Genetic structure of lake whitefish (Coregonus clupeaformis) in Lake Michigan

Canadian Journal of Fisheries and Aquatic Sciences

Volumn 66, Issue 3, 2009, Pages 382-393

  VanDeHey, Justin A ^a,b   Sloss, Brian L ^a   Peeters, Paul J ^c   Sutton, Trent M ^d  

^a UNIVERSITY OF WISCONSIN STEVENS POINT   (United States)

^b SOUTH DAKOTA STATE UNIVERSITY   (United States)

^c WISCONSIN DEPARTMENT OF NATURAL RESOURCES   (United States)

^d UNIVERSITY OF ALASKA FAIRBANKS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BAYESIAN ANALYSIS; CLUPEOID; DIVERGENCE; FISHERY ECONOMICS; GENE FLOW; GENETIC MARKER; GENETIC STRUCTURE; SPAWNING; STOCK ASSESSMENT; STOCK IDENTIFICATION;

GREAT LAKES [NORTH AMERICA]; HOG ISLAND; LAKE MICHIGAN; NORTH AMERICA; UNITED STATES; VIRGINIA;

COREGONUS CLUPEAFORMIS; SUIDAE;

EID: 65249118971     PISSN: 0706652X     EISSN: None     Source Type: Journal    
DOI: 10.1139/F08-213     Document Type: Article

References (73)

1. Bailey, R.M., and Smith, G.R. 1981. Origin and geography of the fish fauna of the Laurentian Great Lakes basin. Can. J. Fish. Aquat. Sci. 38: 1539-1561. doi:10.1139/f81-206.
2. Bernard, A. 2006. Cryptic structure and diversity of lake whitefish (Coregonus clupeaformis) in Ontario waters. M.Sc. thesis, University of Guelph, Guelph, Ont., Canada.
3. Bernatchez, L., and Dodson, J.J. 1991. Phylogeographic structure in mitochondrial DNA of the lake whitefish (Coregonus clupeaformis) in North America and its relationship to Pleistocene glaciations. Evolution, 45: 1016-1035. doi:10.2307/2409706.
4. Bodaly, R.A., Clayton, J.W., Lindsey, C.C., and Vuorinen, J. 1992. Evolution of lake whitefish (Coregonus clupeaformis) in North America during the Pleistocene: genetic differentiation between sympatric populations. Can. J. Fish. Aquat. Sci. 49: 769-779. doi:10.1139/f92-086.
5. Booke, H.E. 1981. The conundrum of the stock concept - are nature and nurture definable in fishery science? Can. J. Fish. Aquat. Sci. 38: 1479-1480. doi:10.1139/f81-200.
6. Burger, C.V., Spearman, W.J., and Cronin, M. 1997. Genetic differentiation of sockeye salmon subpopulations from a geologically young Alaskan lake system. Trans. Am. Fish. Soc. 126: 926-938. doi:10.1577/1548-8659(1997)126<0926:GDOSSS>2.3.CO;2.
7. Casselman, J.M., Collins, J.J., Crossman, E.J., Ihssen, P.E., and Spangler, G.R. 1981. Lake whitefish (Coregonus clupeaformis) stocks of the Ontario waters of Lake Huron. Can. J. Fish. Aquat. Sci. 38: 1772-1789. doi:10.1139/f81-225.
8. Cavalli-Sforza, L.L., and Edwards, A.W.F. 1967. Phylogenetic analysis: models and estimation procedures. Evolution, 21: 550-570. doi:10.2307/2406616.
9. Chouinard, A., and Bernatchez, L. 1998. A study of trophic niche partitioning between larval populations of reproductively isolated whitefish (Coregonus sp.) ecotypes. J. Fish Biol. 53: 1231-1242.
10. Corander, J., Marttinen, P., and Mäntyniemi, S. 2006. Bayesian identification of stock mixtures from molecular marker data. Fish. Bull. (Washington, D.C.), 104: 550-558.
11. Douglas, M.P., Brunner, P.C., and Bernatchez, L. 1999. Do assemblages of Coregonus (Teleostei: Salmoniformes) in the Central Alpine region of Europe represent species flocks? Mol. Ecol. 8: 589-603. doi:10.1046/j.1365-294x.1999.00581.x.
12. Duftner, N., Sefc, K.M., Koblmüller, S., Nevado, B., Verheyen, E., Phiri, H., and Sturmbauer, C. 2006. Distinct population structure in a phenotypically homogeneous rock-dwelling cichlid fish from Lake Tanganyika. Mol. Ecol. 15: 2381-2395. doi:10.1111/ j.1365-294X.2006.02949.x. PMID:16842413.
13. Ebener, M.P., and Copes, F.A. 1985. Population statistics, yield estimates, and management considerations for two lake whitefish stocks in Lake Michigan. N. Am. J. Fish. Manage. 5: 435-448. doi:10.1577/1548-8659(1985) 5<435:PSYEAM>2.0.CO;2.
14. 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: 2611-2620. doi:10.1111/j. 1365-294X.2005.02553.x. PMID:15969739.
15. 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: 479-491. PMID:1644282.
16. 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.
17. Felsenstein, J. 1993. Phylogeny inference package (PHYLIP). Ver. 3.5. University of Washington, Seattle, Washington.
18. Goudet, J. 1995. Fstat version 1.2: a computer program to calculate F-statistics. J. Hered. 86: 485-486.
19. Guo, S.W., and Thompson, E.A. 1992. Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics, 48: 361-372. doi:10.2307/2532296. PMID:1637966.
20. Hedrick, P.W. 2000. Genetics of populations. Jones and Bartlett Publishers, Boston, Mass.
21. Helland, I.P., Freyhof, J., Kasprzak, P., and Mehner, T. 2007. Temperature sensitivity of vertical distributions of zooplankton and planktivorous fish in a stratified lake. Oecologia, 151: 322-330. doi:10.1007/s00442-006-0541-x. PMID:17024386.
22. Henegariu, O., Heerema, N.A., Dlouhy, S.R., Vance, G.H., and Vogt, P.H. 1997. Multiplex PCR: critical parameters and stepby- step protocol. BioTechniques, 23: 504-511. PMID:9298224.
23. Imhoff, M.A. 1977. Population genetic structure of lake whitefish, Coregonus clupeaformis, in Green Bay and northern Lake Michigan, as assessed by electrophoresis of lactate, glycerol-3- phosphate, and malate dehydrogenase isozymes. M.Sc. thesis, College of Natural Resources, University of Wisconsin - Stevens Point, Stevens Point, Wisc.
24. Imhoff, M.A., Leary, R.F., and Booke, H.E. 1980. Population or stock structure of lake whitefish (Coregonus clupeaformis) in northern Lake Michigan as assessed by isozyme electrophoresis. Can. J. Fish. Aquat. Sci. 37: 783-793. doi:10.1139/f80-105.
25. Jensen, J.L., Bohonak, A.J., and Kelley, S.T. 2005. Isolation by distance, web service. Ver. 3.14. BMC Genetics, 6: 13. Available from ibdws.sdsu.edu/.
