Microsatellite diversity in sympatric reproductive ecotypes of pacific steelhead (Oncorhynchus my kiss) from the Middle Fork Eel River, California

Ecology of Freshwater Fish

Volumn 8, Issue 3, 1999, Pages 159-168

  Nielsen, J L ^a,c   Fountain, M C ^b  

^a PACIFIC SOUTHWEST RESEARCH STATION   (United States)

^b U S GEOLOGICAL SURVEY   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Conservation genetics; Evolution; Microsatellites; Oncorhynchus mykiss; Reproductive ecotypes

Indexed keywords

ECOTYPE; FISH; GENETICS; REPRODUCTION;

UNITED STATES;

EID: 0033372015     PISSN: 09066691     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0633.1999.tb00067.x     Document Type: Article

References (98)

1. Allendorf, F.W. & Waples, R.S. 1996. Conservation and genetics of salmonid fishes. In: Avise, J.C. & Hamrick, J.L., eds. Conservation genetics: case histories from nature. New York: Chapman & Hall, pp. 238-280.
2. Angers, B., Bernatchez, L., Angers, A., & Desgroseillers, L. 1995. Specific microsatellite loci for brook char reveal strong population subdivision on a microgeographic scale. Journal of Fish Biology 47(suppl A): 177-185.
3. Applied Biosystems Inc. ABI Prism. 1996. Genotyper 2.0 user's manual. Foster City, CA: Perkins-EImer Corp.
4. Ashley, M.V. & Dow, B.D. 1994. The use of microsatellite analysis in population biology: background, methods, and potential applications. In: Scherwater, B., Stait, B., Wagner, O.P. & DeSalle, R., ed. Molecular ecology and evolution: approaches and application. Basel: Birkhauser Verlag, pp. 185-201.
5. Avise, J.C. 1994. Molecular markers, natural history and evolution. New York: Chapman & Hall, pp. 511.
6. Barnhart, R.A. 1986. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Pacific Southwest) - steelhead. U. S. Fish and Wildlife Service Biological Report 82(11.60).
7. Barker, J. F. S., Moore, S. S. Hetzel, D. J. S. Evans, D. Tan, S. G. & Byrne, K. 1997. Genetic diversity of Asian water Buffalo (Biibalus bubalis): microsatellite variation and a comparison with protein-coding loci. Animal Genetics 28:103-115.
8. Barton, N.H. & Slatkin M. 1986. A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity 56: 409-415.
9. Behnke, R.J. 1992. Native trout of western North America. American Fisheries Society Monograph Number 6, Bethesda, MD. 275 pp.
10. Berg, W.J. 1987. Evolutionary genetics of rainbow trout, Parasalmo gairduerii (Richardson). Ph.D. thesis. Davis: University of California.
11. Bernatchez, L., Vuorinen, J.A., Bodaly, R.A. & Dodson, J.J. 1996. Genetic evidence for reproductive isolation and multiple origins of sympatric trophic ecotypes of whitefish (Coregomis). Evolution 50: 624-635.
12. Bowcock, A., Ruiz-Linares, A., Tomfohrde, J., Minch, E., Kid, J.K.. & Cavalli-Sforza, L.L. 1994. High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368: 455-157.
13. Boyce, W.M., Hedrick, P.W., Muggli-Cockett, N.B., Kalinowski, S., Penedo, M. C. T. & Ramey II, R.R. 1996. Genetic variation of major histocompatibility complex and microsatellite loci: a comparison in bighorn sheep. Genetics 145: 421-433.
14. Bruford, M.W. & Wayne, R.K. 1993. Microsatellites and their application to population genetic studies. Current Opinions in Genetics and Development 3: 939-943.
15. Busby, P.J., Wainwright, T.C., Bryant, G.J., Lierheimer, L.J., Waples, R.S., Waknitz, F.W. & Lagomarsino, I.V 1996. Status review of west coast steelhead from Washington, Idaho, Oregon, and California. National Marine Fisheries Technical Memorandum NMFS-NWFSC-27. Seattle, Washington. 261 pp.
16. Burgner, R.L., Light, J.T., Margolis, L., Okazaki, T., Tautz, A. & Ito, S. 1992. Distribution and origins of steelhead trout (Oncorhynchm mykiss) in offshore waters of the north Pacific Ocean. International North Pacific Fisheries Commission Bulletin Number 51. 92 pp.
17. Chilcote, M.W, Crawford, B.A. & Leider, S.A. 1980. A genetic comparison of sympatric populations of summer and winter steelheads. Transactions of the American Fisheries Society 109: 203-206.
