Skip to main content
SpringerLink
Log in

Loss of historical immigration and the unsuccessful rehabilitation of extirpated salmon populations

  • Original Paper
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Comprehensive evaluations of multiple genetic factors are rarely undertaken in rehabilitation attempts of extirpated populations, despite a growing need to address why some rehabilitation projects succeed and others fail. Using temporally-spaced samples of microsatellite DNA, we tested several genetic hypotheses that might explain an unsuccessful attempt to re-establish Atlantic salmon populations (Salmo salar) in two rivers of the inner Bay of Fundy, Canada. Census sizes (N) in both populations plummeted to near zero from initial increases after reintroduction/human-mediated recolonization occurred. Over the same period (1974–1996), both populations were characterized by low or relatively low effective sizes (N e ) and temporally unstable genetic structuring, whereas neighbouring populations, known historically for their significant salmon production, were not. Despite evidence for genetic bottlenecking and continual linkage disequilibrium over time in both populations, neither exhibited detectable inbreeding or a significant loss of allelic diversity or heterozygosity relative to known donor/source populations. Ratios of N e to N also increased with decreasing N in both populations, implying a buffering capacity against losses of genetic diversity at depressed abundances. Most significantly, multiple lines of evidence were consistent with the hypothesis that there has been substantial and recurrent asymmetric migration (migration rate, m) from neighbouring areas into both populations even after initial rehabilitation. This included migration from a historically productive population that became extirpated during the course of rehabilitation efforts, indicating that both populations might have naturally depended on immigration from neighbouring areas for persistence. Our results highlight the value of incorporating temporal genetic data beyond commonly used metrics of neutral genetic diversity (F ST, allelic richness, heterozygosity) to evaluate rehabilitation successes or failures. They also illustrate how the joint evaluation of multiple genetic concerns in rehabilitation attempts, at spatial scales beyond donor and rehabilitated populations, is useful for focusing future rehabilitation efforts.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adkison MD (1995) Population differentiation in Pacific salmon: local adaptation, genetic drift, or the environment? Can J Fish Aquat Sci 52:2762–2777

    Google Scholar 

  • Alexander DR, Galbraith P (1982) A plan to re-establish a natural population of Atlantic salmon in the Point Wolfe River, Fundy National Park. Can Man Rep Fish Aquat Sci 1667:1–8

    Google Scholar 

  • Amiro PG (2003) Population status of Inner Bay of Fundy Atlantic salmon (Salmo salar), to 1999. Can Tech Rep Fish Aquat Sci 2488:44

    Google Scholar 

  • Angers B, Bernatchez L (1998) Combined use of SMM and non-SMM methods to infer fine structure and evolutionary history of closely related brook charr (Salvelinus fontinalis, Salmonidae) populations from microsatellites. Mol Biol Evol 15:143–159

    CAS  Google Scholar 

  • Ardlie KG, Kruglyak L, Seielstadt M (2002) Patterns of linkage disequilibrium in the human genome. Nature Rev Genet 3:299–309

    Article  CAS  Google Scholar 

  • Ardren WR, Kapuscinski AR (2003) Demographic and genetic estimates of effective population size (N e ) reveals genetic compensation in steelhead trout. Mol Ecol 12:35–49

    Article  PubMed  CAS  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2000) GENETIX 4.02, Logiciel Sous Windows Pour la Genetique des Populations. Laboratoire Genome, Populations, Interactions, Université de Montpellier II, Montpellier, France

  • Chebanov NA (1991) The effect of spawner density on spawning success, egg survival, and size structure of the progeny of the sockeye salmon (Oncorhynchus nerka). J Ichthyo 31:101–106

    Google Scholar 

  • COSEWIC (2006) COSEWIC assessment and update status report on Atlantic salmon (Salmo salar) Inner Bay of Fundy populations. Committee of the Status of Endangered Wildlife in Canada, Ottawa

    Google Scholar 

  • Consuegra S, Verspoor E, Knox D, García de Leániz C. (2005) Asymmetric gene flow and the evolutionary maintenance of␣genetic diversity in small, peripheral Atlantic salmon populations. Conserv Genet 6:823–842