26. Jones, M.L., Arts, M.T., Faisal, M., Ebener, M.P., Wagner, T., Brenden, T.O., Honeyfield, D., and Wright, G. 2008. Magnitude and potential causes of mortality in four lake whitefish populations in Lakes Michigan and Huron: a multidisciplinary approach. Great Lakes Fishery Trust Project Completion Report, Lansing, Mich. Project No. 2003-06.
27. Kalinowski, S.T. 2005. HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol. Ecol. 5: 187-189. doi:10.1111/j.1471-8286.2004.00845.x.
28. Kimura, M., and Weiss, G.H. 1964. The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics, 49: 561-576. PMID:17248204.
29. Kinnunen, R.E. 2003. Great Lakes Commercial Fisheries. Great Lakes Fisheries Leadership Institute Technology Report. Available from www.miseagrant.umich.edu/downloads/fisheries/ GLCommercialFinal.pdf [accessed 10 August 2005].
30. Latch, E.K., Dharmarajan, G., Glaubitz, J.C., and Rhodes, O.E. 2006. Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conserv. Genet. 7: 295-302. doi:10.1007/s10592-005-9098- 1.
31. Leary, R. 1979. Population or stock structure of lake whitefish, Coregonus clupeaformis, in northern Lake Michigan as assessed by isozyme electrophoresis. M.Sc. thesis, College of Natural Resources, University of Wisconsin - Stevens Point, Stevens Point, Wisc.
32. Leberg, P.L. 2002. Estimating allelic richness: effects of sample size and bottlenecks. Mol. Ecol. 11: 2445-2449. doi:10.1046/j. 1365-294X.2002.01612.x. PMID:12406254.
33. Liu, K., and Muse, S.V. 2005. PowerMarker: integrated analysis environment for genetic marker data. Bioinformatics (Oxford), 21: 2128-2129. doi:10.1093/bioinformatics/bti282.
34. Lu, G., and Bernatchez, L. 1999. Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes (Coregonus clupeaformis): support for the ecological speciation hypothesis. Evolution, 53: 1491-1505. doi:10.2307/2640895.
35. Lu, G., Basley, D.J., and Bernatchez, L. 2001. Contrasting patterns of mitochondrial DNA and microsatellite introgressive hybridization between lineages of lake whitefish (Coregonus clupeaformis): relevance for speciation. Mol. Ecol. 10: 965-985. doi:10. 1046/j.1365-294X.2001.01252. x. PMID:11348504.
36. Mantel, N. 1967. The detection of disease clustering and generalized regression approach. Cancer Res. 27: 209-220. PMID:6018555.
37. Markert, J.A., Arnegard, M.E., Danley, P.D., and Kocher, T.D. 1999. Biogeography and population genetics of the Lake Malawi cichlid Melanochromis auratus: habitat transience, philopatry and speciation. Mol. Ecol. 8: 1013-1026. doi:10.1046/j.1365-294x.1999.00658.x.
38. Miller, C.R., Joyce, P., and Waits, L.P. 2002. Assessing allelic dropout and genotype reliability using maximum likelihood. Genetics, 160: 357-366. PMID:11805071.
39. Moritz, C. 1994. Defining 'evolutionarily significant units' for conservation. Trends Ecol. Evol. 9: 373-375. doi:10.1016/0169-5347(94) 90057-4.
40. National Oceanic and Atmospheric Administration. 2007. Bathymetry of Lake Michigan. Available from www.ngdc.noaa.gov/ mgg/greatlakes/lakemich-cdrom/ images/area7hi.gif [accessed 10 March 2007].
41. Navidi, W., Arnheim, N., and Waterman, M.S. 1992. A multipletubes approach for accurate genotyping of very small DNA sam- ples by using PCR: statistical considerations. Am. J. Hum. Genet. 50: 347-359. PMID:1734715.
42. Østbye, K., Næsje, T.F., Bernatchez, L., Sandlund, O.T., and Hindar, K. 2005. Morphological divergence and origin of sympatric populations of European whitefish (Coregonus lavaretus L.) in Lake Femund, Norway. J. Evol. Biol. 18: 683-702. doi:10. 1111/j.1420-9101.2004.00844.x. PMID:15842498.
43. Østbye, K., Amundsen, P.A., Bernatchez, L., Klemetsen, A., Knudsen, R., Kristoffersen, Næsje, T.F., and Hindar, K. 2006. Parallel evolution of ecomorphological traits in the European whitefish Coregonus lavaretus (L.) species complex during postglacial times. Mol. Ecol. 15: 3983-4001. doi:10.1111/j.1365-294X. 2006.03062.x.
44. Page, R.D.M. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comp. Appl. Biosci. 12: 357-358. PMID:8902363.
45. Pamilo, P., and Varvio-Aho, S. 1984. Testing genotype frequencies and heterozygosities. Mar. Biol. (Berl.), 79: 99-100. doi:10. 1007/BF00404990.
46. Parker, H.H., Noonburg, E.G., and Nisbet, R.M. 2001. Models of alternative life-history strategies, population structure and potential speciation in salmonid fish stocks. J. Anim. Ecol. 70: 260-272. doi:10.1046/j.1365-2656.2001.00488.x.
47. Patton, J.C., Gallaway, B.J., Fechhelm, R.G., and Cronin, M.A. 1997. Genetic variation of microsatellite and mitochondrial DNA genetic markers in broad whitefish (Coregonus nasus) in the Colville and Sagavanirktok rivers in northern Alaska. Can. J. Fish. Aquat. Sci. 54: 1548-1556. doi:10.1139/cjfas-54-7-1548.
48. Petit, R., El Mousadik, A., and Pons, O. 1998. Identifying populations for conservation on the basis of genetic markers. Conserv. Biol. 12: 844-855. doi:10.1046/j.1523-1739.1998.96489.x.
