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Conservation Genetics

, Volume 16, Issue 5, pp 1209–1223 | Cite as

Influence of stocking history on the population genetic structure of anadromous alewife (Alosa pseudoharengus) in Maine rivers

  • Meghan C. McBride
  • Daniel J. Hasselman
  • Theodore V. Willis
  • Eric P. Palkovacs
  • Paul Bentzen
Research Article

Abstract

Stocking programs have been used extensively to mitigate declines in anadromous fishes, but these programs can have long-term unintended genetic consequences. Stocking can homogenize population structure, impede local adaptation, and hinder the use of genetic stock identification as a fishery management tool. Using 12 microsatellite loci, we evaluate the spatiotemporal genetic structure of 16 anadromous alewife (Alosa pseudoharengus) populations in Maine, USA, to determine whether inter-basin stocking practices have influenced population structure and the genetic diversity of the species in this region. Although, no pre-supplementation samples exist, comparative analyses of stocked and non-stocked populations show that stock transfers have influenced alewife population genetic structure. Genetic isolation by distance (IBD) was non-significant among stocked populations, but significant among non-stocked populations. However, two populations, Dresden Mills and Sewell Pond, appear to have resisted genetic homogenization despite stocking. Non-significant genic and genetic differentiations were broadly distributed among alewife populations. Hierarchical AMOVA indicated highly significant differentiation among temporal replicates within populations, and Bayesian clustering analysis revealed weak population structure. A significant correlation was observed between stocking (time and events) and pairwise \({\text{F}}_{\text{ST}}^{{\prime }}\) among alewife collections, and an analysis of IBD residuals showed a significant decline in the amount of genetic differentiation among populations as the extent of stocking activity increased. These findings call for an increased awareness of evolutionary processes and genetic consequences of restoration activities such as inter-basin stock transfers by fisheries management and conservation practitioners.

Keywords

Stocking Alewife Alosa Genetic structure Fisheries management Ecological restoration 

Notes

Acknowledgments

This research was supported by a Natural Sciences and Engineering Research Council Discovery Grant to P. Bentzen and Department of Interior, US Fish and Wildlife Service Coastal Program Grant (No. 501818G257), Department of Commerce, National Marine Fisheries Service Grant, National Fish and Wildlife Foundation (No. NSN-60365), National Science Foundation Grant (No. EPS-0904155) to Maine EPSCoR at the University of Maine. We thank T. Apgar for assistance with ArcGIS 10.2 in measuring distances among rivers and Maine Department of Marine Resources for access to stocking records and for their assistance in collecting samples.

Supplementary material

10592_2015_733_MOESM1_ESM.docx (391 kb)
Supplementary material 1 (DOCX 391 kb)