18. Chilcote, M.W, Leider, S.A. & Loch, J.J. 1986. Differential reproductive success of hatchery and wild summer-run steelhead under natural conditions. Transactions of the American Fisheries Society 115: 726-735.
19. Clarke, W.C., Withler, R.E. & Shelbourn, J.E. 1992. Genetic control of juvenile life history patter in chinook salmon (Oncorliynclnts tshanytscha). Canadian Journal of Fisheries and Aquatic Sciences 49: 2300-2306.
20. Danzmann, R.G., Ferguson, M.M., Allendorf, F.W. & Knudsen, K.L. 1986. Heterozygosity and development rate in a strain of rainbow trout (Salnio gairdneri). Evolution 1986: 86-93.
21. Di Rienzo, A., Peterson, A.C., Garza, J.C., Valdes, A.M., Slatkin, M. & Freimer, N.B. 1994. Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Science of the United States of America 91: 3166-3170.
22. Estoup, A., Garnery, C.R., Solignac, M. & Cornuet, J.-M. 1995. Microsatellite variation in honey bee {Apis mellifers L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140: 679-695.
23. Estoup, A., Roussel, F.., Michalakis, Y., Cornuet, J.-M., Adriamanga, M. & Guyomard, R. (1998). Comparative analysis of microsatellite and allozyme markers: a case study investigating microgeographic differentiation in brown trout (Salnw trutta). Molecular Ecology 7: 339-353.
24. Everest, F.H. 1973. Ecology and management of summer steelhead in the Rogue River. Oregon State Came Commission Fisheries Research Report Number 7. 48 pp.
25. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using bootstrap. Evolution 39: 783-791.
26. Felsenstein, J. 1995. PHYL1P version 3.572 - phylogeny inference package distributed by author. Seattle: Department of Genetics SK-10, University of Washington.
27. Ferguson, M.M. 1996. Variation at enzyme coding loci and correlates of fitness in rainbow trout: a cohort analysis. Journal of Fish Biology 48: 1088-1096.
28. FitzSimmons, N.N., Moritz, C. & Moore, S.S. 1995. Conservation and dynamics of microsatellite loci over 300 million years of marine turtle evolution. Molecular Biology and Evolution 12: 432-440.
29. Gall, G.A.E. & Gross, S.J. 1978. A genetic analysis of the performance of three rainbow trout broodstocks. Aquaculture 15: 113-127.
30. Guo, S.W. & Thompson, E.A. 1992. Performing the exact test of Hardy-Weinberg and multiple alleles. Biometrics 43: 805-811.
31. Goldstein, D.B., Linares, A.R., Cavalli-Sforza, L.L. & Feldman, M.W. 1995a. An evaluation of genetic distances for use with microsatellite loci. Genetics 139: 463-471.
32. Goldstein, D.B., Linares, A.R., Cavalli-Sforza, L.L. & Feldman, M.W. 1995b. Genetic absolute dating based on microsatellites and the origins of modern humans. Proceedings of the National Academy of Science of the United States of America 92: 6723-6727.
33. Healey, M.C. & Prince, A. 1995. Scales of variation in life history tactics of Pacific salmon and the conservation of phenotype and genotype. In: Nielsen, J.L. ed. Evolution and the aquatic ecosystem: defining unique units in population conservation. American Fisheries Society Symposium 17, pp. 176-184.
34. Hindar, K., Jonsson, B., Ryman, N. & Stahl, G. 1991. Genetic relationships among landlocked, resident, and anadromous brown trout, Salmo trutta L. Heredity 66: 83-91.
35. Jarne, P. & Lagoda, P.J.-L. 1996. Microsatellites, from molecules to populations and back. Trends in Ecology and Evolution 11: 424-29.
36. Jones, WE. 1980. Summer steelhead (Salmo gairdneri) in the Middle Fork Eel River and their relationship to environmental changes, 1966 through 1978. California Department of Fish and Game Anadromous Fisheries Division Administrative Report Number 80-2. 25 pp.
37. Jones, WE. 1992. Historical distribution and recent trends of summer steelhead, Oncorhynclms mykiss, in the Eel River, California. Proceedings of the Eel River Workshop, Redding California Feb. 6, 1992. Sponsored by the California Department of Fish and Game, California-Nevada Chapter American Fisheries Society, and Pacific Gas and Electric Co. 17 pp.
