Conservation Genetics

, Volume 8, Issue 3, pp 527–546 | Cite as

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

  • Dylan J. Fraser
  • Matthew W. Jones
  • Tara L. McParland
  • Jeffrey A. Hutchings
Original Paper


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.


Rehabilitation Recolonization Reintroduction Atlantic salmon Metapopulation Asymmetric gene flow Effective population size Temporal stability Genetic compensation Effective-census size ratio 


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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.


  1. Adkison MD (1995) Population differentiation in Pacific salmon: local adaptation, genetic drift, or the environment? Can J Fish Aquat Sci 52:2762–2777Google Scholar
  2. 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 1667:1–8Google Scholar
  3. Amiro PG (2003) Population status of Inner Bay of Fundy Atlantic salmon (Salmo salar), to 1999. Can Tech Rep Fish Aquat Sci 2488:44Google Scholar
  4. 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 15:143–159Google Scholar
  5. Ardlie KG, Kruglyak L, Seielstadt M (2002) Patterns of linkage disequilibrium in the human genome. Nature Rev Genet 3:299–309CrossRefGoogle Scholar
  6. Ardren WR, Kapuscinski AR (2003) Demographic and genetic estimates of effective population size (N e) reveals genetic compensation in steelhead trout. Mol Ecol 12:35–49PubMedCrossRefGoogle Scholar
  7. 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, FranceGoogle Scholar
  8. 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 31:101–106Google Scholar
  9. 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, OttawaGoogle Scholar
  10. 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 6:823–842Google Scholar
  11. Cooper AB, Mangel M (1999) The dangers of ignoring metapopulation structure for the conservation of salmonids. Fish Bull 97:213–226Google Scholar
  12. Cornuet J-M, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  13. 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 153:1989–2000PubMedGoogle Scholar
  14. Crow JF, Kimura M (1970) An introduction to population genetics theory. Burgess Publication CoGoogle Scholar
  15. 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 ServiceGoogle Scholar
  16. Department of Fisheries and Oceans (DFO) (2002) Atlantic salmon Maritimes Provinces Overview for 2002. Stock Status Report 2002/026, Department of Fisheries and OceansGoogle Scholar
  17. 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 91:3166–3170PubMedCrossRefGoogle Scholar
  18. Ellegren H (2000) Heterogeneous mutation processes in human microsatellite DNA sequences. Nature Gen 24:400–402CrossRefGoogle Scholar
  19. 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 5:797–812CrossRefGoogle Scholar
  20. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, UKGoogle Scholar
  21. 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 135–149Google Scholar
  22. 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 13:67–80PubMedCrossRefGoogle Scholar
  23. Fraser DJ, Bernatchez L (2005) Adaptive migratory divergence among sympatric brook charr populations. Evolution 59:611–624PubMedCrossRefGoogle Scholar
  24. Fundy National Park (FNP) (2002) Juvenile Atlantic salmon densities, 1983–2002, Fundy National Park. Monitoring project data summaryGoogle Scholar
  25. 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 ScotiaGoogle Scholar
  26. 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 ScotiaGoogle Scholar
  27. 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, LausanneGoogle Scholar
  28. 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 11:2523–2535PubMedCrossRefGoogle Scholar
  29. Hanski I, Gaggiotti O (2004) Ecology, evolution and genetics of metapopulations. Academic Press, San Diego, California USAGoogle Scholar
  30. 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 11:197–214PubMedCrossRefGoogle Scholar
  31. 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 165–181Google Scholar
  32. Hoffman EA, Scheuler FW, Blouin MS (2004) Effective population sizes and temporal stability of genetic structure in Rana pipiens, the northern leopard frog. Evolution 58:2536–2545PubMedCrossRefGoogle Scholar
  33. 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, ScotiaGoogle Scholar
  34. 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 33:829–833Google Scholar
  35. Jessop BM (1986) Atlantic salmon (Salmo salar) of the Big Salmon River, New Brunswick. Canadian Technical Report in Fisheries and Aquatic Sciences #1415Google Scholar
  36. 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, CanadaGoogle Scholar
  37. 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 86:675–684PubMedCrossRefGoogle Scholar
  38. Jones MW, Hutchings JA (2002) Individual variation in Atlantic salmon fertilization success: implications for effective population size. Ecol Appl 12:184–193CrossRefGoogle Scholar
  39. Kalinowski ST (2002) Evolutionary and statistical properties of three genetic distances. Mol Ecol 11:1263–1273PubMedCrossRefGoogle Scholar
