Skip to main content
Log in

Variation in developmental biology and microsatellite DNA in reproductive ecotypes of kokanee, Oncorhynchus nerka: Implications for declining populations in a large British Columbia lake

  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Kokanee are the nonanadromous (freshwater resident) form of sockeyesalmon (Oncorhynchus nerka) found in lake ecosystems throughoutthe North Pacific region. Kokanee commonly exhibit two reproductiveecotypes; `stream-spawners' that reproduce in streams tributary tolakes, and `beach-spawners' that reproduce on submerged lakeshore gravelbeaches. Okanagan Lake, in the southcentral interior of BritishColumbia, Canada, contains beach- and stream-spawning kokanee and bothecotypes have declined dramatically in abundance over the last 20 years.We examined developmental biology (developmental rate to hatching andemergence) and genetic divergence at eight microsatellite loci toinvestigate phenotypic and genetic differentiation between ecotypes tounderstand selective and demographic factors that might influence therecovery of depressed populations. Beach-spawning female kokanee weresmaller and produced smaller eggs than females from stream-spawningpopulations. There was no striking difference in time to 50%hatching between ecotypes, but beach-spawning kokanee developed fasterfrom hatching to emergence. Microsatellite loci were highly polymorphicin kokanee (between 5 and 23 alleles per locus) and showed significantdifferentiation among populations (average θ = 0.018). There was,however, no significant variation attributable to spawning ecotype afteraccounting for variation within ecotypes. Simulated population-mixtureanalyses indicated good potential for genetic classification of kokaneeas beach- or stream-spawners; estimated mixture proportions were within11% of actual proportions averaged over 50 replications. Our datasuggest that Okanagan Lake kokanee constitute at least two managementunits within a single watershed; the ecotypes appear adapted to distinctthermal reproductive environments and show modest moleculardifferentiation from one another. Persistence of kokanee within OkanaganLake may depend, in part, on management plans that recognize thedistinctions between the sympatric reproductive ecotypes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allendorf FW (1983) Isolation, gene flow, and genetic differentiation among populations. In: Genetics and Conservation: A Reference for Managing Wild Animal and Plant Populations (eds. Schonewald-Cox CM, Chambers SM, MacBride B, Thomas WL), pp. 51–65. Benjamin/Cummings, Menlo Park, CA.

    Google Scholar 

  • Allendorf FW, Seeb LW (2000) Concordance of genetic divergence among sockeye salmon populations at allozyme, nuclear DNA, and mitochondrial DNA markers. Evolution, 54, 640–641.

    PubMed  Google Scholar 

  • Ardren WR, Borer S, Thrower F, Joyce JE, Kapuscinski AR (1999) Inheritance of 12 microsatellite loci in Oncorhynchus mykiss. J. Hered., 90, 529–536.

    Google Scholar 

  • Ashley K, Shepherd B, Sabastian D, Thompson L, Matthews S, Vidmanic L, Ward P, Yassien H, McEachern L, Nordin R, Lasenby D, Quirt J, Whall J, Dill P, Taylor E, Pollard S, Wong C, den Dulk J, Scholten G (1998) Okanagan Lake Action Plan Year 1 (1996–97) and Year 2 (1997–98) Report. B.C. Ministry of Fisheries Fish. Project Rpt. RD 73.

  • Ashley K, McGregor B, Shepherd B, Sabastian D, Matthews S, Vidmanic L, Ward P, Yassien H, McEachern L, Andrusak H, Lasenby D, Quirt J,Whall J, Taylor E, Kuiper A, Troffe P,Wong C, Scholten G, Zimmerman M, Epp P, Jensen V, Finnegan R. (1999) Okanagan Lake Action Plan Year 3 (1998) Report. B.C. Ministry of Fisheries Fish. Project Rpt. RD 78.

  • 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 tschawytscha). J. Hered., 90, 281–288.

    Google Scholar 

  • Beacham TD (1988) A genetic analysis of early development in pink (Oncorhynchus gorbuscha) and chum salmon (Oncorhynchus keta) at three different temperatures. Genome, 30, 89–96.

    PubMed  Google Scholar 

  • Beacham TD, Withler FC, Morley RB (1985) Effect of eggs size on incubation time and alevin and fry size in chum salmon (Oncorhynchus keta) and coho salmon (Oncorhynchus kisutch). Can. J. Zool., 63, 847–850.

    Google Scholar 

  • Beacham TD (1988) A genetic analysis of early development in pink (Oncorhynchus gorbuscha) and chum salmon (O. keta) at three different temperatures. Genome, 30, 89–96.

    PubMed  Google Scholar 

  • Beacham TD, Murray CB (1989) Variation in developmental biology of sockeye salmon (Oncorhynchus nerka) and chinook salmon (O. tshawytscha) in British Columbia. Can. J. Zool., 67, 2081–2089.

    Google Scholar 

  • Beacham TD, Margolis, L, Nelson, J (1998) A comparison of methods of stock identification for sockeye salmon (Oncorhynchus nerka) in Barkley Sound, British Columbia. In: Assessment and Status of Pacific Rim Salmonid Stocks (eds.Welch DW, Eggers DM, Wakabayashi K, Karpenko VI), pp. 227–239. North Pac. Anad. Fish Comm. Bull. No. 1.

  • Beacham TD, Wood CC (1999) Application of microsatellite DNA variation to estimation of stock composition and escapement of Nass River sockeye salmon (Oncorhynchus nerka). Can. J. Fish. Aquat. Sci., 56, 297–310.

    Google Scholar 

  • Blair GR, Rogers DE, Quinn TP (1993) Variation in life history characteristics and morphology of sockeye salmon in the Kvichak River system, Bristol Bay, Alaska. Trans. Am. Fish. Soc., 122, 550–559.

    Google Scholar 

  • Bohonak AJ (1999) Dispersal, gene flow, and population structure. Quart. Rev. Biol., 74, 21–45.

    PubMed  Google Scholar 

  • Brannon E (1987) Mechanisms stabilizing salmonid fry emergence timing. In: Sockeye Salmon (Oncorhynchus nerka) Population Biology and Future Management (eds. Smith HD, Margolis L, Wood CC), pp. 120–124. Can. Spec. Publ. Fish. Aquat. Sci., Vol. 96.

  • Burger C, Spearman WJ, Cronin MA (1997) Genetic differentiation of sockeye salmon subpopulations from a geologically young Alaskan lake system. Trans. Am. Fish. Soc., 126, 926–938.

    Google Scholar 

  • Burgner RL (1991) Life history of sockeye salmon (Oncorhynchus nerka) In: Pacific Salmon Life Histories (eds. Groot C, Margolis L), pp. 3–117. Univ. of B.C. Press, Vancouver.

    Google Scholar 

  • Clayton JW (1981) The stock concept and the uncoupling of organismal and molecular evolution. Can. J. Fish. Aquat. Sci., 38, 1515–1522.

    Google Scholar 

  • Cornuet J-M, Piry S, Luikart G, Estoup A, Solignac M (1999) Comparison of methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics, 153, 1989–2000.

    PubMed  Google Scholar 

  • Douglas MR, Brunner PC, Bernatchez L (1998) Do assemblages of Coregonus (Teleostei: Salmoniformes) in the Central Alpine Region of Europe represent species flocks? Mol. Ecol., 7, 589–603.

    Google Scholar 

  • Estoup A, Rousset, 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 (Salmo trutta). Mol. Ecol., 7, 339–354.

    PubMed  Google Scholar 

  • Eyles N, Mullins HT, Hine AC (1991) The seismic stratigraphy of Okanagan Lake, British Columbia: A record of rapid deglaciation in a deep, ‘fjord-lake’ basin. Sedimentary Geol., 73, 13–41.

    Google Scholar 

  • Foote CJ, Wood CC, Withler RE (1989) Biochemical genetic comparison of sockeye salmon and kokanee, the anadromous and non-anadromous forms of Oncorhynchus nerka. Can. J. Fish. Aquat. Sci., 46, 149–158.

    Google Scholar 

  • Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Gen. Res., 66, 95–107.

    Google Scholar 

  • Garant D, Dodson JJ, Bernatchez L (2000) Ecological determinants and temporal stability of within-river population structure in Atlantic salmon (Salmo salar L.). Mol. Ecol., 9, 615–628.

    PubMed  Google Scholar 

  • García de León FJ, Chikhi L, Bonhomme F (1997) Microsatellite polymorphism and population subdivision in natural populations of the European sea bass Dicentrarchus labrax (Linneaus, 1758). Mol. Ecol., 6, 51–62.

    Google Scholar 

  • Goldstein DB, Pollock DD (1997) Launching microsatellites: A review of mutation processes and methods of phylogenetic inference. J. Hered., 88, 335–342.

    PubMed  Google Scholar 

  • Goudet J (1995) FSTAT version 1.2: A computer program to calculate F-statistics. J. Hered., 86, 485–486.

    Google Scholar 

  • Hansen MM, Ruzzante DE, Neilsen EE, Mensberg K-LM (2000) Microsatellite and mitochondrial DNA polymorphism reveals life-hotory dependent interbreeding between hatchery and wild brown trout (Salmo trutta). Mol. Ecol., 9, 583–594.

