Signatures of vicariance, postglacial dispersal and spawning philopatry: Population genetics of the walleye Sander vitreus

Molecular Ecology

Volumn 18, Issue 16, 2009, Pages 3411-3428

  Stepien, C A ^a   Murphy, D J ^a   Lohner, R N ^a   Sepulveda Villet, O J ^a   Haponski, A E ^a  

^a UNIVERSITY OF TOLEDO   (United States)

Author keywords

Glacial refugia; Great Lakes; Natal homing; Percidae; Population genetics; Sander vitreus; Walleye

Indexed keywords

MICROSATELLITE DNA;

ANIMAL; ARTICLE; DNA SEQUENCE; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; PERCH; PHYLOGENY; POPULATION GENETICS; UNITED STATES;

ANIMALS; GENETIC VARIATION; GENETICS, POPULATION; GEOGRAPHY; GREAT LAKES REGION; MICROSATELLITE REPEATS; PERCHES; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

ANIMALIA; PERCIDAE; SANDER VITREUS; STIZOSTEDION VITREUM;

EID: 68349125472     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2009.04291.x     Document Type: Article

References (109)

1. Avise JC (2004) Molecular Markers, Natural History, and Evolution, Second edn. Sinauer Assoc., Sunderland, Massachusetts, USA.
2. Bailey RM, Smith GR (1981) Origin and geography of fish fauna of the Laurentian Great Lakes basin. Canadian Journal of Fisheries and Aquatic Sciences, 38, 1539 1561.
3. Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Molecular Ecology, 11, 155 165.
4. Bernatchez L, Wilson CC (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Molecular Ecology, 7, 431 452.
5. Billington N, Hebert PDN (1988) Mitochondrial DNA variation in Great Lakes walleye (Stizostedion vitreum) populations. Canadian Journal of Fisheries and Aquatic Sciences, 45, 643 654.
6. Billington N, Maceina MJ (1997) Genetic and population characteristics of walleyes in the Mobile drainage of Alabama. Transactions of the American Fisheries Society, 126, 804 814.
7. Billington N, Strange RM (1995) Mitochondrial DNA analysis confirms the existence of a genetically divergent walleye population in northeastern Mississippi. Transactions of the American Fisheries Society, 124, 770 776.
8. Billington N, Barrette RJ, Hebert PDN (1992) Management implications of mitochondrial DNA variation in walleye stocks. North American Journal of Fishery Management, 12, 276 284.
9. Bolsenga SJ, Herdendorf CE (1993) Lake Erie and Lake St. Clair Handbook. Wayne State University Press, Detroit, Michigan, USA.
10. Borer S, Miller LM, Kapuscinski AR (1999) Microsatellites in walleye Stizostedion vitreum. Molecular Ecology, 8, 336 338.
11. Boschung HT Jr., Mayden RL (2004) Fishes of Alabama. Smithsonian Institution, Washington D.C., USA.
12. Burridge CP, Craw D, Jack DC, King TM, Waters JM (2008) Does fish ecology predict dispersal across a river drainage divide? Evolution, 62, 1484 1499.
13. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics, 19, 233 257.
14. Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution., 24, 621 631.
15. Colby PJ, Nepszy SJ (1981) Variation among stocks of walleye (Stizostedion vitreum): management implications. Canadian Journal of Fisheries and Aquatic Sciences, 38, 1814 1831.
16. Colby PJ, Lewis CA, Eschenroder RL, Haas RC, Hushak LJ (1994) Walleye-rehabilitation guidelines for the Great Lakes area. Great Lakes Fishery Commission Technical Report. Great Lakes Fishery Commission, Ann Arbor, Michigan, USA.
17. Diniz-Filho JAF, de Campos Telles MP, Bonatto SL, Eizirik E et al. (2008) Mapping the evolutionary twilight zone: Molecular markers, populations and geography. Journal of Biogeography, 35, 753 763.
18. Dupont PP, Bourret V, Bernatchez L (2007) Interplay between ecological, behavioural and historical factors in shaping the genetic structure of sympatric walleye populations (Sander vitreus). Molecular Ecology, 16, 937 951.
19. Eldridge WH, Bacigalupi MD, Adelman IR, Miller LM et al. (2002) Determination of relative survival of two stocked walleye populations and resident natural-origin fish by microsatellite DNA parentage assignment. Canadian Journal of Fisheries and Aquatic Sciences, 59, 282 290.
20. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Molecular Ecology, 14, 2611 2620.
21. Excoffier L (2007) Arlequin ver. 3.11. http://cmpg.unibe.ch/software/ arlequin3. Last accessed 1 June 2009.
22. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric Distances among DNA haplotypes: application to human mitochondrial DNA data. Genetics, 131, 479 491.
23. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47 50.
24. Faber JE, Stepien CA (1997) The utility of mitochondrial DNA control region sequences for analyzing phylogenetic relationships among populations, species, and genera of the Percidae. In : Molecular Systematics of Fishes (eds Kocher TD, Stepien CA). pp. 129 143, Academic Press, San Diego, CA.
25. Faber JE, Stepien CA (1998) Tandemly repeated sequences in the mitochondrial DNA control region and phylogeography of the pike-perches Stizostedion. Molecular Phylogenetics and Evolution, 10, 310 323.
26. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783 791.
27. Felsenstein J (2008) PHYLIP (Phylogeny Interference Package), ver. 3.68. Distributed by the author, University of Washington, Seattle, Washington, USA. http://evolution.genetics.washington.edu/phylip.html. Last accessed 1 June 2009.
28. Ferguson RG, Derkson AJ (1971) Migrations of adult and juvenile walleyes (Stizostedion vitreum vitreum) in southern Lake Huron, Lake St. Clair, Lake Erie, and connecting waters. Journal of the Fisheries Research Board of Canada, 28, 1133 1142.
29. Fielder DG (2002) Sources of walleye recruitment in Saginaw Bay, Lake Huron. North American Journal of Fisheries Management, 22, 1032 1040.
30. Fielder DG, Liskauskas A, Mohr LC, Boase J (2008) Nearshore fish community. In : The State of Lake Huron 2004 (eds Bence JR, Mohr LC). Fishery Commission Special Publication 08-01, Ann Arbor, Michigan, USA. http://www.glfc.org/pubs/SpecialPubs/Sp08-1.pdf.
31. Flint RF (1971) Glacial and Quaternary Geology. John Wiley & Sons, New York, New York, USA.
32. Ford AM, Stepien CA (2004) Genetic variation and spawning population structure in Lake Erie yellow perch, Perca flavescens: a comparison with a Maine population. In : Proceedings of Percis III: The 3rd International Symposium on Percid Fishes (eds Barry TP, Malison JA). pp. 131 132, University of Wisconsin Sea Grant Institute, Madison, Wisconsin, USA.
33. Gerlach G, Schardt U, Eckmann R, Meyer A (2001) Kin-structured subpopulations in Eurasian perch (Perca fluviatilis L.). Heredity, 86, 213 221.
34. Goodyear CS, Edsall TA, Dempsey DM, Moss GD et al. (1982) Atlas of the Spawning and Nursery Areas of Great Lakes Fishes. U. S. Fish and Wildlife Service, Washington, D.C., USA. FWS/OBS-82/52.
35. Goudet J (1995) FSTAT, Version 1.2, A computer program to calculate F-statistics. Journal of Heredity, 86, 485 486.
36. Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices, ver. 2.9.3.2. http://www2.unil.ch/popgen/softwares/fstat. htm. Last accessed 1 June 2009.
37. Goudet J, Raymond M, de Meeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics, 144, 1933 1940.
38. Grzybowski M, Sepulveda-Villet OJ, Stepien CA, Daniel Rosauer D et al. (2009) Genetic variation of 17 wild yellow perch populations from the midwest and east coastal United States using microsatellites. Transactions of the American Fisheries Society, 138, In press.
39. Guillot G, Estoup A, Mortier F, Cosson JF (2005a) A spatial statistical model for landscape genetics. Genetics, 170, 1261 1280.
40. Guillot G, Mortier F, Estoup A (2005b) GENELAND: a computer package for landscape genetics. Molecular Ecology Notes, 5, 708 711.
41. Guillot G, Santos F, Estoup A (2008) Analysing georeferenced population genetics data with GENELAND: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics, 24, 1406 1407. Ver. 2.3.41 http://folk.uio.no/gillesg/Geneland/geneland.html. Last accessed 1 June 2009.
42. Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics, 48, 361 372.
43. Hackney PA, Holbrook JA II. (1978) Sauger, walleye, and yellow perch in the southeastern United States. American Fisheries Society Special Publication, 11, 74 81.
44. Haponski AE, Stepien CA (2008) Molecular, morphological, and biogeographic resolution of cryptic taxa in the greenside darter Etheostoma blennioides complex. Molecular Phylogenetics and Evolution, 49, 69 83.
45. Haponski AE, Bollin T, Jedlicka M, Stepien CA (2009) Landscape genetic patterns of the rainbow darter: a watershed analysis of mitochondrial DNA sequences and nuclear microsatellites. Journal of Fish Biology, 74, In Press.
46. Hedrick PW (2005) Genetics of Populations, 3rd edn. Jones & Bartlet Publishers, Boston, Massachusetts, USA.
47. Hocutt CH, Jenkins RE, Stauffer JR Jr. (1986) Zoogeography of the fishes of the central Appalachians and central Atlantic coastal plain In : The Zoogeography of North American Freshwater Fishes (ed. Hocutt CH, Wiley EO) pp. 161 211, John Willey & Sons, Inc, New York, New York, USA
48. Horrall RM (1981) Behavioral stock-isolating mechanisms in Great Lakes fishes with special reference to homing and site imprinting. Canadian Journal of Fisheries and Aquatic Sciences, 38, 1481 1496.
49. Hudson RR (1998) Island models and the coalescent process Molecular Ecology, 7, 413 418
50. Irwin DE (2002) Phylogeographic breaks without geographic barriers to gene flow Evolution, 53, 2382 2394
51. Jennings MJ, Claussen JE, Philipp DP (1996) Evidence for heritable preferences for spawning habitat between two walleye groups Transactions of the American Fisheries Society, 125, 978 982
52. Koed A, Mejlhelde P, Balleby K, Aarestrup K (2000) Annual movement of adult pikeperch in a lowland river Journal of Fish Biology, 57, 1266 1279
53. Koed A, Balleby K, Mejlhelde P (2002) Migratory behavior of adult pikeperch (Stizostedion lucioperca) in a lowland river Hydrobiologia, 483, 175 184
54. Larson G, Schaetzl R (2001) Origin and evolution of the Great Lakes Journal of Great Lakes Research, 27, 518 546
55. LeClerc E, Mailhot Y, Mingelbier M, Bernatchez L (2008) The landscape genetics of yellow perch (Perca flavescens) in a large fluvial ecosystem Molecular Ecology, 27, 1702 1717
56. Lewis CF, Moore TC Jr., Rea DK, Dettman DL et al. (1994) Lakes of the Huron basin: their record of runoff from the Laurentide ice sheet Quaternary Sciences Reviews, 13, 891 992
57. Mandrak NE, Crossman EJ (1992) Postglacial dispersal of freshwater fishes into Ontario Canadian Journal of Zoology, 70, 2247 2259
58. Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics Trends in Ecology and Evolution, 18, 189 197
59. Manni FE, Guerard E, Heyer E (2004a) Geographical patterns of (genetic, morphologic, linguistic) variation: How barriers can be detected by "Monmonier's algorithm" Human Biology, 76, 173 190
60. Manni FE, Guerard E, Heyer E (2004b) Barrier 2.2 Museum of Mankind, Paris, France http://www.mnhn.fr/mnhn/ecoanthropolagie/software/barrier.html. Last accessed 1 June 2009.
61. Mantel N (1967) The detection of disease clustering and a generalized regression approach Cancer Research, 27, 209 220
62. Marjoram P, Donelly P (1994) Pairwise comparisons of mitochondrial DNA sequences in subdivided populations and implications for early human evolution Genetics, 136, 673 683
63. Mayden RL (1987) Pleistocene glaciation and historical biogeography of North American central-highland fishes In : Quaternary Environments of Kansas (ed. Johnson WC) pp. 141 151, Kansas Geological Survey, Guidebook Series 5, Lawrence, Kansas, USA
64. Miller L (2003) Microsatellite DNA loci reveal genetic structure of yellow perch in Lake Michigan Canadian Journal of Fisheries and Aquatic Sciences, 132, 503 513
65. Mills E, Forney J, Clady M, Schaffer W (1978) Oneida Lake In : Lakes of New York State, Vol 2 (ed. Bloomfield J et al. pp. 367 452 Academic Press, New York, New York, USA
66. Monmonier MS (1973) Maximum-difference barriers: an alternative numerical regionalization method Geographical Analysis, 3, 245 261
67. Murdoch MH, Hebert PDN (1997) Mitochondrial DNA evidence of distinct glacial refugia for brown bullhead (Ameriurus nebulosus) in the Great Lakes Canadian Journal of Fisheries and Aquatic Sciences, 54, 1450 1460
68. Murphy BR (1990) Evidence for a genetically unique walleye population in the upper Tombigbee River system of northeastern Mississippi Proceedings of the Southeastern Fishes Council, 22, 12 16
69. Olson DE, Scidmore WJ (1962) Homing behavior in spawning walleyes Transactions of the American Fisheries Society, 91, 355 561
70. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data Molecular Ecology Notes, 4, 535 538
71. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2006) MICRO-CHECKER http://wwwmicrocheckerhullacuk.
72. Palmer GC, Murphy BR, Hallerman EM (2005) Movements of walleyes in Claytor Lake and the upper New River, Virginia, indicate distinct lake and river populations North American Journal of Fishery Management, 25, 1448 1455
73. Parker AD, Stepien CA, Sepulveda-Villet OJ, Ruehl CB, Uzarski DJ (2009) The interplay of morphology, ecological habitat, resource use, and population genetics in young yellow perch Transactions of the American Fisheries Society, 138, 899 914.
74. Poissant J, Knight TW, Ferguson MM (2005) Nonequilibrium conditions following landscape rearrangement: the relative contribution of past and current hydrological landscapes on the genetic structure of a stream-dwelling fish Molecular Ecology, 14, 1321 1331
75. Pritchard JK, Wen W (2004) Documentation for Structure Software: Ver 2.2.3 Department of Human Genetics, University of Chicago, Chicago, Illinois, USA http://pritch.bsd.uchicago.edu/structure.html. Last accessed 1 June 2009.
76. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data Genetics, 155, 945 959
77. r Development Core Team (2008) r: A Language and Environment for Statistical Computing r Foundation for Statistical Computing, Vienna http://wwwRproject.org. Last accessed 1 June 2009.
78. Raymond M, Rousset F (1995) An exact test for population differentiation Evolution, 49, 1280 1283
79. Regier HA, Applegate VC, Ryder RA (1969) The ecology and management of the walleye in western Lake Erie Great Lakes Fishery Commission Technical Report, 15, 1 101
80. Rempel LL, Smith DG (1998) Postglacial fish dispersal from the Mississippi refuge to the Mackenzie River basin Canadian Journal of Fisheries and Aquatic Sciences, 55, 893 899
81. Rice WR (1989) Analyzing tables of statistical tests Evolution, 43, 223 225
82. Ricklefs RE (1989) Speciation and diversity: the integration of local and regional processes In : Speciation and Its Consequences (ed. Otte D, Endler JA) pp. 599 622, Sinauer Assoc, Inc, Sunderland, Massachusetts, USA
83. Robison HW (1986) Zoogeographic implications of the Mississippi River Basin In : The Zoogeography of North American Freshwater Fishes (ed. Hocutt CH, Wiley EO) pp. 267 286, John Willey & Sons, Inc, New York, New York, USA
84. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance Genetics, 145, 1219 1228
85. Rousset F (2008) Genepop'007: a complete re-implementation of the genepop software for Windows and Linux Molecular Ecology Resources, 8, 103 106, ver 4.0 http://kimura.univ- montp2.fr/∼rousset/Genepop.htm. Last accessed 1 June 2009.
86. Ryan PA, Knight R, MacGregor R, Towns G et al. (2003) Fish-community goals and objectives for Lake Erie Great Lakes Fishery Commission Special Publication 03-02, 1 56
87. Saitou N, Nei M (1987) The neighbor joining method: a new method for reconstructing phylogenetic trees Molecular Biology and Evolution, 4, 406 425