38. Jones, WE. 1997. Summer steelhead, Oncorhynclnis mykiss, in the Middle Fork of the Eel River, Trinity and Mendocino Counties: 1996 Annual Survey and Trends. California Department of Fish and Game Anadromous Fisheries Division Administrative Report, Sacramento CA. 28 pp.
39. Klicka, J. & Zink, R.M. 1997. The importance of recent ice ages in speciation: a failed paradigm. Science 277: 1666-1669.
40. Leider, S.A., Chilcote, M.W. & Loch, J.J. 1984. Spawning characteristics of sympatric populations of steelhead trout (Salmo gairdneri): evidence for partial reproductive isolation. Canadian Journal of Fisheries and Aquatic Science 41: 1454-1462.
41. McConnell, S.K., O'Reilly, P., Hamilton, L., Wright, J.M. & Bentzen, P. 1995. Polymorphic microsatellite loci from Atlantic salmon (Salmo salar): genetic differentiation of North American and European populations. Canadian Journal of Fisheries and Aquatic Science 52: 1863-1872.
42. McKay, L.R., Ihssen, P.E., Friars, G.W. 1986. Genetic parameters of growth in rainbow trout, Salmo gairdneri, prior to maturation. Canadian Journal of Genetics and Cytology 28: 306-312.
43. Mills, L.S. & Allendorf, F.W. 1996. The one-migrant-per-generation rule in conservation and management. Conservation Biology 10: 1509-1518.
44. Moritz, C. 1994. Defining "evolutionary significant units" for conservation. Trends in Ecology and Evolution 9: 373-375.
45. Morris, D.B., Richard, K.R. & Wright, J.M. 1996. Microsalellites from rainbow trout (Oncorhynchus mykiss) and their use for genetic studies of salmonids. Canadian Journal of Fisheries and Aquatic Science 53: 120-126.
46. Nakamoto, R.J. 1994. Characteristics of pools used by adult summer steelhead oversummering in the New River, California. Transactions of the American Fisheries Society 123: 757-765.
47. Neave, F. 1944. Racial characteristics and migratory habits in Salmo gairdneri. Journal of the Fisheries Research Board of Canada 6: 245-251.
48. Nei, M. 1987. Molecular evolutionary genetics. New York: Columbia University Press, 512 pp.
49. Nielsen, J.L. ed. 1995. Evolution and the aquatic ecosystem: defining unique units in population conservation. American Fisheries Society Symposium 17, 433 pp.
50. Nielsen, J.L. 1996. Molecular genetics and conservation of salmonid biodiversity: Oncorhynchus at the edge of their range. In: Smith, T.B. & Wayne, R.K., ed. Molecular genetics in conservation. Oxford: Oxford University Press, pp. 383-398.
51. Nielsen, J.L., Gan, C.A., Wright, J.M., Morris, D.B. & Thomas, W.K. 1994a. Biogeographic distributions of mitochondrial and nuclear markers for southern steelhead. Molecular Marine Biology and Biotechnology 3: 281-293.
52. Nielsen, J.L., Lisle, T.E. & Ozaki, V 1994b. Thermally stratified pools and their use by steelhead in northern California streams. Transactions of the American Fisheries Society 123: 613-626.
53. Nielsen, J.L., Fountain, M.C. & Wright, J.M. 1997a. Biogeographic analysis of Pacific trout (Oncorhynchus mykiss) in California and Mexico based on mitochondrial DNA and nuclear microsatellites. In: Kocher T. & Stepien C. eds. Molecular systematics of fishes. New York: Academic Press, pp. 53-73.
54. Nielsen, J.L., Carpanzano, C., Fountain, M.C. & Gan, C.A. 1997b. Mitochondrial DNA and nuclear microsatellite diversity in hatchery and wild Oncorhynchus mykiss from freshwater habitats in southern California. Transactions of the American Fisheries Society 126: 397-17.
55. Nielsen, J.L., Fountain, M.C., Favela, J.C., Cobble, K. & Jensen, B.J. 1998. Oncorhynchus at the southern extent of their range: a study of mtDNA control-region sequence with special reference to an undescribed subspecies of O. mykiss from Mexico. Environmental Biology of Fishes 51: 7-23.
56. O'Reilly, P.T., Hamilton, L.C., McConnell, S.K., & Wright, J.M. 1996. Rapid detection of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Canadian Journal of Fisheries and Aquatic Sciences 53: 2292-2298.
