Abstract
Large scale harvesting and other anthropogenic activities have caused severe population declines in many commercially important fish populations, but accurate information about census and effective population size is often hard to come by. Available evidence suggests that in marine fishes, effective population size (N e) is often several orders of magnitude smaller than census size, such that intensively harvested populations may be particularly vulnerable to loss of genetic diversity. The European whitefish (Coregonus lavaretus) has a long history of heavy exploitation in the Baltic Sea, and the Finnish commercial catch of the species has been substantially reduced, despite high fishing effort. We investigated the temporal genetic stability of migratory whitefish populations from two Finnish rivers (Tornionjoki and Kiiminkijoki), sampled at least twice between 1981 and 2006, by assaying variability in 21 microsatellite loci. Our results suggest a small, albeit significant (F ST = 0.004; p = 0.008) and temporally stable, degree of differentiation between rivers. However, in contrast to earlier reports, heterochronous runs (ascending groups) from Tornionjoki did not exhibit significant genetic divergence. Bayesian estimates of N e suggest substantial declines from historic levels dating to ca 250 years. Yet despite a probable decrease in census population size over the study period, we detected no significant change in contemporary N e. Within group genetic diversity appeared largely unchanged over this time frame; however, we detected a trend towards decreased differentiation between spawning groups (rivers) since the 1980s. These results are discussed in light of stocking programs and conservation of genetic diversity of natural populations.
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References
Allendorf FW, Ryman N (1987) Genetic management of hatchery stocks. In: Ryman N, Utter F (eds) Population genetics and fisheries management. University of Washington Press, Seattle, pp 141–159
Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622
Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337
Amos W, Hoffman JI, Frodsham A, Zhang L, Best S, Hill AVS (2007) Automated binning of microsatellite alleles: problems and solutions. Mol Ecol Notes 7:10–14
Araki H, Schmid C (2010) Is hatchery stocking a help or harm? Evidence, limitations and future directions in ecological and genetic surveys. Aquaculture 308:S2–S11
Araki H, Ardren WR, Olsen E, Cooper B, Blouin MS (2007) Reproductive success of captive-bred steelhead trout in the wild: evaluation of three hatchery programs in the Hood River. Conserv Biol 21:181–190
Aronsuu K, Huhmarniemi A (2004) Changes in the European whitefish (Coregonus lavaretus L.) population of the Kalajoki—potential consequences of the alterations of fishing patterns in the Gulf of Bothnia. Ann Zool Fenn 41:195–204
Arsan EL, Bartholomew JL (2008) Potential for dissemination of the nonnative salmonid parasite Myxobolus cerebralis in Alaska. J Aquat Anim Health 20:136–149
Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029
Bernatchez L (1996) Caractérisation génétique des formes naines et normales de grand corégone du réservoir Caniapiscau et du Lac Sérigny à l’aide de marqueurs microsatellites. Réseau de suivi environnemental du complexe La Grande. Hydro-Québec, Montréal
Bernatchez L, Dodson JJ, Boivin S (1989) Population bottlenecks—influence on mitochondrial DNA diversity and its effect in coregonine stock discrimination. J Fish Biol 35:233–244
Bninska M (2000) Commercial fisheries versus water quality in lakes with special reference to coregonid management. Fish Manag Ecol 7:105–114
Bohlin T, Sundström LF, Johnsson JI, Höjesjö J, Pettersson J (2002) Density-dependent growth in brown trout: effects of introducing wild and hatchery fish. J Anim Ecol 71:683–692
Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by tag DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20:1004–1006
Cano JM, Shikano T, Kuparinen A, Merilä J (2008) Genetic differentiation, effective population size and gene flow in marine fishes: implications for stock management. J Integr Field Biol 5:1–10
Cavalli-Sforza LI, Edwards AWF (1967) Phylogenetic analysis—models and estimation procedures. Evolution 21:550–570
Chikhi L, Sousa VC, Luisi P, Goossens B, Beaumont MA (2010) The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics 186:983–995
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Cross TF, King J (1983) Genetic effects of hatchery rearing in Atlantic salmon. Aquaculture 33:33–40
El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree Argania spinosa (L) Skeels endemic to Morocco. Theor Appl Genet 92:832–839
Eronen M, Glückert G, Hatakka L, Van De Plassche O, Van Der Plicht J, Rantala P (2001) Rates of Holocene isostatic uplift and relative sea-level lowering of the Baltic in SW Finland based on studies of isolation contacts. Boreas 30:17–30
FAO (1997) Review of the state if the world fisheries resources: marine fisheries. Food and Agriculture Organization of the United Nations (FAO), Marine Resources Service, Fishery Resources Division, Rome
FAO (2009) The state of world fisheries and aquaculture—2008. Food and Agriculture Organization of the United Nations (FAO), Fisheries and Aquaculture Department, Rome
Felsenstein (2005) PHYLIP (Phylogeny Inference Package) (2005) Version 3.6, distributed by the author. Department of Genome Sciences, University of Washington
Frankham R (1995) Effective-population size adult-population size ratios in wildlife: a review. Genet Res 66:95–107
Franklin IR, Frankham R (1998) How large must populations be to retain evolutionary potential? Anim Conserv 1:69–70
Fraser DJ, Hansen MM, Østergaard S, Tessier N, Legault M, Bernatchez L (2007) Comparative estimation of effective population sizes and temporal gene flow in two contrasting population systems. Mol Ecol 16:3866–3889
Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Goudet J (2005) HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186
Hansen MM, Ruzzante DE, Nielsen EE, Bekkevold D, Mensberg KLD (2002) Long-term effective population sizes, temporal stability of genetic composition and potential for local adaptation in anadromous brown trout (Salmo trutta) populations. Mol Ecol 11:2523–2535
Hansen MM, Fraser DJ, Als TD, Mensberg KLD (2008) Reproductive isolation, evolutionary distinctiveness and setting conservation priorities: the case of European lake whitefish and the endangered North Sea houting (Coregonus spp.). BMC Evol Biol 8(1):137
Hauser L, Adcock GJ, Smith PJ, Ramírez JHB, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci USA 99:11742–11747
Hedrick PW, Hedgecock D, Hamelberg S (1995) Effective population-size in winter-run Chinook salmon. Conserv Biol 9:615–624
Hedrick PW, Hedgecock D, Hamelberg S, Croci SJ (2000) The impact of supplementation in winter-run Chinook salmon on effective population size. J Hered 91:112–116
Hill WG (1981) Estimation of effective population-size from data on linkage disequilibrium. Genet Res 38:209–216
Hindar K, Ryman N, Utter F (1991) Genetic effects of cultured fish on natural fish populations. Can J Fish Aquat Sci 48:945–957
Hoarau G, Boon E, Jongma DN, Ferber S, Palsson J, Van der Veer HW, Rijnsdorp AD, Stam WT, Olsen JL (2005) Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.). Proc R Soc B 272:497–503
Hundertmark KJ, Van Daele LJ (2010) Founder effect and bottleneck signatures in an introduced, insular population of elk. Conserv Genet 11:139–147
Hutchings JA (2000) Collapse and recovery of marine fishes. Nature 406:882–885
Hutchings JA, Baum JK (2005) Measuring marine fish biodiversity: temporal changes in abundance, life history and demography. Philos Trans R Soc B 360:315–338
Hutchinson WF, van Oosterhout C, Rogers SI, Carvalho GR (2003) Temporal analysis of archived samples indicates marked genetic changes in declining North Sea cod (Gadus morhua). Proc R Soc Lond B 270:2125–2132
Huusko O, Grotnes P (1988) Population dynamics of the anadromous whitefish, Coregonus lavaretus (L.), of the Kiiminkijoki. Finland. Finn Fish Res 9:245–254
Kitada S, Shishidou H, Sugaya T, Kitakado T, Hamasaki K, Kishino H (2009) Genetic effects of long-term stock enhancement programs. Aquaculture 290:69–79
Laikre L, Schwartz MK, Waples RS, Ryman N (2010) Compromising genetic diversity in the wild: unmonitored large-scale release of plants and animals. Trends Ecol Evol 25:520–529
Larsson LC, Laikre L, André C, Dahlgren TG, Ryman N (2010) Temporally stable genetic structure of heavily exploited Atlantic herring (Clupea harengus) in Swedish waters. Heredity 104:40–51
Leonard JA (2008) Ancient DNA applications for wildlife conservation. Mol Ecol 17:4186–4196
Leskelä A, Jokikokko E, Huhmarniemi A, Siira A, Savolainen H (2004) Stocking results of spray-marked one-summer old anadromous European whitefish in the Gulf of Bothnia. Ann Zool Fenn 41:171–179
Lind EA, Kaukoranta E (1974) Characteristics, population structure and migration of the whitefish, Coregonus lavaretus (L.) in the Oulujoki River. Ichthyol Fenn Bor 4:160–217
McEachern MB, Van Vuren DH, Floyd CH, May B, Eadie JM (2011) Bottlenecks and rescue effects in a fluctuating population of golden-mantled ground squirrels (Spermophilus lateralis). Conserv Genet 12:285–296
Miller LM, Kapuscinski AR (1997) Historical analysis of genetic variation reveals low effective population size in a northern pike (Esox lucius) population. Genetics 147:1249–1258
Murphy HM, Jenkins GP (2010) Observational methods used in marine spatial monitoring of fishes and associated habitats: a review. Mar Freshwater Res 61:236–252
Nielsen EE, Hansen MM (2008) Waking the dead: the value of population genetic analyses of historical samples. Fish Fisher 9:450–461
Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. CABIOS 12:357–358
Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447
Patton JC, Gallaway BJ, Fechhelm RG, Cronin MA (1997) Genetic variation of microsatellite and mitochondrial DNA markers in broad whitefish (Coregonus nasus) in the Colville and Sagavanirktok rivers in northern Alaska. Can J Fish Aquat Sci 54:1548–1556
Peel et al (2004) NEESTIMATOR: software for estimating effective population size, version 1.3. Queensland Government, Department of Primary Industries and Fisheries
Peter BM, Wegmann D, Excoffier L (2010) Distinguishing between population bottleneck and population subdivision by a Bayesian model choice procedure. Mol Ecol 19:4648–4660
Petersson A (1966) Results of whitefish taggings in Norrbotten. Svensk Fisk Tids 75:6–8
Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503
Poulsen NA, Nielsen EE, Schierup MH, Loeschcke V, Grønkjær P (2006) Long-term stability and effective population size in North Sea and Baltic Sea cod (Gadus morhua). Mol Ecol 15:321–331
Quinn TP (1993) A review of homing and straying of wild and hatchery-produced salmon. Fish Res 18:29–44
Raymond M, Rousset F (1995) Genepop (version 1.2): population-genetics software for exact tests and ecumenicism. J Hered 86:248–249
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
RKTL (2010) Official statistics of Finland—agriculture, forestry and fishery. Commercial marine fishery 2009. Finnish Game and Fisheries Research Institute (RKTL), Helsinki
Rogers SM, Marchand MH, Bernatchez L (2004) Isolation, characterization and cross-salmonid amplification of 31 microsatellite loci in the lake whitefish (Coregonus clupeaformis, Mitchill). Mol Ecol Notes 4:89–92
Ruzzante DE, Taggart CT, Doyle RW, Cook D (2001) Stability in the historical pattern of genetic structure of Newfoundland cod (Gadus morhua) despite the catastrophic decline in population size from 1964 to 1994. Conserv Genet 2:257–269
Ryman N, Laikre L (1991) Effects of supportive breeding on the genetically effective population size. Conserv Biol 5:325–329
Ryman N, Utter F, Laikre L (1995) Protection of intraspecific biodiversity of exploited fishes. Rev Fish Biol Fisher 5:417–446
Säisä M, Rönn J, Ahö T, Björklund M, Pasanen P, Koljonen ML (2008) Genetic differentiation among European whitefish ecotypes based on microsatellite data. Hereditas 145:69–83
Sakamoto T, Danzmann RG, Okamoto N, Ferguson MM, Ihssen PE (1999) Linkage analysis of quantitative trait loci associated with spawning time in rainbow trout (Oncorhynchus mykiss). Aquaculture 173:33–43
Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33
Shama LNS, Kubow KB, Jokela J, Robinson CT (2011) Bottlenecks drive temporal and spatial genetic changes in alpine caddisfly metapopulations. BMC Evol Biol 11:278
Storz JF, Beaumont MA (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56:154–166
Taggart JB, Hynes RA, Prodöhl PA, Ferguson A (1992) A simplified protocol for routine total DNA isolation from salmonid fishes. J Fish Biol 40:963–965
Tallmon DA, Gregovich D, Waples RS, Baker CS, Jackson J, Taylor BL, Archer E, Martien KK, Allendorf FW, Schwartz MK (2010) When are genetic methods useful for estimating contemporary abundance and detecting population trends? Mol Ecol Resour 10:684–692
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
Thorstad EB, Økland F, Aarestrup K, Heggberget TG (2008) Factors affecting the within-river spawning migration of Atlantic salmon, with emphasis on human impacts. Rev Fish Biol Fish 18:345–371
Turgeon J, Estoup A, Bernatchez L (1999) Species flock in the North American Great Lakes: molecular ecology of Lake Nipigon ciscoes (Teleostei, Coregonidae, Coregonus). Evolution 53:1857–1871
Turner TF, Wares JP, Gold JR (2002) Genetic effective size is three orders of magnitude smaller than adult census size in an abundant, estuarine-dependent marine fish (Sciaenops ocellatus). Genetics 162:1329–1339
Urho L, Pennanen JT, Koljonen M-L (2010) Fish. In: Rassi P, Hyvärinen E, Juslén A, Mannerkoski I (eds) The 2010 red list of Finnish species. Ministry of the Environment and Finnish Environment Institute, Helsinki, pp 336–343
Utter F (2000) Patterns of subspecific anthropogenic introgression in two salmonid genera. Rev Fish Biol Fisher 10:265–279
Vasemägi A, Gross R, Paaver T, Koljonen ML, Nilsson J (2005) Extensive immigration from compensatory hatchery releases into wild Atlantic salmon population in the Baltic sea: spatio-temporal analysis over 18 years. Heredity 95:76–83
Wandeler P, Hoeck PEA, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends Ecol Evol 22:634–642
Wang JL (2001) A pseudo-likelihood method for estimating effective population size from temporally spaced samples. Genet Res 78:243–257
Wang JL, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429–446
Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379–391
Waples RS (1991) Genetic interactions between hatchery and wild salmonids—lessons from the pacific-northwest. Can J Fish Aquat Sci 48:124–133
Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Mol Ecol 14:3335–3352
Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol. Ecol. Resour. 8:753–756
Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262
Winkler KA, Weiss S (2008) Eighteen new tetranucleotide microsatellite DNA markers for Coregonus lavaretus cloned from an alpine lake population. Mol Ecol Resour 8:1055–1058
Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790
Yue GH, David L, Orban L (2007) Mutation rate and pattern of microsatellites in common carp (Cyprinus carpio L.). Genetica 129:329–331
Acknowledgments
We thank Oili Huusko-Tuohino for historic scale samples from Kiiminkijoki, and Pirkko Söderkultalahti for help in obtaining catch and effort data. Thanks are also due to Marika Karjalainen and Kirsi Kähkönen for assistance in the laboratory. Our research was supported by the Academy of Finland (AK, JM and RJSM through a grant to JM; Academy professorship 134,728) and the Finnish Graduate School in Population Genetics (BP).
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McCairns, R.J.S., Kuparinen, A., Panda, B. et al. Effective size and genetic composition of two exploited, migratory whitefish (Coregonus lavaretus lavaretus) populations. Conserv Genet 13, 1509–1520 (2012). https://doi.org/10.1007/s10592-012-0394-2
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DOI: https://doi.org/10.1007/s10592-012-0394-2