References

  1. A’Hara SW, Amouroux P, Argo EE, Avand-Faghih A, Barat A, Barbieri L, Bert TM (2012) Permanent genetic resources added to molecular ecology resources Database 1 Aug–30 Sep 2011. Mol Ecol Resour 12:185–189CrossRefPubMedGoogle Scholar
  2. Araki H, Cooper B, Blouin MS (2007) Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318:100–103CrossRefPubMedGoogle Scholar
  3. ASMFC (Atlantic States Marine Fisheries Commission) (2012) River herring benchmark stock assessment. Vol 1. Stock Assessment Report No. 12-02 of the Atlantic States Marine Fisheries Commission, Washington, DCGoogle Scholar
  4. Atkins CG (1887) The river fisheries of Maine. In: C.G. Goode (ed) The Fisheries and Fishery Industries of the United States, vol. 1, Sect. V. U.S Govt, pp 673–728Google Scholar
  5. Aunins AW, Epifanio JM, Brown BL (2014) Genetic evaluation of supplementation-assisted American shad restoration in the James River, Virginia. Mar Coast Fish 6:127–141CrossRefGoogle Scholar
  6. Beever EA, Mattson B, Germino M, Post Van der Burg M, Bradford J, Brunson M (2014) Successes and challenges of 11 broad-extent conservation programs, from formation to implementation. Conserv Biol 2:302–314CrossRefGoogle Scholar
  7. Belding DL (1920) The preservation of the alewife. Trans Am Fish Soc 49:92–104CrossRefGoogle Scholar
  8. Bentzen P, Paterson I (2005) Genetic analyses of freshwater and anadromous alewife (Alosa pseudoharengus) populations from the St. Croix River, Maine/New Brunswick. Final Report to Maine Rivers 3Google Scholar
  9. Berger J, Cain SL, Cheng E, Dratch P, Ellison K, Francis J, Frost HC, Gende S, Groves C, Karesh WA, Leslie E, Machlis G, Medellin RA, Noss RF, Redford KH, Soukup M, Wilcove D, Zack S (2014) Optimism and challenge for science-based conservation of migratory species in and out of U.S. National Parks. Conserv Pract Policy 28:1–9Google Scholar
  10. Brunner PC, Douglas MR, Bernatchez L (1998) Microsatellite and mitochondrial DNA assessment of population structure and stocking effects in Arctic charr (Salvelinus alpinus) (Teleostei: Salmonidae) from central Alpine lakes. Mol Ecol 7:209–223CrossRefGoogle Scholar
  11. Carlson SM, Quinn TP, Hendry AP (2011) Eco-evolutionary dynamics in Pacific salmon. Heredity 3:438–447CrossRefGoogle Scholar
  12. Crane J (2009) Setting the river free: the removal of the Edwards dam and restoration of the Kennebec river. Water Hist 1:131–148CrossRefGoogle Scholar
  13. Eldridge WH, Naish KA (2007) Long-term effects of translocation and release numbers on fine-scale populations structure among coho salmon (Oncorhynchus mykiss). Mol Ecol 16:2407–2421CrossRefPubMedGoogle Scholar
  14. Eldridge WH, Myers JM, Naish KA (2009) Long-term changes in the fine-scale population structure of coho salmon populations (Onchorhynchus kisutch) subject to extensive supportive breeding. Heredity 103:299–309CrossRefPubMedGoogle Scholar
  15. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  16. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47PubMedCentralGoogle Scholar
  17. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedCentralPubMedGoogle Scholar
  18. Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327CrossRefPubMedGoogle Scholar
  19. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  20. Hall CJ, Jordaan A, Frisk MG (2011) The historic influence of dams on diadromous fish habitat with a focus on river herring and hydrologic longitudinal connectivity. Landsc Ecol 26:95–107CrossRefGoogle Scholar
  21. Hall CJ, Jordaan A, Frisk MG (2012) Centuries of anadromous forage fish loss: consequences for ecosystem connectivity and productivity. Bioscience 62:723–731CrossRefGoogle Scholar
  22. Hansen MM (2002) Estimating the long-term effects of stocking domesticated trout into wild brown trout (Salmo trutta) populations: an approach using microsatellite DNA analysis of historical and contemporary samples. Mol Ecol 11:1003–1015CrossRefPubMedGoogle Scholar
  23. Hansen MM, Nielson EE, Ruzzante DE, Bouza C, Mensbery KLD (2000) Genetic monitoring of supportive breeding in brown trout (Salmo trutta L.), using microsatellite DNA markers. Can J Fish Aquat Sci 57:2130–2139CrossRefGoogle Scholar
  24. Hasselman DJ, Limburg KE (2012) Alosine restoration in the twenty first century: challenging the status quo. Mar Coast Fish 4:174–187CrossRefGoogle Scholar
  25. Hasselman DJ, Bradford RG, Bentzen P (2010) Taking stock: defining populations of American shad (Alosa sapidissima) in Canada using neutral genetic markers. Can J Fish Aquat Sci 67:1021–1039CrossRefGoogle Scholar
  26. Hasselman DJ, Ricard D, Bentzen P (2013) Genetic diversity and differentiation in a wide ranging anadromous fish, American shad (Alosa sapidissima), is correlated with latitude. Mol Ecol 22(6):1558–1573CrossRefPubMedGoogle Scholar
  27. Hasselman DJ, Argo EE, McBride MC, Bentzen P, Schultz TF, Perez-Umphrey AA, Palkovacs EP (2014) Human disturbances causes the formation of hybrid swarm between two naturally sympatric fish species. Mol Ecol 23(5):1137–1152Google Scholar
  28. Havey KA (1961) Restoration of anadromous alewives at Long Pond, Maine. Trans Am Fish Soc 90:281–286CrossRefGoogle Scholar
  29. Hightower JE, Wicker AM, Endres KM (1996) Historical trends in abundance of American shad and river herring in Albermarle Sound, North Carolina. N Am J Fish Manag 16:257–271CrossRefGoogle Scholar
  30. Hilborn R, Quinn TP, Schindler DE, Rogers DE (2003) Biocomplexity and fisheries sustainability. Proc Natl Acad Sci 100:6564–6568CrossRefPubMedCentralPubMedGoogle Scholar
  31. Hindar K, Jonsson B, Ryman N, Staahl G (1991) Genetic relationships among landlocked, resident, and anadromous brown trout, Salmo trutta L. Heredity 66:83–91CrossRefGoogle Scholar
  32. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  33. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806CrossRefPubMedGoogle Scholar
  34. Jones O, Wang J (2009) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555CrossRefPubMedGoogle Scholar
  35. Julian SE, Bartron ML (2007) Microsatellite DNA markers for American shad (Alosa sapidissima) and cross-species amplification within the family Clupeidae. Mol Ecol Notes 7:805–807CrossRefGoogle Scholar
  36. Labbe EM (2012) Influence of stocking history and geography on the population genetics of alewife (Alosa pseudoharengus) in Maine rivers. MSc thesis. University of Southern MaineGoogle Scholar
  37. Laikre L, Schwartz MK, Waples RS, Ryman N, The GeM Working Group (2010) Compromising genetic diversity in the wild: unmonitored large-scale release of plants and animals. Trends Ecol Evol 25:520–529CrossRefPubMedGoogle Scholar
  38. Lamaze FC, Garant D, Bernatchez L (2013) Stocking impacts the expression of candidate genes and physiological condition in introgressed brook charr (Salvelinus fontinalis) populations. Evol Appl 6:393–407CrossRefPubMedCentralPubMedGoogle Scholar
  39. Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE Jr. (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of popualtion differentiation. Conserv Genet 7:295–302CrossRefGoogle Scholar
  40. Lauber TB, Stedman RC, Decker DJ, Knuth BA (2011) Linking knowledge to action in collaborative conservation. Conserv Biol 6:1186–1194CrossRefGoogle Scholar
  41. Leberg P (2008) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11:2445–2449CrossRefGoogle Scholar
  42. Limburg KE, Waldman JR (2009) Dramatic declines in North Atlantic diadromous fishes. Bioscience 59:955–965CrossRefGoogle Scholar
  43. López-Hoffman L, Varady RG, Flessa kw, Balvanera P (2010) Ecosystem services across borders: a framework for transboundary conservation policy. Front Ecol Environ 8:84–91CrossRefGoogle Scholar
  44. Lynch M, O’Hely M (2001) Captive breeding and the genetic fitness of natural populations. Conserv Genet 2:363–378CrossRefGoogle Scholar
  45. Marie AD, Bernatchez L, Garant D (2010) Loss of genetic integrity correlates with stocking intensity in brook charr (Salvelinus fontinalis). Mol Ecol 19:2025–2037CrossRefPubMedGoogle Scholar
  46. McBride MC (2013) Population structure of river herring (Alewife, Alosa pseudoharengus, and Blueback herring, Alosa aestivalis) examined using neutral genetic markers. MSc thesis. Dalhousie UniversityGoogle Scholar
  47. McBride MC, Willis TV, Bradford RG, Bentzen P (2014) Genetic diversity and structure of two hybridizing anadromous fishes (Alosa pseudoharengus, Alosa aestivalis) across the northern portion of their ranges. Conserv Genet 15:1281–1298CrossRefGoogle Scholar
  48. MDEP (Maine Department of Environmental Protection) (2009) January 1, 2009 status reports: hydropower projects in maine, DEPLW0363-2009, and Dam removals in Maine and dams subject to regulated minimum flow releasesGoogle Scholar
  49. MDMR (2009) Operational plan for the restoration of diadromous fishes to the Penobscot River, Maine Department of Marine ResourcesGoogle Scholar
  50. MDMR (2010) Species information: Maine River herring. Retrieved July 2010. http://www.maine.gov/dmr/searunfish/alewife/index.htm
  51. Messieh SN (1977) Population structure and biology of alewives (Alosa pseudoharengus) and blueback herring (A. aestivalis) in the Saint John river, New Brunswick. Environ Biol Fishes 2:195–210CrossRefGoogle Scholar
  52. Moritz CC, Potter S (2013) The importance of an evolutionary perspective in conservation policy planning. Mol Ecol 24:5969–5971CrossRefGoogle Scholar
  53. Neff BD, Garner SR, Pitcher TE (2011) Conservation and enhancement of wild fish populations: preserving genetic quality versus genetic diversity. Can J Fish Aquat Sci 68:1139–1154CrossRefGoogle Scholar
  54. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data, II. Gene frequency data. J Mol Evol 19:153–170CrossRefPubMedGoogle Scholar
  55. Nielson EE, Hansen MM, Batch LA (2001) Looking for a needle in a haystack: discovery of indigenous Atlantic salmon (Salmo salar L.) in stocked populations. Conserv Genet 2:219–232CrossRefGoogle Scholar
  56. Oksanen JF, Blnachet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2013) Package ‘vegan’. http://cran.r-project.org, http://vegan.r-forge.r-project.org/. Accessed June 2014
  57. Palkovacs EP, Dion KB, Post DM, Caccone A (2008) Independent evolutionary origins of landlocked Alewife populations and rapid parallel evolution of phenotypic traits. Mol Ecol 17:582–597CrossRefPubMedGoogle Scholar
  58. Palkovacs EP, Hasselman DJ, Argo EE, Gephard SR, Limburg KE, Post DM, Schultz TF, Willis TV (2014) Combining genetic and demographic information to prioritize conservation efforts for anadromous alewife and blueback herring. Evol Appl 7:212–226CrossRefPubMedCentralPubMedGoogle Scholar
  59. Pearse DE, Martinez E, Garza JC (2011) Disruption of historical patterns of isolation by distance in coastal steelhead. Conserv Genet 12:691–700CrossRefGoogle Scholar
  60. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  61. Quinn TP, Kinnision MT, Unwin MJ (2001) Evolution of Chinook salmon (Onchorynchus tshawytscha) populations in New Zealand: patterns, rate, and process. Genetica 112–113:493–513CrossRefPubMedGoogle Scholar
  62. R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org. Accessed June 2014
  63. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  64. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  65. Rounsefell G, Stringer L (1945) Restoration and management of the New England alewife fisheries with special reference to Maine. Trans Am Fish Soc 73:394–424CrossRefGoogle Scholar
  66. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedCentralPubMedGoogle Scholar
  67. Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefPubMedGoogle Scholar
  68. Schindler DE, Schneuerell MD, Moore JW, Gende SM, Francis TB, Palen WJ (2003) Pacific salmon and the ecology of coastal ecosystems. Front Ecol Environ 1:31–37CrossRefGoogle Scholar
  69. Schindler DE, