Population structure of lake trout (Salvelinus namaycush) in a large glacial-fed lake inferred from microsatellite DNA and morphological analysis

Canadian Journal of Fisheries and Aquatic Sciences

Volumn 67, Issue 7, 2010, Pages 1171-1186

  Northrup, Sara ^a   Connor, Mark ^b   Taylor, Eric B ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Taku River Tlingit First Nation Fisheries Department   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CONSERVATION STATUS; GENETIC ANALYSIS; GENETIC DIFFERENTIATION; GENETIC MARKER; GLACIAL LAKE; INTRASPECIFIC VARIATION; MORPHOLOGY; PHENOTYPIC PLASTICITY; POPULATION STRUCTURE; PRISTINE ENVIRONMENT; SALMONID; STOCK ASSESSMENT;

ATLIN LAKE; CANADA; TAGISH LAKE;

SALMONIDAE; SALVELINUS NAMAYCUSH;

EID: 77955132482     PISSN: 0706652X     EISSN: None     Source Type: Journal    
DOI: 10.1139/F10-054     Document Type: Article

References (84)

1. Alfonso, N.R. 2004. Evidence for two morphotypes of lake charr, Salvelinus namaycush, from Great Bear Lake, Northwest Territories, Canada. Environ. Biol. Fishes, 71(1): 21-32. doi:10. 1023/B:EBFI.0000043176.61258.3d.
2. Allendorf, F.W., and Luikart, G. 2007. Conservation and the genetics of populations. Blackwell Publishing, Oxford, UK.
3. Anderson, E.C., Waples, R.S., and Kalinowski, S.T. 2008. An improved method for predicting the accuracy of genetic stock identification. Can. J. Fish. Aquat. Sci. 65(7): 1475-1486. doi:10. 1139/F08-049.
4. Belkhir, K., Castric, V., and Bonhomme, F. 2002. IDENTIX, a software to test for relatedness in a population using permutation methods. Mol. Ecol. Notes, 2(4): 611-614., doi:10.1046/j.1471-8286.2002.00273.x
5. Bernatchez, L., and Wilson, C.C. 1998. Comparative phylogeography of Nearctic and Palearctic fishes. Mol. Ecol. 7(4): 431-452. doi:10.1046/j.1365-294x.1998.00319.x.
6. Blackie, C.T., Weese, D.J., and Noakes, D.L.G. 2003. Evidence for resource polymorphism in the lake charr (Salvenlinus namaycush) population of Great Bear Lake, Northwest Territories, Canada. Ecoscience, 10: 509-514.
7. Bodaly, R.A., and Lindsey, C.C. 1977. Pleistocene watershed exchanges and the fish fauna of the Peel River Basin, Yukon Territory. J. Fish. Res. Board Can. 34: 388-395.
8. Bohonak, A.J. 1999. Dispersal, gene flow, and population structure. Q. Rev. Biol. 74(1): 21-45. doi:10.1086/392950. PMID:10081813.
9. Bookstein, F.L. 1991. Morphometric tools for landmark data: geometry and biology. Cambridge University Press, New York.
10. Booth, R.E., and Grime, J.P. 2003. Effects of genetic impoverishment on plant community diversity. J. Ecol. 91(5): 721-730. doi:10.1046/j.1365-2745.2003.00804.x.
11. Bowen, B.W. 1999. Preserving genes, species, or ecosystems? Healing the fractured foundations of conservation policy. Mol. Ecol. 8(12, Suppl. 1): S5-S10. doi:10.1046/j.1365-294X.1999.00798.x. PMID:10703547.
12. Bronte, C.R., and Moore, S.A. 2007. Morphological variation of siscowet lake trout in Lake Superior. Trans. Am. Fish. Soc. 136(2): 509-517. doi:10.1577/T06-098.1.
13. Brown, E.H., Jr., Eck, G.W., Foster, N.R., Horrall, R.M., and Coberly, C.E. 1981. Historical evidence for discrete stocks of lake trout (Salvelinus namaycush) in Lake Michigan. Can. J. Fish. Aquat. Sci. 38(12): 1747-1758. doi:10.1139/f81-223.