  40. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241Google Scholar
  41. 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 10:807–821PubMedCrossRefGoogle Scholar
  42. 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 59:1116–1131CrossRefGoogle Scholar
  43. Koskinen M, Haugen T, Primmer C (2002) Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:826–830PubMedCrossRefGoogle Scholar
  44. Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460PubMedCrossRefGoogle Scholar
  45. Langella O (2001) Centre National de la Recherche Scientifique, Laboratoire Populations, Génétique et Evolution, Gif sur Yvettev;
  46. 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 6:981–997CrossRefGoogle Scholar
  47. Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11:2445–2449PubMedCrossRefGoogle Scholar
  48. McVean GAT (2002) A genealogical interpretation of linkage disequilibrium. Genetics 162:987–991PubMedGoogle Scholar
  49. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  50. Nunney L (1999) The effective size of a hierarchically-structured population. Evolution 53:1–10CrossRefGoogle Scholar
  51. Ohta T (1982) Linkage disequilibrium with the island model. Genetics 101:139–155PubMedGoogle Scholar
  52. 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, OttawaGoogle Scholar
  53. 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 ScotiaGoogle Scholar
  54. 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 53:2292–2298CrossRefGoogle Scholar
  55. 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 12:3123–3135PubMedCrossRefGoogle Scholar
  56. Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comp Appl Biosci 12:357–358PubMedGoogle Scholar
  57. 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 BrunswickGoogle Scholar
  58. 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 90:502–503CrossRefGoogle Scholar
  59. Policansky D, Magnuson JJ (1998) Genetics, metapopulations, and ecosystem management of fisheries. Ecol Appl 8:S119–S123CrossRefGoogle Scholar
  60. Raymond M, Rousset F (1995) GENEPOP (3.3): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  61. Reznick DN, Bryga H, Endler JA (1990) Experimentally-induced life history variation in a natural population. Nature 346:357–359CrossRefGoogle Scholar
  62. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  63. Rieman BE, Dunham JB (2000) Metapopulations and salmonids: a synthesis of life history patterns and empirical observations. Ecol Fresh Fish 9:51–64CrossRefGoogle Scholar
  64. 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 55:1–14CrossRefGoogle Scholar
  65. Ryman N, Jorde PE (2001) Statistical power when testing for genetic differentiation. Mol Ecol 10:2361–2373PubMedCrossRefGoogle Scholar
  66. Shrimpton JM, Heath DD (2003) Census vs. effective population size in chinook salmon: large and small-scale environmental perturbation effects. Mol Ecol 12:2571–2583PubMedCrossRefGoogle Scholar
  67. Shriver MD, Jin L, Chakraborty R, Boerwinkle E (1993) VNTR allele frequency distributions under the stepwise mutation approach: a computer simulation approach. Genetics 134:983–993PubMedGoogle Scholar
  68. 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 12:2073–2085PubMedCrossRefGoogle Scholar
  69. 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 26:217–232CrossRefGoogle Scholar
  70. Wang J (2001) A pseudo-likelihood method for estimating effective population size from temporally placed samples. Genet Res 78:243–257PubMedCrossRefGoogle Scholar
  71. Wang J, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429–446PubMedGoogle Scholar
  72. Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379–391PubMedGoogle Scholar
  73. Waples RS (1990a) Conservation genetics of Pacific salmon III. Estimating effective population size. J Hered 81:277–289Google Scholar
  74. Waples RS (1990b) Conservation genetics of Pacific Salmon. II. Effective population size and the rate of loss of genetic variability. J Hered 81:267–276Google Scholar
  75. 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 147–168Google Scholar
  76. Waples RS (2002b) The effective size of fluctuating salmon populations. Genetics 161:783–791Google Scholar
  77. Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply?. Mol Ecol 14:3335–3352PubMedCrossRefGoogle Scholar
  78. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  79. Whitlock MC, Barton NH (1997) The effective size of a subdivided population. Genetics 146:427–441PubMedGoogle Scholar
  80. Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562CrossRefGoogle Scholar
  81. Wilson G, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 168:1177–1191Google Scholar
  82. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Dylan J. Fraser
    • 1
  • Matthew W. Jones
    • 1
  • Tara L. McParland
    • 1
  • Jeffrey A. Hutchings
    • 1
  1. 1.Department of BiologyDalhousie UniversityHalifaxCanada

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