    PubMed  Google Scholar 

  • Hedrick PW (1995) Gene flow and genetic restoration: The Florida panther as a case study. Conserv. Biol., 9, 996–1002.

    Google Scholar 

  • Hendry AP, Quinn TP, Utter FM (1996) Genetic evidence fo the persistence and divergence of native and introduced sockeye salmon (Oncorhynchus nerka) within Lake Washington, Washington. Can. J. Fish. Aquat. Sci., 53, 823–832.

    Google Scholar 

  • Hendry AP, Quinn TP (1997) Variation in adult life history and morphology among Lake Washington sockeye salmon (Oncorhynchus nerka) populations in relation to habitat features and ancestral affinities. Can. J. Fish. Aquat. Sci., 54, 75–84.

    Google Scholar 

  • Hendry AP, Hensleigh JE, Reisenbichler RR (1998) Incubation temperature, developmental biology, and the divergence of sockeye salmon (Oncorhynchus nerka) within Lake Washington. Can. J. Fish. Aquat. Sci., 55, 1387–1394.

    Google Scholar 

  • Jarne P, Lagoda JL (1996) Microsatellites, from molecules to populations and back. Trends Ecol. Evol., 11, 424–429.

    Google Scholar 

  • Lynch M (1996) A quantitative-genetic perspective on conservation issues. In: Conservation Genetics. Case Histories from Nature (eds. Avise JC, Hamrick JL), pp. 471–501. Chapman & Hall, New York.

    Google Scholar 

  • Luikart G, Allendorf FW, Cornuet J-M, Sherwin WB (1998) Distortion of allele frequency distributions provides a test of recent population bottlenecks. J. Hered. 89, 238–247.

    PubMed  Google Scholar 

  • Morris DB, Richard K, Wright JM (1996) Microsatellites from rainbow trout (Oncorhynchus mykiss) and their use for genetic study of salmonids. Can. J. Fish. Aquat. Sci., 53, 120–126.

    Google Scholar 

  • Murray CB, McPhail JD (1988) Effect of incubation temperature on the development of five species of Pacific salmon (Oncorhynchus) embryos and alevins. Can. J. Zool., 66, 266–273.

    Google Scholar 

  • Murray CB, Rosenau ML, McPhail JD (1989) Reproductive and developmental biology of kokanee from Upper Arrow Lake, British Columbia. Trans. Am. Fish. Soc., 118, 503–509.

    Google Scholar 

  • Nei M, Chakravarti A (1977) Drift variances of Fst and Gst statistics obtained from a finite number of isolated populations. Theor. Pop. Biol., 11, 307–325.

    Google Scholar 

  • Neigel JE (1997) A comparison of alternative strategies for estimating gene flow from genetic markers. Ann. Rev. Ecol. Syst., 28, 105–128.

    Google Scholar 

  • Nelson RJ, Beacham TD (1999) Isolation and cross species ampli-fication of microsatellite DNA useful for study of Pacific salmon. Ani. Genet., 30, 228–229.

    Google Scholar 

  • Nelson JS (1968) Distribution and nonemclature of North American kokanee, Oncorhynchus nerka. J. Fish. Res. Bd. Canada, 25, 409–414.

    Google Scholar 

  • O'Brien SJ (1996) Conservation genetics of the Felidae. In: Conservation Genetics. Case Histories from Nature (eds. Avise JC, Hamrick JL), pp. 50–74. Chapman & Hall, New York.

    Google Scholar 

  • O'Reilly PT, Hamilton L, McConnell L, Wright JM (1996) Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Can. J. Fish. Aquat. Sci., 53, 2292–2298.

    Google Scholar 

  • Pella JJ, Milner GB (1987) Use of genetic marks in stock composition analysis. In: Population Genetics and Fisgery Management (eds. Ryman N, Utter FM), pp. 247–276. University of Washington Press, Seattle.

    Google Scholar 

  • Petkaeu D, Calvert W, Stirling I, Strobeck C, (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol. Ecol., 4, 347–354.

    PubMed  Google Scholar 

  • Paetkau D, Waits LP, Clarkson PL, Craighead L, Strobeck C (1997) An empirical evaluation of genetic distance statistics using microsatellite data from bear (Ursidae) populations. Genetics, 147, 1943–1957.

    PubMed  Google Scholar 

  • Piry S, Luikart G, Cornvet J-M (1999) BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. J. Hered., 90, 502–503.

    Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc. Natl. Acad. Sci. USA, 94, 9197–9221.