88. Scott WB, Crossman EJ (1973) Freshwater Fishes of Canada Fisheries Research Board of Canada Bulletin, 184, 1 966
89. Sepulveda-Villet OJ, Ford AM, Williams JD, Stepien CA (2009) Population genetic diversity and phylogeographic divergence patterns of the yellow perch (Perca flavescens) Journal of Great Lakes Research, 35, 107 119
90. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn WH Freeman and Co, Inc, New York, New York, USA
91. Stepien CA (1995) Population genetic divergence and geographic patterns from DNA sequences: examples from marine and freshwater fishes In : Evolution and the Aquatic Ecosystem: Defining Unique Units in Group Conservation (ed. Neilson J) American Fisheries Society Symposium 17, pp. 263 287. American Fisheries Society, Bethesda, Maryland, USA
92. Stepien CA, Faber JE (1998) Population genetic structure, phylogeography and spawning philopatry in walleye (Stizostedion vitreum) from mitochondrial DNA control region sequences Molecular Ecology, 7, 1757 1769
93. Stepien CA, Murphy D, Strange RM (2007) Broad- to fine scale population genetic patterning in the smallmouth bass Micropterus dolomieu across the Laurentian Great Lakes and beyond: An interplay of behavior and geography Molecular Ecology, 16, 1605 1624
94. Storfer A, Murphy MA, Evans JS et al. (2007) Putting the 'landscape' in landscape genetics Heredity, 98, 128 142
95. Strange RM, Burr BM (1997) Intraspecific phylogeography of North American highland fishes: a test of the Pleistocene vicariance hypothesis Evolution, 51, 885 897
96. Strange RM, Stepien CA (2007) Genetic divergence and connectivity among river and reef spawning populations of walleye (Sander vitreus) in Lake Erie Canadian Journal of Fisheries and Aquatic Sciences, 64, 437 448
97. Todd TN, Haas RC (1993) Genetic and tagging evidence for movement of walleyes between Lake Erie and Lake St Clair Journal of Great Lakes Research, 19, 445 452
98. Todd TN, Hatcher CO (1993) Genetic variability and glacial origins of yellow perch (Perca flavescens) in North America Canadian Journal of Fisheries and Aquatic Sciences, 50, 1828 1834
99. Trautman MB (1981) The Fishes of Ohio Ohio State University Press, Columbus, Ohio, USA
100. Turgeon J, Bernatchez L (2001) Mitochondrial DNA phylogeography of lake cisco (Coregonus artedi): evidence supporting extensive secondary contacts between two glacial races Molecular Ecology, 10, 987 1001
101. Underhill JC (1986) The fish fauna of the Laurentian Great Lakes, the St Lawrence lowlands, Newfoundland and Labrador In : The Zoogeography of North American Freshwater Fishes (ed. Hocutt CH, Wiley EO) pp. 105 136, John Willey & Sons, Inc, New York, New York, USA.
102. VanDeHey JA, Sloss BL, Peeters PJ, Sutton TM (2009) Genetic structure of lake whitefish (Coregonus clupeaformis) in Lake Michigan Canadian Journal of Fisheries and Aquatic Sciences, 66, 382 393
103. Wakely J, Aliacar N (2001) Gene genealogies in a metapopulation Genetics, 159, 893 905
104. Waples RS, 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 Molecular Ecology, 15, 1419 1439
105. Ward RD, Billington N, Hebert PDN (1989) Comparison of allozyme and mitochondrial DNA variation in populations of walleye (Stizostedion vitreum) Canadian Journal of Fisheries and Aquatic Sciences, 46, 2074 2084
106. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure Evolution, 38, 1358 1370
107. Wiley EO, Mayden RL (1985) Species and speciation in phylogenetic systematics, with examples from the North American fish fauna Annals of the Missouri Botanical Garden, 72, 596 635
108. Wirth T, Saint-Laurent R, Bernatchez L (1999) Isolation and characterization of microsatellite loci in the walleye (Stizostedion vitreum), and cross-species amplification within the family Percidae Molecular Ecology, 8, 1960 1962
109. Wolfert DR, Van Meter HD (1978) Movements of walleyes tagged in eastern Lake Erie, 1985-1987 New York Fish and Game Journal, 25, 16 22