Abstract
Pacific salmon (Oncorhynchus spp.) have been central to the development of management concepts associated with evolutionarily significant units (ESUs), yet there are still relatively few studies of genetic diversity within threatened and endangered ESUs for salmon or other species. We analyzed genetic variation at 10 microsatellite loci to evaluate spatial population structure and genetic variability in indigenous Chinook salmon (Oncorhynchus tshawytscha) across a large wilderness basin within a Snake River ESU. Despite dramatic 20th century declines in abundance, these populations retained robust levels of genetic variability. No significant genetic bottlenecks were found, although the bottleneck metric (M ratio) was significantly correlated with average population size and variability. Weak but significant genetic structure existed among tributaries despite evidence of high levels of gene flow, with the strongest genetic differentiation mirroring the physical segregation of fish from two sub-basins. Despite the more recent colonization of one sub-basin and differences between sub-basins in the natural level of fragmentation, gene diversity and genetic differentiation were similar between sub-basins. Various factors, such as the (unknown) genetic contribution of precocial males, genetic compensation, lack of hatchery influence, and high levels of current gene flow may have contributed to the persistence of genetic variability in this system in spite of historical declines. This unique study of indigenous Chinook salmon underscores the importance of maintaining natural populations in interconnected and complex habitats to minimize losses of genetic diversity within ESUs.
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Abdelkrim J, Pascal M, Samadi S (2005) Island colonization and founder effects: the invasion of the Guadeloupe islands by ship rats (Rattus rattus). Mol Ecol 14:2923–2931
Allendorf FW, Waples RS (1996) Conservation and genetics of salmonid fishes. In: Avise JC, Hamrick JL (eds) Conservation genetics: case histories from nature. Chapman & Hall, New York, pp 238–280
Angers B, Magnan P, Plante M, Bernatchez L (1999) Canonical correspondence analysis for estimating spatial and environmental effects on microsatellite gene diversity in brook charr (Salvelinus fontinalis). Mol Ecol 8:1043–1053
Ardren W, Kapuscinski AR (2003) Demographic and genetic estimates of effective population size (N e) reveals genetic compensation in steelhead trout. Mol Ecol 12:35–49
Balloux F, Lugon-Moulin N (2001) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165
Banks MA, Blouin MS, Baldwin BA, Rashbrook VK, Fitzgerald HA, Blankenship SM, Hedgecock D (1999) Isolation and inheritance of novel microsatellites in Chinook salmon (Oncorhynchus tshawytscha). J Heredity 90:281–288
Banks MA, Rashbrook VK, Calavetta MJ, Dean CA, Hedgecock D (2000) Analysis of microsatellite DNA resolves genetic structure and diversity of Chinook salmon (Oncorhynchus tshawytscha) in Californiaȁ9s Central Valley. Can J Fish Aquat Sci 57:915–927
Bartley DM, Gall GAE (1990) Genetic structure and gene flow in Chinook salmon populations of California. Trans Am Fish Soc 119:55–71
Beacham TD, Supernault JK, Wetklo M (2003) The geographic basis for population structure in Fraser River Chinook salmon (Oncorhynchus tshawytscha). Fish Bull 101:229–242
Bentzen P, Olsen JB, Mclean JE, Seamons TR, Quinn TP (2001) Kinship analysis of Pacific salmon: insights into mating, homing, and timing of reproduction. J Heredity 92:127–136
Bernatchez L, Martin S (1996) Mitochondrial DNA diversity in anadramous rainbow smelt, Osmerus mordax Mitchell: a genetic assessment of the member-vagrant hypothesis. Can J Fish Aquat Sci 53:424–433
Blanchfield PJ, Ridgway MS, Wilson CC (2003) Breeding success of male brook trout (Salvelinus fontinalis) in the wild. Mol Ecol 12:2417–2428
Brannon EL, Powell MS, Quinn TP, Talbot A (2004) Population structure of Columbia River Basin Chinook salmon and steelhead trout. Rev Fish Sci 12:99–232
Brown EM (2002) 2000 salmon spawning ground surveys. Pacific Salmon Treaty Program, Award Number NA77FP0445, Idaho Fish Game Rep. 02-33, Boise, Idaho
Cairney M, Taggart JB, Hoyheim B (2000) Characterization of microsatellite and minisatellite loci in Atlantic salmon (Salmo salar L.) and cross species amplification in other salmonids. Mol Ecol 9:2175–2178
Castric V, Bernatchez L (2003) The rise and fall of isolation by distance in the anadromous brook charr (Salvelinus fontinalis Mitchill). Genetics 163:983–996
Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 32:550–570
Consuegra S, Verspoor E, Knox D, Leaniz CG (2005) Asymmetric gene flow and the evolutionary maintenance of genetic diversity in small, peripheral Atlantic salmon populations. Conserv Genet 6:823–842
Cornuet J-M, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Cornuet J-M, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000
Costello AB, Down TE, Pollard SM, Pacas CJ, Taylor EB (2003) The influence of history and contemporary stream hydrology on the evolution of genetic diversity within species: an examination of microsatellite DNA variation in bull trout, Salvelinus confluentus (Pisces: Salmonidae). Evolution 57:328–344
Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evolut 15:290–295
Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M,␣Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci 91:3166–3170
Dittman AH, Quinn TP (1996) Homing in Pacific salmon: mechanisms and ecological basis. J Exp Biol 199:83–91
Dizon AE, Lockyer C, Perrin WF, Demaster DP, Sisson J (1992) Rethinking the stock concept: a phylogenetic approach. Conserv Biol 6:24–36
Doerner KC, Braden W, Cork J, Cunningham T, Rice A, Furman BJ, McElroy D (2005) Population genetics of resurgence: white-tailed deer in Kentucky. J. Wildlife Manage 69:345–355
Dunham JB, Peacock M, Tracy CR, Nielsen J, Vinyard GL (1999) Assessing extinction risk: integrating genetic information. Conserv Ecol [Online] Available URL:http//www.consecol.org/vol3/iss1/art2
England PR, Osler GHR, Woodworth LM, Montgomery ME, Briscoe DA, Frankham R (2003) Effects of intense versus diffuse population bottlenecks on microsatellite genetic diversity and evolutionary potential. Conserv Genet 4:595–604
Ford MJ (2004) Conservation units and preserving diversity. In: Hendry AP, Stearns SC (eds) Evolution illuminated: salmon and their relatives. Oxford University Press, Oxford, pp␣338–357
Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140
Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752
Garcia-Vazquez E, Moran P, Martinez JL, Perez J, deGaudemar B, Beall E (2001) Alternative mating strategies in Atlantic salmon and brown trout. J Heredity 92:146–149
Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version (2)(9)3). Available from http://www.unil.ch/izea/softwares/fstat.html
Greig CJD, Banks MA (1999) Five multiplexed microsatellite loci for rapid response run identification of Californiaȁ9s endangered winter Chinook salmon. Anim Genet 30:316–324
Guinand B, Scribner KT (2003) Evaluation of methodology for detection of genetic bottlenecks: inferences from temporally replicated lake trout populations. Comp Rendus Biol 326:S61–S67
Habicht C, Olsen JB, Faira L, Seeb JE (2004) Smaller effective population sizes evidenced by loss of microsatellite alleles in tributary-spawning populations of sockeye salmonfrom the Kvichak River, Alaska drainage. Environ Biol Fishes 69:51–62
Halupka KC, Willson MF, Bryant MD, Everest FH, Gharrett AJ (2003) Conservation of population diversity of Pacific salmon in southeast Alaska. North Am J Fish Manage 23:1057–1086
Hansen MM, Mensberg K-L (1998) Genetic differentiation and relationship between genetic and geographical distance in Danish sea trout (Salmo trutta L.) populations. Heredity 81:493–504
Hansen MM, Nielsen EE, Ruzzante DE, Bouza C, Mensberg K-L (2000) Genetic monitoring of supportive breeding in brown trout (Salmo trutta L.), using microsatellite DNA markers. Can J Fish Aquat Sci 57:2130–2139
