Abstract
Freshwater fisheries represent important natural resources, yet a vast majority are threatened by anthropogenic stressors. Accurate baseline information on stock diversity, population history and hatchery representation are required for implementing effective conservation and management strategies for mitigating declines. Genetic tools have played key roles for informing fisheries management, including for kokanee, the freshwater resident form of sockeye salmon (Oncorhynchus nerka), particularly in the southern portion of its North American range. Here, we investigated stock diversity, population history and hatchery representation of kokanee at the northern extent of its range in Canada in Kluane National Park and Reserve (KNPR) in the Yukon that underwent a 12-year population crash followed by a rapid increase in numbers. Using restriction-site associated DNA sequencing, we genotyped individuals at 11,442 single nucleotide polymorphisms (SNPs) that were sampled from putative reproductive ecotypes spawning on the shore of Sockeye Lake (n = 26), within Sockeye Creek (n = 20) or near an outlet in between (n = 2), as well as broodstock from the Whitehorse Rapids Fish Hatchery (n = 29). We found no evidence of ecotype differentiation based on neutral SNPs nor outlier loci. Within-population genetic diversity and effective population size were substantially higher in the wild population relative to the hatchery and significant differentiation was detected, suggesting the hatchery population was not representative of wild stock diversity. Overall, our results indicate that separate management of kokanee in KNPR based on ecotype is not warranted at this time and that supplementation with the existing hatchery stock is not appropriate.
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Availability of data and material
All Illumina raw reads are available from the NCBI sequence read archive (BioProject ID: PRJNA761341); RAD loci sequences and SNP genotypic data are deposited in DRYAD (https://doi.org/10.5061/dryad.ffbg79cvz).
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References
Allendorf FW, Thorgaard GH (1984) Tetraploidy and the evolution of salmonid fishes. In: Evolutionary genetics of fishes. Springer, Berlin, pp 1–53
Allendorf FW, Ryman N, Utter FM (1987) Genetics and fishery management. In: Population genetics and fishery management, pp 1–19
Allendorf FW, Bassham S, Cresko WA, Limborg MT, Seeb LW, Seeb JE (2015) Effects of crossovers between homeologs on inheritance and population genomics in polyploid-derived salmonid fishes. J Hered 106(3):217–227
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410
Anderson JH, Warheit KI, Craig BE, Seamons TR, Haukenes AH (2020) A review of hatchery reform science in Washington State. Washington Department of Fish and Wildlife
Araki H, Cooper B, Blouin MS (2007) Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318(5847):100–103
Barton NH, Charlesworth B (1984) Genetic revolutions, founder effects, and speciation. Annu Rev Ecol Syst 15(1):133–164
Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PloS One 3(10)
Beacham TD, Candy JR, McIntosh B, MacConnachie C, Tabata A, Kaukinen K, et al (2001). Estimation of stock composition of sockeye salmon in the North Pacific Ocean. NPAFC Doc, 783
Beamish RJ, Neville CM, Cass AJ (1997) Production of Fraser River sockeye salmon (Oncorhynchus nerka) in relation to decadal-scale changes in the climate and the ocean. Can J Fish Aquat Sci 54(3):543–554
Begg GA, Friedland KD, Pearce JB (1999) Stock identification and its role in stock assessment and fisheries management: an overview. Fish Res 43(1–3):1–8
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(4):550–559
Buktenica MW, Girdner SF, Larson GL, McIntire CD (2007) Variability of kokanee and rainbow trout food habits, distribution, and population dynamics, in an ultraoligotrophic lake with no manipulative management. Hydrobiologia 574(1):235–264
Camak DT, Osborne MJ, Turner TF (2021) Population genomics and conservation of Gila Trout (Oncorhynchus gilae). Conserv Genet 22:729–743
Carlson AK, Taylor WW, Kinnison MT, Sullivan SMP, Weber MJ, Melstrom RT et al (2019) Threats to freshwater fisheries in the United States: perspectives and investments of state fisheries administrators and agricultural experiment station directors. Fisheries 44(6):276–287
Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: building and genotyping loci de novo from short-read sequences. G3: Genes Genomes Genet 1(3):171–182
Christensen KA, Rondeau EB, Minkley DR, Sakhrani D, Biagi CA, Flores A-M et al (2020) The sockeye salmon genome, transcriptome, and analyses identifying population defining regions of the genome. PLoS ONE 15(10):e0240935
Christie MR, Marine ML, French RA, Blouin MS (2012) Genetic adaptation to captivity can occur in a single generation. Proc Natl Acad Sci 109(1):238–242
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144(4):2001–2014
Cranbrook B, Nelson B (2016) Kootenay Lake Action Plan-2016. The Ministry of Forests, Lands and Natural Resource Operations, Nelson, BC. Prepared by Redfish Consulting Ltd
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA et al (2011) The variant call format and VCFtools. Bioinformatics 27(15):2156–2158
Des Roches S, Pendleton LH, Shapiro B, Palkovacs EP (2021) Conserving intraspecific variation for nature’s contributions to people. Nat Ecol Evol 5(5):574–582
Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14(1):209–214
Eckert C, Samis K, Lougheed S (2008) Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond. Mol Ecol 17(5):1170–1188
Ehrlich PR (1988) The loss of diversity. In: Biodiversity. National Academy of Sciences, National Academies Press, Washington, DC, pp 21–22
Elliott LD, Ward HG, Russello MA (2020) Kokanee–sockeye salmon hybridization leads to intermediate morphology and resident life history: Implications for fisheries management. Can J Fish Aquat Sci 77(2):355–364
Essington TE, Quinn TP, Ewert VE (2000) Intra-and inter-specific competition and the reproductive success of sympatric Pacific salmon. Can J Fish Aquat Sci 57(1):205–213
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620
Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180(2):977–993
Ford MJ (2002) Selection in captivity during supportive breeding may reduce fitness in the wild. Conserv Biol 16(3):815–825
Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17(1):325–333
Frazer K, Russello M (2013) Lack of parallel genetic patterns underlying the repeated ecological divergence of beach and stream-spawning kokanee salmon. J Evol Biol 26(12):2606–2621
Hardie D, David CH, Jeffrey AH (2010) Evolutionary ecology at the extremes of species’ ranges. Environ Rev 18:1–20
Hilborn R (1992) Institutional learning and spawning channels for sockeye salmon (Oncorhynchus nerka). Can J Fish Aquat Sci 49(6):1126–1136
Hohenlohe PA, Amish SJ, Catchen JM, Allendorf FW, Luikart G (2011) Next-generation RAD sequencing identifies thousands of SNPs for assessing hybridization between rainbow and westslope cutthroat trout. Mol Ecol Resour 11:117–122
Holmes B, Stone R (1994) Biologists sort the lessons of fisheries collapse. Science 264(5163):1252
Huntsman BM, Falke JA, Savereide JW, Bennett KE (2017) The role of density-dependent and–independent processes in spawning habitat selection by salmon in an Arctic riverscape. PLoS ONE 12(5):e0177467
Jackson DA (1993) Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74(8):2204–2214
Kimura M, Ohta T (1969) The average number of generations until fixation of a mutant gene in a finite population. Genetics 61(3):763
Kitada S, Kishino H (2006) Lessons learned from Japanese marine finfish stock enhancement programmes. Fish Res 80(1):101–112
Larson WA, Limborg MT, McKinney GJ, Schindler DE, Seeb JE, Seeb LW (2017) Genomic islands of divergence linked to ecotypic variation in sockeye salmon. Mol Ecol 26(2):554–570
Lemay MA, Russello MA (2012) Neutral loci reveal population structure by geography, not ecotype, in Kootenay Lake kokanee. North Am J Fish Manag 32(2):282–291
Lemay MA, Russello MA (2015) Genetic evidence for ecological divergence in kokanee salmon. Mol Ecol 24(4):798–811
Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. ArXiv Preprint ArXiv:1303.3997
Limborg MT, Larson WA, Seeb LW, Seeb JE (2017) Screening of duplicated loci reveals hidden divergence patterns in a complex salmonid genome. Mol Ecol 26(17):4509–4522
Lischer HE, Excoffier L (2012) PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics 28(2):298–299
Litzow MA, Mueter FJ, Urban JD (2013) Rising catch variability preceded historical fisheries collapses in Alaska. Ecol Appl 23(6):1475–1487
Lorenzen K, Leber KM, Blankenship HL (2010) Responsible approach to marine stock enhancement: an update. Rev Fish Sci 18(2):189–210
Luu K, Bazin E, Blum MGB (2017) pcadapt: an R package to perform genome scans for selection based on principal component analysis. Mol Ecol Resour 17(1):67–77
Lynch M, O’hely M (2001) Captive breeding and the genetic fitness of natural populations. Conserv Genet 2(4):363–378
Lynch AJ, Deines A, Nguyen V, Phouthavong K, Taylor W (2016) The social, economic, and environmental importance of inland fish and fisheries. Environ Rev 24(2):115–121
Lyons J, González-Hernández G, Soto-Galera E, Guzmán-Arroyo M (1998) Decline of freshwater fishes and fisheries in selected drainages of West-Central Mexico. Fisheries 23(4):10–18
Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111(3):675–689
Mayr E (1999) Systematics and the origin of species, from the viewpoint of a zoologist. Harvard University Press, Cambridge
McKinney GJ, Waples RK, Seeb LW, Seeb JE (2017) Paralogs are revealed by proportion of heterozygotes and deviations in read ratios in genotyping-by-sequencing data from natural populations. Mol Ecol Resour 17(4):656–669
Meirmans PG (2020) genodive version 3.0: easy-to-use software for the analysis of genetic data of diploids and polyploids. Mol Ecol Resour 20(4):1126–1131
Mobrand LE, Barr J, Blankenship L, Campton DE, Evelyn TT, Flagg TA et al (2005) Hatchery reform in Washington State: principles and emerging issues. Fisheries 30(6):11–23
Moreira AL, Taylor EB (2015) The origin and genetic divergence of “black” kokanee, a novel reproductive ecotype of Oncorhynchus nerka. Can J Fish Aquat Sci 72(10):1584–1595
Mullon C, Fréon P, Cury P (2005) The dynamics of collapse in world fisheries. Fish Fish 6(2):111–120
Myers RA, Mertz G, Bridson JM, Bradford MJ (1998) Simple dynamics underlie sockeye salmon (Oncorhynchus nerka) cycles. Can J Fish Aquat Sci 55(10):2355–2364
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Nichols KM, Kozfkay CC, Narum SR (2016) Genomic signatures among Oncorhynchus nerka ecotypes to inform conservation and management of endangered Sockeye Salmon. Evol Appl 9(10):1285–1300
Peterman RM (1977) A simple mechanism that causes collapsing stability regions in exploited salmonid populations. J Fish Board Can 34(8):1130–1142
Pironon S, Papuga G, Villellas J, Angert AL, García MB, Thompson JD (2017) Geographic variation in genetic and demographic performance: new insights from an old biogeographical paradigm. Biol Rev 92(4):1877–1909
Piry S, Luikart G, Cornuet JM (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90(4):502–503
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
Reid AJ, Carlson AK, Creed IF, Eliason EJ, Gell PA, Johnson PT et al (2019) Emerging threats and persistent conservation challenges for freshwater biodiversity. Biol Rev 94(3):849–873
Riddell B (2004) Pacific salmon resources in central and north coast British Columbia. Pacific Fisheries Resource Conservation Council Vancouver.
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4(1):137–138
Russello MA, Kirk SL, Frazer KK, Askey PJ (2012) Detection of outlier loci and their utility for fisheries management. Evol Appl 5(1):39–52
Satake A, Satake A, Araki H, Araki H (2012) Stocking of captive-bred fish can cause long-term population decline and gene pool replacement: predictions from a population dynamics model incorporating density-dependent mortality. Thyroid Res 5(2):283–296
Scott W, Crossman E (1973) Freshwater fishes of Canada. Bulletin, p 184
Shepherd BG (1999) A case history: the kokanee stocks of Okanagan Lake (vol 15, p 19). Presented at the proceedings of a conference on the biology and management of species and habitats at risk, Kamloops, BC
Stojanova B, Šurinová M, Zeisek V, Münzbergová Z, Pánková H (2020) Low genetic differentiation despite high fragmentation in the endemic serpentinophyte Minuartia smejkalii (M. verna agg., Caryophyllaceae) revealed by RADSeq SNP markers. Conserv Genet 21(2):187–198
Storey J, Base A, Dabney A, Robinson D (2019) Qvalue: Q-value estimation for false discovery rate control. R package version 2.10. 0. 2015.