    PubMed  Google Scholar 

  • Raymond M, Rousset, F (1995) GENEPOP (version 1.2): Population genetics software for exact tests and ecumenism. J. Hered., 86, 248–249.

    Google Scholar 

  • Rice WR (1989). Analyzing tables of statistical tests. Evolution, 43, 223–225.

    Google Scholar 

  • Rombough PJ (1985) Initial egg weight, time to maximum alevin weight, and optimal ponding times for chinook salmon, Oncorhynchus tshawytscha. Can. J. Fish. Aquat. Sci., 42, 287–291.

    Google Scholar 

  • Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature, 392, 491–494.

    Google Scholar 

  • Schneider S, Kueffer J-M, Roessli D, Excoffier, L (1997) ARLEQUIN Version 1: An Exploratory Population Genetics Software Environment. Genetics and Biometry Laboratory, University of Geneva, Switzerland.

    Google Scholar 

  • Scribner KT, Gust J, Fields RL (1996) Isolation and characterization of novel salmon microsatellite loci: Cross-species amplification and population genetic applications. Can. J. Fish. Aquat. Sci., 53, 833–841.

    Google Scholar 

  • Sebastian DC, Scholten G (1999) Okanagan Lake Kokanee Abundance, Size, and Age Structure Based on Trawl and Acoustic Surveys. Okanagan Lake Action Plan Year 3 (1998) Report. B.C. Ministry of Fisheries Fish. Project Rpt. RD No. 78. pp., 69–79.

  • Shepherd B (1997) Comparison of the Thermal Development Rates of Kokanee and Sockeye. Unpublished Report. B.C. Fish and Wildlife Branch, Penticton, B.C.

    Google Scholar 

  • Slatkin M (1987) Gene flow in natural populations. Ann. Rev. Ecol. Syst., 16, 393–430.

    Google Scholar 

  • Stacey PB, Johnson VA, Taper ML (1997) Migration within metapopulations. The impact upon local population dynamics. In: Metapopulation Dynamics. Ecology, Genetics, and Evolution (eds. Hanski I, Gilpin ME), pp. 267–291. Academic Press, San Diego.

    Google Scholar 

  • Taylor EB, Foote CJ, Wood CC (1996) Molecular genetic evidence for parallel life-history evolution within a Pacific salmon (sockeye salmon and kokanee, Oncorhynchus nerka). Evolution, 50, 401–416.

    Google Scholar 

  • Taylor EB, Harvey S, Pollard S, Volpe J (1997) Postglacial genetic differentiation of reproductive ecotypes of kokanee Oncorhynchus nerka in Okanagan Lake, British Columbia. Mol. Ecol., 6, 503–517.

    PubMed  Google Scholar 

  • Tessier N, Bernatchez L (1999) Stability of population structure and genetic diversity across generations assessed by microsatellites among sympatric populations of landlocked Atlantic salmon Salmo salar L.). Mol. Ecol., 8, 169–180.

    Google Scholar 

  • Utter FM, Seeb, JE Seeb LW(1993) Complementary uses of ecological and biochemical genetic data in identifying and conserving salmon populations. Fish. Res., 18, 59–76.

    Google Scholar 

  • Waples RS (1991) Pacific salmon, Oncorhynchus spp., and the definition of 'species’ under the Endangered Species Act. Mar. Fish. Rev., 53, 11–22.

    Google Scholar 

  • Waples RS, Teal DJ (1990) Conservation genetics of Pacific salmon. I. Temporal changes in allele frequency. Cons. Biol., 4, 144–156.

    Google Scholar 

  • Wood CC (1995) Life history variation and population structure in sockeye salmon. Am. Fish. Soc. Symp., 17, 195–216.

    Google Scholar 

  • Wood CC, Foote CJ (1990) Genetic differences in the early development and growth of sympatric sockeye salmon and kokanee (Oncorhynchus nerka) and their hybrids. Can. J. Fish. Aquat. Sci., 47, 2250–2260.

    Google Scholar 

  • Wood CC, Foote CJ (1996) Genetic differentiation of sympatric anadromous and non-anadromous morphs of sockeye salmon (Oncorhynchus nerka). Evolution, 50, 1265–1279.

    Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics, 16, 97–159.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eric B. Taylor.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Taylor, E.B., Kuiper, A., Troffe, P. et al. Variation in developmental biology and microsatellite DNA in reproductive ecotypes of kokanee, Oncorhynchus nerka: Implications for declining populations in a large British Columbia lake. Conservation Genetics 1, 231–249 (2000). https://doi.org/10.1023/A:1011553705015

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1011553705015

Navigation