    Google Scholar 

  • Cooper AB, Mangel M (1999) The dangers of ignoring metapopulation structure for the conservation of salmonids. Fish Bull 97:213–226

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Crow JF, Kimura M (1970) An introduction to population genetics theory. Burgess Publication Co

  • Dadswell M (1968) Atlantic salmon (Salmo salar) investigations in the Point Wolfe and Upper Salmon Rivers in Fundy National Park. Manuscript Report, Limnology Section, Canadian Wildlife Service

  • Department of Fisheries and Oceans (DFO) (2002) Atlantic salmon Maritimes Provinces Overview for 2002. Stock Status Report 2002/026, Department of Fisheries and Oceans

  • Di Rienzo A, Peterson AC, Garza JC, Values AM, Slatkin M, Freimer NB (1994) Mutational processes of simple sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170

    Article  PubMed  CAS  Google Scholar 

  • Ellegren H (2000) Heterogeneous mutation processes in human microsatellite DNA sequences. Nature Gen 24:400–402

    Article  CAS  Google Scholar 

  • Ford MJ, Teel D, Van Doornik DM, Kuligowski D, Lawson PW (2004) Genetic population structure of central Oregon coast coho salmon (Oncorhynchus kisutch). Conserv Genet 5:797–812

    Article  CAS  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, UK

    Google Scholar 

  • Franklin IR (1980) Evolutionary changes in small populations. In: Soule ME, Wilcox BA (eds) Conservation biology. An evolutionary-ecological perspective. Sinauer Assoc, Sunderland, Massachusetts, pp 135–149

    Google Scholar 

  • Fraser DJ, Lippe C, Bernatchez L (2004) Consequences of unequal effective population size, asymmetric gene flow, and sex-biased dispersal on population structure in brook charr (Salvelinus fontinalis). Mol Ecol 13:67–80

    Article  PubMed  CAS  Google Scholar 

  • Fraser DJ, Bernatchez L (2005) Adaptive migratory divergence among sympatric brook charr populations. Evolution 59:611–624

    Article  PubMed  Google Scholar 

  • Fundy National Park (FNP) (2002) Juvenile Atlantic salmon densities, 1983–2002, Fundy National Park. Monitoring project data summary

  • Gibson AJF, Amiro PG (2003) Abundance of Atlantic salmon (Salmo salar) in the Stewiacke River, Nova Scotia, from 1965–2002. Research document 2002/108, Canadian Science Advisory Secretariat, Department of Fisheries and Oceans, Dartmouth, Nova Scotia

  • Gibson AJF, Bryan J, Amiro PG (2003) Release of hatchery-reared Atlantic salmon into inner Bay of Fundy rivers from 1900–2002. Canadian Data Report of Fisheries and Aquatic Sciences 1123, Department of Fisheries and Oceans, Dartmouth, Nova Scotia

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices, Version 2.9.3. Institut d’Écologie, UniversitÉ de Lausanne, Lausanne

  • 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

    Article  PubMed  Google Scholar 

  • Hanski I, Gaggiotti O (2004) Ecology, evolution and genetics of metapopulations. Academic Press, San Diego, California USA

    Google Scholar 

  • Heath DD, Busch C, Kelly J, Atagi DY (2002) Temporal change in genetic structure and effective population size in steelhead trout (Oncorhynchus mykiss). Mol Ecol 11:197–214

    Article  PubMed  CAS  Google Scholar 

  • Hedrick PW, Gilpin ME (1997) Genetic effective size of a metapopulation. In: Hanski I, Gilpin ME (eds) Metapopulation biology: ecology, genetics and evolution. Academic Press, San Diego, CA, pp 165–181

    Google Scholar 

  • Hoffman EA, Scheuler FW, Blouin MS (2004) Effective population sizes and temporal stability of genetic structure in Rana pipiens, the northern leopard frog. Evolution 58:2536–2545

    Article  PubMed  Google Scholar 

  • Hutchings JA (2003) Development of a population recovery strategy for inner Bay of Fundy Atlantic salmon populations in Fundy National park. Dalhousie University, Halifax Nova, Scotia