14. Crispo, E., and Hendry, A.P. 2005. Does time since colonization influence isolation-by-distance? A meta-analysis. Conserv. Genet. 6(5): 665-682. doi:10.1007/s10592-005-9026-4.
15. Currens, K.P., Schreck, C.B., and Li, H.W. 1990. Allozyme and morphological divergence of rainbow trout (Oncorhynhcus my-kiss) above and below waterfalls in the Deschutes River, Oregon. Copeia, 1990(3): 730-746. doi:10.2307/1446439.
16. Dehring, T.R., Brown, A.F., Daugherty, C.H., and Phelps, S.R. 1981. Survey of the genetic variation among eastern Lake Superior lake trout (Salvelinus namaycush). Can. J. Fish. Aquat. Sci. 38(12): 1738-1746. doi:10.1139/f81-222.
17. DeKoning, J., Keatley, K., Phillips, R., Rhydderch, J., Janssen, J., and Noakes, M. 2006. Genetic analysis of wild lake trout embryos recovered from Lake Michigan. Trans. Am. Fish. Soc. 135(2): 399-407. doi:10.1577/T05-044.1.
18. DeWoody, J.A., and Avise, J.C. 2000. Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J. Fish Biol. 56(3): 461-473., doi:10.1111/j.1095-8649.2000.tb00748.x
19. Dextrase, A.J., and Mandrak, N.E. 2006. Impacts of alien invasive species on freshwater fauna at risk in Canada. Biol. Invasions, 8(1): 13-24. doi:10.1007/s10530-005-0232-2.
20. Evanno, G., Regnaut, S., and Goudet, J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14(8): 2611-2620. doi:10.1111/j. 1365-294X.2005.02553.x. PMID:15969739.
21. Excoffier, L., Smouse, P.E., and Quattro, J.M. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131(2): 479-491. PMID:1644282.
22. Excoffier, L., Laval, G., and Schneider, S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol. Bioinform. Online, 1: 47-50. PMID:19325852.
23. Fraley, D., and Raftery, A.E. 2003. Enhanced model-based clustering, density estimation, and discriminant analysis software: MCLUST. J. Classif. 20(2): 263-286 http://www.stat. washington.edu/fraley/mclust. doi:10.1007/s00357-003-0015-3.
24. Frankam, R., Ballou, J.D., and Briscoe, D.A. 2002. Introduction to conservation genetics. United Kingdom University Press, Cambridge, UK.
25. Fraser, D.J., Duchesne, P., and Bernatchez, L. 2005. Migratory charr schools exhibit population and kin associations beyond juvenile stages. Mol. Ecol. 14(10): 3133-3146. doi:10.1111/j.1365-294X.2005.02657.x. PMID:16101779.
26. Futuyma, D.J. 1997. Evolutionary biology. Sinauer, Sunderland, Mass.
27. Goudet, J. 1999. PCA-GEN for Windows. Available from the Institute of Ecology, Biology Building, University of Lausanne, Lausanne, Switzerland.
28. Goudet, J. 2001. FSTAT version 2.9.3.1. Updated from Goudet, J. (1995). J. Hered. 86: 485-486.
29. Grewe, P.M., Krueger, C.C., Marsden, J.E., Aquadro, C.F., and May, B. 1994. Hatchery origins of naturally produced lake trout fry captured in Lake Ontario: temporal and spatial variability based on allozyme and mitochondrial DNA data. Trans. Am. Fish. Soc. 123(3): 309-320. doi:10.1577/1548-8659(1994) 123<0309:HOONPL>2.3.CO;2.
30. Guinand, B., Scribner, K.T., Page, K.S., and Burnham-Curtis, M.K. 2003. Genetic variation over space and time: analyses of extinct and remnant lake trout populations in the upper Great Lakes. Proc. R. Soc. Lond. Ser. B Biol. Sci. 270(1513): 425-433. doi:10.1098/rspb.2002.2250.
31. Gunn, J.M., Steedman, R.J., and Ryder, R.A. 2003. Boreal shield watersheds: lake trout ecosystems in a changing environment. CRC Press, Boca Raton, Florida.
32. Hammer, Ø., Harper, D.A.T., and Ryan, P.D. 2001. PAST: palaeontological statistics software package for education and data analysis. Palaeontol. Electronica, 4: 1-9.
33. 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(4): 618-620. doi:10. 1046/j.1471-8286.2002.00305.x.
34. Hendry, A.P., and Taylor, E.B. 2004. How much of the variation in adaptive divergence can be explained by gene flow? An evaluation using lake-stream stickleback pairs. Evolution, 58(10): 2319-2331. PMID:15562693.
35. Hendry, A.P., Castric, V., Kinnison, M.T., and Quinn, T.P. 2004. The evolution of dispersal: homing versus straying in salmonids. In Evolution illuminated: salmon and their relatives. Edited by A.P. Hendry and S.C. Stearns. Oxford University Press, Oxford, UK. pp. 52-91.
36. Hilborn, R. 2007. Managing fisheries is managing people: what has been learned? Fish Fish. 8: 282-296.
37. Hilborn, R., Quinn, T.P., Schindler, D.E., and Rogers, D.E. 2003. Biocomplexity and fisheries sustainability. Proc. Natl. Acad. Sci. U.S.A. 100(11): 6564-6568. doi:10.1073/pnas.1037274100. PMID:12743372.
38. Ihssen, P.E., Casselman, J.M., Martin, G.W., and Phillips, R.B. 1988. Biochemical genetic differentiation of lake trout (Salvelinus namaycush) stocks of the Great Lakes region. Can. J. Fish. Aquat. Sci. 45(6): 1018-1029. doi:10.1139/f88-125.
39. Imre, I., McLaughlin, R.L., and Noakes, D.L.G. 2002. Phenotypic plasticity in brook charr: changes in caudal fin induced by water flow. J. Fish Biol. 61(5): 1171-1181. doi:10.1111/j.1095-8649. 2002.tb02463.x.
40. Keeley, E.R., Parkinson, E.A., and Taylor, E.B. 2007. The origins of ecotypic variation of rainbow trout: a test of environmental vs. genetically based differences in morphology. J. Evol. Biol. 20(2): 725-736. doi:10.1111/j.1420-9101.2006.01240.x. PMID: 17305838.
41. Lindsey, C.C. 1975. Proglacial lakes and fish dispersal in the south-western Yukon. Verh. Internat. Verein. Limnol. 19: 2364-2370.
42. Magnan, P., Audet, C., Glemet, H., Legault, M., Rodriguez, A., and Taylor, E.B. 2002. Developments in the ecology, evolution, and behaviour of the charrs, genus Salvelinus: relevance for their management and conservation. Environ. Biol. Fishes, 64(1/3): 9-14. doi:10.1023/A:1016010903489.
43. Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Res. 27(2): 209-220. PMID: 6018555.
44. Mathieu, E., Autern, M., Roux, M., and Bonhomme, F. 1990. Épreves de validation dans l'analyze de structures génétiques multivariées: comment tester l'équilibre panmictique? Rev. Stat. Appl. 38: 47-66.
45. McKay, J.K., and Latta, R.G. 2002. Adaptive population divergence: markers, QTL and traits. Trends Ecol. Evol. 17(6): 285-291. doi:10.1016/S0169-5347(02)02478-3.
46. McPhail, J.D. 2007. The freshwater fishes of British Columbia. The University of Alberta Press, Edmonton, Alberta.
47. Millar, R.B. 1987. Maximum likelihood estimation of mixed stock fishery composition. Can. J. Fish. Aquat. Sci. 44(3): 583-590. doi:10.1139/f87-071.
48. Miller, M.P. 1997. Tools for population genetic analysis (TFPGA) 1.3: a Windows program for the analysis of allozyme and molecular population genetic data. Computer software distributed by author (http://www.marksgeneticsoftware.net/tfpga.htm).
49. Miller, C.T., Beleza, S., Pollen, A.A., Schluter, D., Kittles, R.A., Shriver, M.D., and Kingsley, D.M. 2007. cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell, 131(6): 1179-1189. doi:10. 1016/j.cell.2007.10.055. PMID:18083106.
50. Moore, S.A., and Bronte, C.R. 2001. Delineation of sympatric morphotypes of lake trout in Lake Superior. Trans. Am. Fish. Soc. 130(6): 1233-1240. doi:10.1577/1548-8659(2001)130<1233:DOSMOL>2.0. CO;2.