49. Planes, S., and Fauvelot, C. 2002. Isolation by distance and vicariance drive genetic structure of a coral reef fish in the Pacific Ocean. Evolution, 56: 378-399. PMID:11926506.
50. Pogson, G.H., Taggart, C.T., Mesa, K.A., and Boutillier, R.G. 2001. Isolation by distance in the Atlantic cod, Gadus morhua, at large and small geographic scales. Evolution, 55: 131-146. PMID:11263734.
51. Pritchard, J.K., Stephens, P., and Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics, 155: 945-959. PMID:10835412.
52. Pritchard, J.K., Wen, X., and Falush, D. 2007. Documentation for structure software. Ver. 2.2. Available from pritch.bsd.uchicago. edu/software [accessed 15 July 2008].
53. Raymond, M., and Rousset, F. 1995. An exact test for differentiation. Evolution, 49: 1280-1283. doi:10.2307/2410454.
54. Rice, W.R. 1989. Analyzing tables of statistical tests. Evolution, 43: 223-225. doi:10.2307/2409177.
55. Rogers, S.M., Marchand, M.H., and Bernatchez, L. 2004. Isolation, characterization and cross-salmonid amplification of 31 microsatellite loci in the lake whitefish (Coregonus clupeaformis, Mitchill). Mol. Ecol. 4: 89-92. doi:10.1046/j.1471-8286.2003.00578. x.
56. Rowe, M. 1984. Population dynamics of lake whitefish in the Big Bay de Noc, Bark and Cedar Rivers, and Portage Bay areas of Lake Michigan. M.Sc. thesis, College of Natural Resources, University of Wisconsin - Stevens Point, Stevens Point, Wisc. Saitou, N., and Nei, M. 1987. The neighbor-joining method: a method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425. PMID:3447015.
57. Scheerer, P.D., and Taylor, W.W. 1985. Population dynamics and stock differentiation of lake whitefish in northeastern Lake Michigan with implications for their management. N. Am. J. Fish. Manage. 5: 526-536. doi:10.1577/1548-8659(1985)5<526: PDASDO>2.0.CO;2.
58. Schneeberger, P.J., Ebener, M.P., Toneys, M., and Peeters, P.J. 2005. Status of lake whitefish in Lake Michigan. Gt. Lakes Fish. Comm. Tech. Rep. 66: 67-86.
59. Schwartz, M.K., and McKelvey, K.S. 2008. Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv. Genet. doi:10.1007/s10592-008-9622-1.
60. Shaklee, J.B., and Currens, K.P. 2003. Genetic stock identification and risk assessment. In Population genetics: principles and applications for fisheries scientists. Edited by E.M. Hallerman. American Fisheries Society, Bethesda, Md. pp. 291-328.
61. Stepien, C.A., and Faber, J.E. 1998. Population genetic structure, phylogeography and spawning philopatry in walleye (Stizostedion vitreum) from mitochondrial DNA control region sequences. Mol. Ecol. 7: 1757-1769. doi:10.1046/j.1365-294x. 1998.00512.x. PMID:9859203.
62. Stott, W., Todd, T.N., and Kallemeyn, L. 2004. Genetic variability among lake whitefish from Isle Royale and the upper Great Lakes. Ann. Zool. Fenn. 41: 51-59.
63. Turgeon, J., and Bernatchez, L. 2001. Clinal variation at microsatellite loci reveals historical secondary intergradation between glacial races of Coregonus artedi (Teleostei: Coregoninae). Evolution, 55: 2274-2286. PMID:11794787.
64. Turgeon, J., Estoup, A., and Bernatchez, L. 1999. Species flock in the North American Great Lakes: molecular ecology of Lake Nipigon ciscoes (Teleostei: Coregonidae: Coregonus). Evolution, 53: 1857-1871. doi:10.2307/2640446.
65. Utter, F., and Ryman, N. 1993. Genetic markers and mixed stock fisheries. Fisheries, 18: 11-21. doi:10.1577/1548-8446(1993) 018<0011: GMAMSF>2.0.CO;2.
66. Van Den Avyle, M.J. 1993. Dynamics of exploited fish populations. In Inland fisheries management in North America. Edited by C.C. Kohler and W.A. Hubert. American Fisheries Society, Bethesda, Md. pp. 105-134.
67. Walker, S.H., Prout, M.W., Taylor, W.W., and Winterstein, S.R. 1993. Population dynamics and management of lake whitefish stocks in Grand Traverse Bay, Lake Michigan. N. Am. J. Fish. Manage. 13: 73-85. doi:10.1577/1548-8675(1993)013<0073: PDAMOL>2.3.CO;2.
68. 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: 1419-1439. doi:10.1111/j.1365-294X.2006.02890.x. PMID:16629801.
69. Waples, R.S., Teel, D.J., Myers, J.M., and Marshall, A.R. 2004. Life-history divergence in chinook salmon: historic contingency and parallel evolution. Evolution, 58: 386-403. doi:10.1554/03-323. PMID:15068355.
70. Weir, B.S., and Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38: 1358-1370. doi:10.2307/2408641.
71. Wilmot, R.L., and Burger, C.V. 1985. Genetic differences among populations of Alaskan sockeye salmon. Trans. Am. Fish. Soc. 114: 236-243. doi:10.1577/1548-8659(1985)114<236:GDAPOA>2.0. CO;2.
72. Wright, S. 1931. Evolution in Mendelian populations. Genetics, 16: 97-159. PMID:17246615.
73. Wright, S. 1943. Isolation by distance. Genetics, 28: 114-138. PMID:17247074.