    Google Scholar 

  • Jessop BM (1976) Distribution and timing of tag recoveries from native and nonnative Atlantic salmon (Salmo salar) released into the Big Salmon River, New Brunswick. J Fish Res Board Can 33:829–833

    Google Scholar 

  • Jessop BM (1986) Atlantic salmon (Salmo salar) of the Big Salmon River, New Brunswick. Canadian Technical Report in Fisheries and Aquatic Sciences #1415

  • Jones MW, Clay D (1995) Components of Atlantic salmon database in Fundy National Park: 1957–1994.Unpublished manuscript of Parks Canada 93–15, Alma, New Brunswick, Canada

  • Jones MW, Hutchings JA (2001) The influence of male parr body size and mate competition on fertilization success and effective population size in Atlantic salmon. Heredity 86:675–684

    Article  PubMed  CAS  Google Scholar 

  • Jones MW, Hutchings JA (2002) Individual variation in Atlantic salmon fertilization success: implications for effective population size. Ecol Appl 12:184–193

    Article  Google Scholar 

  • Kalinowski ST (2002) Evolutionary and statistical properties of three genetic distances. Mol Ecol 11:1263–1273

    Article  PubMed  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Korman J, Ahrens RMN, Higgins PS, Walters CJ (2002). Effects of observer efficiency, arrival timing, and survey life on estimates of escapement for steelhead trout (Oncorhynchus mykiss) derived from repeat mark-recapture experiments. Can J Fish Aquat Sci 59:1116–1131

    Article  Google Scholar 

  • Koskinen M, Haugen T, Primmer C (2002) Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:826–830

    Article  PubMed  CAS  Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460

    Article  PubMed  CAS  Google Scholar 

  • Langella O (2001) Centre National de la Recherche Scientifique, Laboratoire Populations, Génétique et Evolution, Gif sur Yvettev; http://www.cnrsgif.fr/page/bioinfo/populations

  • Latch EK, Rhodes Jr. OE (2005) The effects of gene flow and population isolation on the genetic structure of reintroduced wild turkey populations: are genetic signatures of source populations maintained?. Conserv Genet 6:981–997

    Article  CAS  Google Scholar 

  • Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11:2445–2449

    Article  PubMed  CAS  Google Scholar 

  • McVean GAT (2002) A genealogical interpretation of linkage disequilibrium. Genetics 162:987–991

    PubMed  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  Google Scholar 

  • Nunney L (1999) The effective size of a hierarchically-structured population. Evolution 53:1–10

    Article  Google Scholar 

  • Ohta T (1982) Linkage disequilibrium with the island model. Genetics 101:139–155

    PubMed  Google Scholar 

  • O’Connell MF, Dempson JB, Mullins CC, Reddin DG, Bourgeois CE, Porter TR, Cochrane NM, Caines D (2002) Status of Atlantic salmon (Salmo salar L.) stocks of insular Newfoundland (SFAs 3–14A), 2001. Canadian Science Advisory Secretariat Research Document 2002/028, Department of Fisheries and Oceans, Ottawa

  • O’Reilly PT (1997) Development of molecular genetic markers in Atlantic salmon (Salmo salar) and an illustration of their application to aquaculture and fisheries. PhD Dissertation, Dalhousie University, Halifax, Nova Scotia

  • O’Reilly PT, Hamilton LC, McConnell SK, 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

    Article  CAS  Google Scholar 

  • Ostergaard S, Hansen MM, Loeschcke V, Nielsen EE (2003) Long-term temporal changes of genetic composition in brown trout (Salmo trutta L.) populations inhabiting an unstable environment. Mol Ecol 12:3123–3135

    Article  PubMed  Google Scholar 

  • Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comp Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Perley MH (1851) Report upon the fisheries of the Bay of Fundy. Her Majesty’s Emigration officer. J House Assembly. Saint John, New Brunswick. Microfilm, Provincial Archives of New Brunswick

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

    Article  Google Scholar 

  • Policansky D, Magnuson JJ (1998) Genetics, metapopulations, and ecosystem management of fisheries. Ecol Appl 8:S119–S123