51. Northrup, S. 2008. Population structure of lake trout (Salvelinus namaycush) in Atlin Lake, British Columbia, and contributions to local fisheries: a microsatellite DNA-based assessment. M.Sc. thesis, Department of Zoology, University of British Columbia, Vancouver, British Columbia.
52. Page, K.S., Scribner, K.T., Bennett, K.R., Garzel, L.M., and Burnham-Curtis, M.K. 2003. Genetic assessment of strain-specific sources of lake trout recruitment in the Great Lakes. Trans. Am. Fish. Soc. 132(5): 877-894. doi:10.1577/T02-092.
53. Page, K.S., Scribner, K.T., and Burnham-Curtis, M.K. 2004. Genetic diversity of wild and hatchery lake trout populations: relevance for management and restoration in the Great Lakes. Trans. Am. Fish. Soc. 133(3): 674-691. doi:10.1577/T03-007.1.
54. Pakkasmaa, S., and Piironen, J. 2001. Water velocity shapes juvenile salmonids. Evol. Ecol. 14(8): 721-730. doi:10.1023/A:1011691810801.
55. Perkins, D.L., Fitzsimons, J.D., Marsden, J.E., Krueger, C.C., and May, B. 1995. Differences in reproduction among hatchery strains of lake trout at eight spawning areas in Lake Ontario: genetic evidence from mixed-stock analysis. J. Great Lakes Res. 21: 364-374. doi:10.1016/S0380-1330(95)71110-8.
56. Piller, K., Wilson, C.C., Lee, C.E., and Lyons, J. 2005. Conservation genetics of inland lake trout in the upper Mississippi River basin: stocked or native ancestry? Trans. Am. Fish. Soc. 134(4): 789-802. doi:10.1577/T04-040.1.
57. Power, G. 2002. Charrs, glaciations and seasonal ice. Environ. Biol. Fishes, 64(1/3): 17-35. doi:10.1023/A:1016066519418.
58. Pritchard, J.K., Stephens, M., and Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics, 155(2): 945-959. PMID:10835412.
59. R Development Core Team. 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.R-project.org.
60. Rannala, B., and Mountain, J.L. 1997. Detecting immigration by using multilocus genotypes. Proc. Natl. Acad. Sci. U.S.A. 94(17): 9197-9201. doi:10.1073/pnas.94.17.9197. PMID: 9256459.
61. Raymond, M., and Rousset, F. 1995. Genepop (version 1.2), population genetics software for exact tests and ecumenicism. J. Hered. 86: 248-249.
62. Reusch, T.B.H., Ehlers, A., Hämmerli, A., and Worm, B. 2005. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc. Natl. Acad. Sci. U.S.A. 102(8): 2826-2831. doi:10.1073/pnas.0500008102. PMID:15710890.
63. Rice, W.R. 1989. Analyzing tables of statistical tests. Evolution, 43(1): 223-225. doi:10.2307/2409177.
64. Rohlf, F.J. 1997. TPSDIG and TPSRELW programs. Available from http://life.bio.sunysb.edu/morph.
65. Saint-Laurent, R., Legault, M., and Bernatchez, L. 2003. Divergent selection maintains adaptive differentiation despite high gene flow between sympatric rainbow smelt ecotypes (Osmerus mordax Mitchill). Mol. Ecol. 12(2): 315-330. doi:10.1046/j.1365-294X.2003.01735.x. PMID:12535084.
66. Schwartz, M.K., Luikart, G., and Waples, R.S. 2007. Genetic monitoring as a promising tool for conservation and management. Trends Ecol. Evol. 22(1): 25-33. doi:10.1016/j.tree.2006.08.009. PMID:16962204.
67. Scott, W.B., and Crossman, E.J. 1998. Freshwater fishes of Canada. Galt House Publications, Ltd., Oakville, Ontario, Canada.
68. Slatkin, M. 1993. Isolation by distance in equilibrium and non-equilibrium populations. Evolution, 47(1): 264-279. doi:10. 2307/2410134.
69. Smith, B.R., and Tibbles, J.J. 1980. Sea lamprey (Petromyzon marinus) in Lakes Huron, Michigan, and Superior: history of invasion and control, 1936-78. Can. J. Fish. Aquat. Sci. 37(11): 1780-1801. doi:10.1139/f80-222.
70. Stamford, M.D., and Taylor, E.B. 2004. Phylogeographical lineages of Arctic grayling (Thymallus arcticus) in North America: divergence, origins, and affinities with Eurasian Thymallus. Mol. Ecol. 13: 1533-1549. doi:10.1111/j.1365-294X.2004.02174.x.PMID:15140096.
71. Stevens, M., and Merilaita, S. 2009. Animal camouflage: current issues and new perspectives. Philos. Trans. R. Soc. B Biol. Sci., 364(1516): 423-427. doi:10.1098/rstb.2008.0217.
72. Stuart-Fox, D., and Moussalli, A. 2009. Camouflage, communication and thermal regulation: lessons from colour-changing organisms. Philos. Trans. R. Soc. B Biol. Sci., 364(1516): 463-470. doi:10.1098/rstb.2008.0254.
73. Taylor, E.B., Tamkee, P., Sterling, G., and Hughson, W. 2007. Microsatellite DNA analysis of rainbow trout (Oncorhynchus my-kiss) from western Alberta, Canada: native status and evolutionary distinctiveness of "Athabasca" rainbow trout. Conserv. Genet. 8(1): 1-15. doi:10.1007/s10592-006-9142-9.
74. Thorpe, R.S. 1976. Biometric analysis of geographic variation and racial affinities. Biol. Rev. Camb. Philos. Soc. 51(4): 407-425. doi:10.1111/j.1469-185X.1976.tb01063.x. PMID:1088084.
75. Waples, R.S., and Gaggiotti, O. 2006. What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol. Ecol. 15(6): 1419-1439. doi:10.1111/j.1365-294X.2006.02890.x. PMID:16629801.
76. Waters, J.M., and Wallis, G.P. 2000. Across the Southern Alps by river capture? Freshwater fish phylogeography in South Island, New Zealand. Mol. Ecol. 9(10): 1577-1582. doi:10.1046/j.1365-294x.2000.01035.x. PMID:11050552.
77. Weir, B.S., and Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38(6): 1358-1370. doi:10.2307/2408641.
78. Whitlock, M.C. 2003. Fixation probability and time in subdivided populations. Genetics, 164(2): 767-779. PMID:12807795.
79. Whitlock, M.C., and Barton, N.H. 1997. The effective size of a subdivided population. Genetics, 126: 427-441.
80. Wilson, C.C., and Hebert, P.D.N. 1998. Phylogeography and postglacial dispersal of lake trout (Salvelinus namaycush) in North America. Can. J. Fish. Aquat. Sci. 55(4): 1010-1024. doi:10. 1139/cjfas-55-4-1010.
81. Wilson, C.C., and Mandrak, N.E. 2003. History and evolution of lake trout in shield lakes: past and future challenges In Boreal shield watersheds: lake trout ecosystems in a changing environment. Edited by J.M. Gunn, R.J. Steedman, and R.A. Ryder. CRC Press, Boca Raton, Florida. pp. 21-33.
82. Zemlak, T.S., Habit, E.M., Walde, S.J., Battini, M.A., Adams, E.D., and Ruzzante, D.E. 2008. Across the southern Andes on fin: glacial refugia, drainage reversals and a secondary contact zone revealed by the phylogeographical signal of Galaxias platei in Patagonia. Mol. Ecol. 17(23): 5049-5061. doi:10.1111/j. 1365-294X.2008.03987.x. PMID:19017262.
83. Zimmerman, M.S., Krueger, C.C., and Eshenroder, R.L. 2006. Phenotypic diversity of lake trout in Great Slave Lake: differences in morphology, buoyancy, and habitat depth. Trans. Am. Fish. Soc. 135(4): 1056-1067. doi:10.1577/T05-237.1.
84. Zimmerman, M.S., Krueger, C.C., and Eshenroder, R.L. 2007. Morphological and ecological differences between shallow and deep-water lake trout in Lake Mistassini, Quebec. J. Great Lakes Res. 33(1): 156-169. doi:10.3394/0380-1330(2007)33[156:MAEDBS]2. 0.CO;2.