genet. 26: 277-285.
65. Slettan, A., Olsaker, I., and Lie, O. 1996. Polymorphic Atlantic salmon (Salmo salar) microsatellites at the SSOSL438, SSOSL439, and SSOSL444 loci. Anim. Genet. 27: 57-58.
66. Ståhl, G. 1987. Genetic population structure of Atlantic salmon. In Population genetics and fishery management. Edited by N. Ryman and F. Utter. University of Washington Press, Seattle, Wash. pp. 121-141.
67. Svendsen, J.I., Astakhov, V.I., Bolshiyanov, D.Yu., Demidov, I., Dowdeswell, J.A., Gataullin, V., Hjort, C., Hubberten, H.W., Larsen, E., Mangerud, J., Melles, M., Möller, P., Saarnisto, M., and Siegert, M.J. 1999. Maximum extent of the Eurasian ice sheets in the Barents and Kara Sea region during the Weichselian. Boreas, 28: 234-242.
68. Taggart, J.B., Hynes, R.A., Prodöhl, P.A., and Ferguson, A. 1992. A simplified protocol for routine total DNA isolation from salmonid fishes. J. Fish Biol. 40: 963-965.
69. Takezaki, N. 1998. NJBAFD: Neighbor-joining tree construction from allele frequency data. National Institute of Genetics, Misima, Sizuoka-ken, Japan.
70. Takezaki, N., and Nei, M. 1996. Genetic distances and reconstruction of phylogenetic trees from microsatellite data. Genetics, 144: 389-399.
71. Taylor, E.B. 1991. A review of local adaptations in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture, 98: 185-207.
72. Ukkonen, P. 1993. The post-glacial history of the Finnish mammalian fauna. Ann. Zool. Fenn. 30: 249-264.
73. Verspoor, E. 1988. Reduced genetic variability in first generation populations of Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 45: 1686-1690.
74. Verspoor, E., and Jordan, W.C. 1989. Genetic variation at the Me-2 locus in the Atlantic salmon within and between rivers: evidence for its selective maintenance. J. Fish Biol. 35(Suppl. A): 205-213.
75. Verspoor, E., McCarthy, E.M., Knox, D., Bourke, E.A., and Cross, T.F. 1999. The phylogeography of European Atlantic salmon (Salmo salar L.) based on RFLP analysis of the ND1/16sRNA region of the mtDNA. Biol. J. Linn. Soc. 68: 129-146.
76. Vuorinen, J. 1982. Little genetic variation in the Finnish lake salmon, Salmo salar sebago (Girard). Hereditas, 101: 97-102
77. Weir, B.C., and Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38: 1350-1370.
78. Wennevik, V., Skaala, Ø., Titov, S.F., Studyonov, I., and Nævdal, G. 2004. Microsatellite variation in populations of Atlantic Salmon from North Europe. Environ. Biol. Fishes, 69: 143-152.