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (3.3): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reznick DN, Bryga H, Endler JA (1990) Experimentally-induced life history variation in a natural population. Nature 346:357–359

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Rieman BE, Dunham JB (2000) Metapopulations and salmonids: a synthesis of life history patterns and empirical observations. Ecol Fresh Fish 9:51–64

    Article  Google Scholar 

  • Ruzzante DE (1998) A comparison of several measures of genetic distance and population structure with microsatellite data: bias and sampling variance. Can J Fish Aquat Sci 55:1–14

    Article  Google Scholar 

  • Ryman N, Jorde PE (2001) Statistical power when testing for genetic differentiation. Mol Ecol 10:2361–2373

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Shriver MD, Jin L, Chakraborty R, Boerwinkle E (1993) VNTR allele frequency distributions under the stepwise mutation approach: a computer simulation approach. Genetics 134:983–993

    PubMed  CAS  Google Scholar 

  • Tero N, Aspi J, Siikimaki P, Jakalaniemi A, Tuomi J (2003) Genetic structure and gene flow in a metapopulation of an endangered plant species, Silene tatarica. Mol Ecol 12:2073–2085

    Article  PubMed  CAS  Google Scholar 

  • Thurow RF, Peterson JB, Guzevich JW (2006) Utility and validation of day and night snorkel counts for estimating bull trout abundance in first and third order streams. North Am J Fish Manage 26:217–232

    Article  Google Scholar 

  • Wang J (2001) A pseudo-likelihood method for estimating effective population size from temporally placed samples. Genet Res 78:243–257

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429–446

    PubMed  CAS  Google Scholar 

  • Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379–391

    PubMed  CAS  Google Scholar 

  • Waples RS (1990a) Conservation genetics of Pacific salmon III. Estimating effective population size. J Hered 81:277–289

    Google Scholar 

  • Waples RS (1990b) Conservation genetics of Pacific Salmon. II. Effective population size and the rate of loss of genetic variability. J Hered 81:267–276

    Google Scholar 

  • Waples RS (2002a) Definition and estimation of effective population size in the conservation of endangered species. In: Beissinger SR, McCullough DR (eds) Population viability analysis. Univ. Chicago Press, pp 147–168

  • Waples RS (2002b) The effective size of fluctuating salmon populations. Genetics 161:783–791

    Google Scholar 

  • Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply?. Mol Ecol 14:3335–3352

    Article  PubMed  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Whitlock MC, Barton NH (1997) The effective size of a subdivided population. Genetics 146:427–441

    PubMed  CAS  Google Scholar 

  • Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562

    Article  Google Scholar 

  • Wilson G, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 168:1177–1191

    Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank D. Clay for help especially during planning stages and his support during fieldwork. We also thank the following individuals who kindly contributed scale samples or assisted in the collection of samples: G. Sinclair, R. Sutherland and the Fundy National Park Wardens (Fundy National Park); P. Amiro (Department of Fisheries and Oceans (DFO), Halifax), T. Pettigrew (New Brunswick Department of Natural Resources and Energy), J. Mallory (DFO Fredericton), R. Jones (DFO Moncton). Comments from R.S. Waples, A. Calvert and two anonymous reviewers thoroughly improved the quality of the paper. This work was funded by Parks Canada through Science Advisory Board research grants to Fundy National Park, a National Sciences and Engineering Research Council of Canada (NSERC) grant to JAH, and a NSERC Postdoctoral fellowship to DJF.

Author information

Authors and Affiliations

  1. Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada, B3H 1J1

    Dylan J. Fraser, Matthew W. Jones, Tara L. McParland & Jeffrey A. Hutchings

Authors
  1. Dylan J. Fraser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew W. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tara L. McParland
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jeffrey A. Hutchings
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dylan J. Fraser.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fraser, D.J., Jones, M.W., McParland, T.L. et al. Loss of historical immigration and the unsuccessful rehabilitation of extirpated salmon populations. Conserv Genet 8, 527–546 (2007). https://doi.org/10.1007/s10592-006-9188-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-006-9188-8

Keywords

Search

Navigation