57. Parkinson, E. A. 1984. Genetic variation in populations of steelhead trout (Salmo gairdneri) in British Columbia. Canadian Journal of Fisheries and Aquatic Science 41: 1412-1420.
58. Pucket, L.K. 1975. The status of spring-run steelhead (Salmo gairdneri) of the Eel River system. California Department of Water resources and Department of Fish and Game Memorandum Report, Sacramento, CA. 27 pp.
59. Raymond, M. & Roussel, F. 1995 An exact test for population differentiation. Evolution 49: 1280-1283.
60. Raymond, M. & Roussel, F. 1997 GENEPOP version 3. l a, August 1997. Univ. Monlpellier II, 34095 Montpellier cedex 05, France, (available through anonymous login at ftp.cefe.cnrsmop.fr or e-mail: Raymond@isem.univ-montp2.fr), 30 pp.
61. Reznick, D.N., Bryga, H.A. 1996. Life-history evolution in guppies (Poecilia reticulata: Poeciliidae) V. Genetic basis of parallelism in life histories. American Naturalists 147: 339-359.
62. Rice, W.R. 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.
63. Rico, C, Rico, I. & Hewitt, G. 1996. 470 million years of conservation of microsatellite loci among fish species. Proceedings of the Royal Society of London 263: 549-557.
64. Roelofs, T.D. 1983. Current status of California summer steelhead (Salmo gairdneri) stocks and habitat and recommendations for their management. Report to the U. S. Forest Service Region 5, San Francisco, CA.
65. Roussel, F. 1996. Equilibrium values of measures of population subdivision for stepwise mutation processes. Genetics 142: 1357-1362.
66. Roussel, F. & Raymond, M. 1995. Testing helerozygote excess and deficiency. Genetics 140: 1413-1419.
67. Rubinszlein, D.C., Amos, W., Leggo, J., Goodburn, S., Jain, S., Li, S-H., Margolis, R.L., Ross, C.A. & Ferguson-Smilh, M.A. 1995. Microsalellile evolulion - evidence for direclionalily and varialion in rate between species. Nature Genetics 10: 337-343.
68. Sawailova, K.A., Maksimov, VA., Mina, M.V, Novikov, G.G., Kokhmenko, L.V. & Malsuk, V.E. 1973. The noble Irouls of Kamchalka: syslemalics, ecology, and Ihe possibilities of using them as Ihe objecl of Iroul-cullure and acclimalizalion. The Voronezh University Publishers. 119 pp.
69. Schneider, S., Schneider, S., Kueffer, J.-M., Roessli, D. & Excoffier, L. 1997. ARLEQUIn: An exploratory population genetics software environment. Available: htlp://anlhropologie.unige.ch/arlequin
70. Scribner, K.T., Gusl, J.R. & Fields, R.L. 1996. Isolalion and characterization of novel microsatellile loci: cross-species amplificalion and populalion genelic applications. Canadian Journal of Fisheries and Aqualic Sciences 53: 685-693.
71. Shapovalov, L. & Tafl, A.C. 1954. Life hislories of steelhead rainbow troul (Salmo gairdneri gairdneri) and silver salmon (Oncorhynchus kisutch) wilh special reference to Waddell Creek, California, and recommendations regarding Iheir managemenl. California Deparlmenl of Fish and Game Bullelin 98, 375 pp.
72. Shriver, M.D., Jin, L., Chakraborty, R. & Boerwinkle, E. 1993. VNTR allele frequency dislribulions under Ihe stepwise mutation model: a computer simulalion approach. Genelics 134: 983-993.
73. Shriver, M.D., Jin, L., Boerwinkle, E., Deka, R., Ferrell, R.E. & Chakraborly, R. 1995. A novel measure of genetic distance for highly polymorphic tandem repeat loci. Molecular Biology and Evolution 12: 914-920.
74. Skaala, 0. & Nvdal, G. 1989. Genetic differcntialion belween freshwaler residenl and anadromous brown troul, Salmo iruita, wilhin walercourses. Journal of Fish Biology 34: 597-605.
75. Slalkin, M. 1985. Rare alleles as indicalors of gene flow. Evolulion 39: 53-65.
76. Slalkin, M. 1995. A measure of populalion subdivision based on microsalellile allele frequencies. Genetics 139: 457-462.
77. Sletlan, A., Olsaker, I. & Lie, O. 1996. Polymorphic Allanlic salmon, Salmo salar L., microsalelliles al Ihe SSOSL438, SSOSL439, and SSOSL444 loci. Animal Genelics 27: 57-64.
78. Smilh, S.B. 1968. Reproductive isolalion in summer and winler races of sleelhead iroul. In: Norlhcote, T.G., ed. Symposium on Salmon and Trout in Streams. HR MacMillan Lectures in Fisheries, Universily of Brilish Columbia, Vancouver, pp. 21-38.
79. Stearns, S.C. 1976. Life history taclics: a review of Ihe idea. Quarlerly Reviews in Biology 51: 3-47.
80. Takahala, N. & Slalkin, M. 1984. Mitochondrial gene flow.
81. Proceedings of the National Academy of Sciences of the United States of America 81: 1764-1767.
82. Takezaki, N. & Nei, M. 1996. Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144: 389-399.
83. Taylor, E.B., Foote, C.J. & Wood, C.C. 1996. Molecular genetic evidence for parallel life history evolution in a Pacific salmon: sockeye salmon and kokanee (Oncorhynclua nerka). Evolution 50: 401-116.
84. Tessier, N.T., Bernatchez, L., Presa, P. & Angers, B. 1995. Gene diversity analysis of mitochondrial DNA, microsatellites and allozymes in landlocked Atlantic salmon. Journal of Fish Biology 47(suppl A): 156-163.
85. Tessier, N.T., Bernatchez, L. & Wright, J.M. 1997. Population structure and impact of a supportive breeding program inferred from mitochondrial and microsatellite DNA analyses in sympatric landlocked Atlantic salmon populations (Salnto salar L.) Molecular Ecology 6: 735-750.
86. Thorgaard, G. H. 1977. Chromosome studies of steelhead. In: Gall, G., ed. Proceedings of the genetic implications of steelhead management symposium. Special Report 77-1. California Cooperative Fishery Research Unit. Davis: University of California, pp. 4-18.
87. Utter, F. M. & Allendorf, F.W. 1977. Determination of the breeding structure of steelhead populations through gene frequency analysis. In: Gall, G., ed. Proceedings of the genetic implications of steelhead management symposium. Special Report 77-1. California Cooperative Fishery Research Unit. Davis: University of California, pp. 22-25.
88. Utter, P.M., Allendorf, F.W. & Hodgins, H.O. 1974. Genetic variability and relationships in Pacific salmon and related trout based on protein variation. Systematic Zoology 22: 257-270.
89. Wangila, B.C.C. & Dick, T.A. 1988. Influence of genotype and temperature on the relationship between specific growth rate and size of rainbow trout. Transactions of the American Fisheries Society 117: 560-564.
90. Waples, R.S. 1995. Evolutionarily significant units and the conservation of biological diversity under the endangered species act. In: Nielsen, J.L., ed. Evolution and the aquatic ecosystem: defining unique units in population conservation. American Fisheries Society Symposium 17, pp. 8-27.
91. Ward, M.B. 1988. Adult summer steelhead trout utilization of summer holding pools, Middle Fork Eel River, California. Proceedings of the 68th Annual Conference of the Western Association of Fish and Wildlife Agencies. Albuquerque, N.M. July 10-13, 1988.
92. Weber, J.L. & Wong, C. 1993. Mutation of human short tandem repeats. Human Molecular Genetics 2: 1123-1128.
93. Williams, R.N., Shiozawa, O.K., Carter, J.E. & Leary, R.F. 1996. Genetic detection of putative hybridization between native and introduced rainbow trout populations of the upper Snake River. Transactions of the American Fisheries Society 125: 387-01.
94. Wilson, A.C., Carlson, S.S. & White, T.J. 1977. Biochemical evolution. Annual Reviews in Biochemistry 46: 573-639.
95. Withler, I.L. 1966. Variability in life history characteristics of steelhead trout (Salmo gairdneri) along the Pacific coast of North America. Journal of the Fisheries Research Board of Canada 23: 365-393.
96. Wood, C.C. 1995. Life history variation and population structure in sockeye salmon. In: Nielsen, J.L., ed. Evolution and the aquatic ecosystem: defining unique units in population conservation. American Fisheries Society Symposium 17, pp. 195-216.
97. Wright, S. 1931. Evolution in Mendelian populations. Genetics 16: 97-259.
98. Wright, S. 1968. Evolution and the genetics of populations. Vol. 1. Chicago: University of Chicago Press.