Taylor EB, Foote CJ, Wood C (1996) Molecular genetic evidence for parallel life-history evolution within a Pacific salmon (sockeye salmon and kokanee, Oncorhynchus nerka). Evolution 50(1):401–416
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(6):503–517
Valiquette E, Perrier C, Thibault I, Bernatchez L (2014) Loss of genetic integrity in wild lake trout populations following stocking: Insights from an exhaustive study of 72 lakes from Québec, Canada. Evol Appl 7(6):625–644
Veale AJ, Russello MA (2017a) An ancient selective sweep linked to reproductive life history evolution in sockeye salmon. Sci Rep 7(1):1–10
Veale AJ, Russello MA (2017b) Genomic changes associated with reproductive and migratory ecotypes in sockeye salmon (Oncorhynchus nerka). Genome Biol Evol 9(10):2921–2939
Vörösmarty CJ, McIntyre PB, Gessner MO, Dudgeon D, Prusevich A, Green P et al (2010) Erratum: global threats to human water security and river biodiversity. Nature 468(7321):334–334
Waples RS (2002) Effective size of fluctuating salmon populations. Genetics 161(2):783–791
Waples RS, Drake J (2004) Risk/benefit considerations for marine stock enhancement: a pacific salmon perspective
Waples RK, Seeb LW, Seeb JE (2016) Linkage mapping with paralogs exposes regions of residual tetrasomic inheritance in chum salmon (Oncorhynchus keta). Mol Ecol Resour 16(1):17–28
Ward HG, Askey PJ, Weir T, Frazer KK, Russello MA (2019) Genetic stock identification reveals that angler harvest is representative of cryptic stock proportions in a high-profile Kokanee fishery. N Am J Fish Manag 39(3):415–425
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6):1358–1370
Welcomme R, Bartley D (1998) Current approaches to the enhancement of fisheries. Fish Manage Ecol 5(5):351–382
Wickstrom R (1982) Creel census, spawning enumeration and other studies of kokanee of the Kathleen drainage, Kluane National Park, Yukon Territory (Canadian Wildlife Service report to Parks Canada). Winnipeg, p 146
Williamson KS, Murdoch AR, Pearsons TN, Ward EJ, Ford MJ (2010) Factors influencing the relative fitness of hatchery and wild spring Chinook salmon (Oncorhynchus tshawytscha) in the Wenatchee River, Washington, USA. Can J Fish Aquat Sci 67(11):1840–1851
Wong C (2017) Status of Ecological Integrity in Kluane National Park and Reserve 2017: Technical Compendium to the State of the Park Report. Whitehorse, Yukon: Parks Canada, p 66
Woodings LN, Murphy NP, Liggins GW, Miller ME, Ballinger GM, Lau SC, Strugnell JM (2021) Population genomics of the Eastern Rock Lobster, Sagmariasus verreauxi, during spawning stock recovery from over-exploitation. ICES J Mar Sci
Acknowledgements
We thank Parks Canada staff for collecting samples from Sockeye Lake in Kluane National Park and Reserve, Lawrence Vano and Warren Kapaniuk at the Whitehorse Rapids Fish Hatchery for providing hatchery samples, Laura Grieve for GIS help in the generation of Figure 1, and Lorne LaRocque for background on the establishment of the Whitehorse Rapids Fish Hatchery population. Computational resources were made available by Compute Canada through the Resources for Research Groups program. Funding for this work was provided by Parks Canada Conservation and Restoration Program agreement # GC-1160 and the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant # RGPIN‐2019‐04621 to MAR.
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Setzke, C., Wong, C. & Russello, M.A. Genome-wide assessment of kokanee salmon stock diversity, population history and hatchery representation at the northern range margin. Conserv Genet 23, 243–253 (2022). https://doi.org/10.1007/s10592-021-01418-2
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DOI: https://doi.org/10.1007/s10592-021-01418-2
Keywords
- Oncorhynchus nerka
- Fisheries
- RADseq
- Hatchery
- Demographic history
- Peripheral population