Hansen MM, Kenchington E, Nielsen EE (2001) Assigning individual fish to populations using microsatellite DNA markers. Fish Fish 2:93–112
Hanski I (1991) Single-species metapopulation dynamics: concepts, models and observations. Biol J Linn Soc 42:17–38
Hassemer PF (1993) Salmon spawning ground surveys, 1989–1992 Project F-73-R-(15) Idaho Department of Fish and Game. Boise
Heath DD, Pollard S, Herbinger C (2001) Genetic structure and relationships among steelhead trout (Oncorhynchus mykiss) populations in British Columbia. Heredity 86:618–627
Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic measures: inferring the relative influence of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914
Ingvarsson PK (2001) Restoration of genetic variation lost—the genetic rescue hypothesis. Trends Ecol Evolut 16:62–63
Isaak DJ, Thurow RF, Rieman BE, Dunham JB (2003) Temporal variation in synchrony among Chinook salmon (Oncorhynchus tshawytscha) redd counts from a wilderness area in central Idaho. Can J Fish Aquat Sci 60:840–848
Isaak DJ, Thurow RF (2006) Network-scale spatial and temporal variation in Chinook salmon (Oncorhynchus tshawytscha) redd distributions: patterns inferred from spatially continuous replicate surveys. Can J Fish Aquat Sci 63:285–296
King TL, Kalinowski ST, Schill WB, Spidle AP, Lubinski BA (2001) Population structure of Atlantic salmon (Salmo salar L.): a range-wide perspective from microsatellite DNA variation. Mol Ecol 10:807–821
Langella O (2002) POPULATIONS. Centre National de la Recherche Scientifique, Laboratoire Populations, Génétique et Evolution, Gif sur Yvettev; http://www.cnrs-gif.fr/pge/bioinfo/populations
Lee DC, Sedell JR, Rieman BE, Thurow RF, Williams JE (1997) Broadscale assessment of aquatic species and habitats. U.S. For. Serv., Gen. Tech. Rep. PNW-GTR-405, Portland
Lichatowich JA, Mobrand LE (1995) Analysis of Chinook salmon in the Columbia River from an ecosystem perspective. Report for U.S. Department of Energy, Bonneville Power Administration, Contract No. DE-Am79-92BP25105, Portland
Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evolut 18:189–197
Marshall AR, Blankenship HL, William PC (2000) Genetic characterization of naturally spawned Snake River fall-run Chinook salmon. Trans Am Fish Soc 129:680–698
McClure M, Spruell P, Utter F, Carmichael R, Cooney T, Hassemer P, Howell P, McCullough D, Petrosky C, Schaller H. (2003a). Independent populations of listed Chinook salmon, sockey salmon and steelhead Evolutionarily Significant Units in the Interior Columbia Basin. Draft Technical Recovery Team document released for co-manager review. http://www.nwfsc.noaa.gov/trt/trt_pop_id.htm
McClure MM, Holmes EE, Sanderson BL, Jordan CE (2003b). A large-scale, multispecies status assessment: anadromous salmonids in the Columbia River basin. Ecological Applications 13:964–989
McConnell SKJ, Ruzzante DE, Oȁ9Reilly PT, Hamilton L, Wright JM (1997) Microsatellite loci reveal highly significant genetic differentiation among Atlantic salmon (Salmo salar L.) stocks from the east coast of Canada. Mol Ecol 6:1075–1089
McElhany P, Ruckelshaus MH, Ford MJ, Wainwright TC, Bjorkstedt EP (2000) Viable salmonid populations and the recovery of evolutionarily significant units. U.S. Dept. Commer., NOAA Tech. Memo. NMFS-NWFSC-42, p. 156
McPhail JD, Lindsey CC (1986) Zoogeography of the freshwater fishes of Cascadia (the Columbia system and rivers north to the Stikine). In: Hocutt CH, Wiley EO (eds) Zoogeography of North American freshwater fishes. John Wiley & Sons, New York
Meyer GA, Leidecker ME (1999) Fluvial terraces along the Middle Fork Salmon River, Idaho, and their relation to glaciation, landslide dams, and incision rates: a preliminary analysis and river-mile guide. In: Hughes SS, Thackray GD (eds) Guidebook to the Geology of Eastern Idaho. Idaho Museum of Natural History, Pocatello, pp 219–235
Minshall GW, Robinson CT, Lawrence DE, Andrews DA, Brock JT (2001) Benthic macroinvertebrate assemblages in five central Idaho (USA) streams over a 10-year period following disturbance by wildfire. Int J Wildland Fire 10:201–213
Moritz C (1994) Defining ȁ8evolutionary significant unitsȁ9 for conservation. Trends Ecol Evolut 9:373–375
Naish KA, Park LK (2002) Linkage relationships for 35 new microsatellite loci in Chinook salmon Oncorhynchus tshawytscha. Anim Genet 33:316–318
Nehlsen W, Williams JE, Lichatowich JA (1991) Pacific salmon at the crossroads: stocks at risk from California, Oregon, Idaho, and Washington. Fisheries 16:4–21
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Neville H, Dunham J, Peacock M (in press-a) Assessing connectivity in salmonid fishes with DNA microsatellite markers. In: Crooks K, Sanjayan MA (eds) Connectivity conservation. Cambridge University Press, Cambridge, UK
Neville HM, Dunham JB, Peacock MM (in press-b) Landscape attributes and life history variability shape genetic structure of trout populations in a stream network. Landscape Ecol
Nielsen JL, Powers DA (eds) (1995) Evolution and the aquatic ecosystem: defining unique units in population conservation. American Fisheries Society, Bethesda, MD
Olsen JB, Bentzen P, Seeb JE (1998) Characterization of seven microsatellite loci derived from pink salmon. Mol Ecol 7:1087–1089
Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Computer Appl Biosci 12:357–358
Piry S, Luikart G, J.-M. Cornuet. (1997) Bottleneck: http://www.ensam.inra.fr/URLB
Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J␣Heredity 90:502–503
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Quinn TP (1993) A review of homing and straying of wild and hatchery-produced salmon. Fish Res 18:29–44
Quinn TP (2005) The behavior and ecology of Pacific salmon and trout. American Fisheries Society in association with University of Washington Press
Ramstad KM, Woody CA, Sage GK, Allendorf FW (2004) Founding events influence genetic population structure of sockeye salmon (Oncorhynchus nerka) in Lake Clark, Alaska. Mol Ecol 13:277–290
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283
Raymond M, Rousset F (2004) GENEPOP. http://www.wbiomed.curtin.edu.au/genepop/
Rexroad CE, Coleman RL, Martin AM, Hershberger WK, Killefer J (2001) Thirty-five polymorphic microsatellite markers for rainbow trout (Oncorhynchus mykiss). Anim Genet 32:317–319
Rundle HD, Mooers AO, Whitlock MC (1998) Single founder-flush events and the evolution of reproductive isolation. Evolution 52:1850–1855
Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evolut 1:9–10
Ryman N, Laikre L (1991) Effects of supportive breeding on the genetically effective population size. Conserv Biol 5:325–329
Saccheri I, Kuussaari M, Kankare M, Vikman PFW, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulations. Nature 392:491–494
Shrimpton JM, Heath DD (2003) Census vs. effective population size in Chinook salmon: large- and small-scale environmental perturbation effects. Mol Ecol 12:2571–2583
Slatkin M (1993) Isolation by distance in equilibrium and non-equlibrium populations. Evolution 47:264–279
Stacey PB, Johnson VA, Taper ML (1997) Migration within metapopulation: the impact upon local population dynamics. In: Hanski IA, Gilpin ME (eds) Metapopulations biology: ecology, genetics, and evolution. Academic Press, Inc., San Diego, pp 267–291
Takezaki N, Nei M (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite data. Genetics 144:389–399
Taylor EB (1991) A review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture 98:185–207
Teel DJ, Milner GB, Winans GA, Grant WS (2000) Genetic population structure and origin of life history types in Chinook salmon in British Columbia, Canada. Trans Am Fish Soc 129:194–209
Templeton AR (1980) The theory of speciation via the founder principle. Genetics 94:1011–1038
Tessier N, Bernatchez L, Wright JM (1997) Population structure and impact of supportive breeding inferred from mitochondrial and microsatellite DNA analyses in land-locked Atlantic salmon Salmo salar L. Mol Ecol 6:735–750
Thurow RF, Lee DC, Rieman BE (1997) Distribution and status of seven native salmonids in the interior Columbia River basin and portions of the Klamath River and Great basins. North Am J Fish Manage 17:1094–1110
Thurow RF, Lee DC, Rieman J (2000) Status and distribution of Chinook salmon and steelhead in the interior Columbia River basin and portions of the Klamath River basin. In: Knudsen E, Steward C, MacDonald D, Williams J, Reiser D (eds) Sustainable fisheries management: Pacific salmon. CRC Press, Boca Raton, pp 133–160
Utter F, Milner G, Stahl G, Teel D (1989) Genetic population structure of Chinook salmon, Oncorhynchus tshawytscha, in the Pacific northwest. Fish Bull 87:239–264
Utter F (2004) Population genetics, conservation and evolution in salmonids and other widely cultured fishes: some perspectives over six decades. Rev Fish Biol Fish 14:125–144
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley PF (2003) MicroChecker. The University of Hull
Waples RS (1990a) Conservation genetics of pacific salmon II. Effective population size and rate of loss of genetic variability. J Heredity 81:267–276
Waples RS (1990b) Temporal changes of allele frequency in Pacific salmon: implications for mixed-stock fishery analysis. Can J Fish Aquat Sci 47:968–976
Waples RS (1990c) Conservation genetics of Pacific salmon III. Estimating effective population size. J Heredity 81:277–289
Waples RS (1991) Pacific salmon, Oncorhynchus spp., and the definition of “species” under the Endangered Species Act. U.S. Natl Marine Fish Serv Mar Fish Rev 53:11–22
Waples RS (1995) Evolutionarily significant units and the conservation of biological diversity under the Endangered Species Act. Am Fish Soc 17:8–27
Waples RS, Gustafson RG, Weitkamp LA, Myers JM, Johnson OW, Busby PJ, Hard JJ, Bryant GJ, Waknitz FW, Neely K, Teel D, Grant WS, Winans GA, Phelps S, Marshall A, Baker BM (2001) Characterizing diversity in salmon from the Pacific Northwest. J Fish Biol 59:1–41
Waples RS (2002) Effective size of fluctuating salmonid populations. Genetics 161:783–791
Waples RS, Teel DJ, Myers JM, Marshall AR (2004) Life-history divergence in Chinook salmon: historic contingency and parallel evolution. Evolution 58:386–403
Ward RD, Woodwark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44:213–232
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wenburg JK, Bentzen P (2001) Genetic and behavioral evidence for restricted gene flow among coastal cutthroat trout populations. Trans Am Fish Soc 130:1049–1069
Williamson KS, Cordes JF, May B (2002) Characterization of microsatellite loci in Chinook salmon (Oncorhynchus tshawytscha) and cross-species amplification in other salmonids. Mol Ecol Not 2:17–19
Acknowledgements
We thank T. Williams, T. Antonich, K. Ball, S. Meyer, L. Isaak, C. Justice, R. Nelson, T. Archibald, Q. Tucket, and G. Burak for their assistance in collecting tissue samples. We also thank J. Johnson and T. Copeland of the Idaho Department of Fish and Game for providing access to their genetic tissue database. The Bonneville Power Administration provided funding for field crews. M. Powell, S. Narum, P. Moran and T. Lundrigan were helpful in selecting and optimizing microsatellite loci. We are grateful to M. Campbell, C. Cegelski, M.␣McClure and three anonymous reviewers who provided insightful comments on earlier drafts of this manuscript. HN was funded by a Joint Venture Agreement (JV-11222014-095) between the USDA Forest Service Rocky Mountain Research Station and the University of Nevada, Reno, with additional funding provided by NOAA Fisheries (Northwest Fisheries Science Center). The use of trade names in this paper is for reader information only and does not imply endorsement by the U.S. Department of Agriculture of any product or service
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Neville, H., Isaak, D., Thurow, R. et al. Microsatellite variation reveals weak genetic structure and retention of genetic variability in threatened Chinook salmon (Oncorhynchus tshawytscha) within a Snake River watershed. Conserv Genet 8, 133–147 (2007). https://doi.org/10.1007/s10592-006-9155-4
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DOI: https://doi.org/10.1007/s10592-006-9155-4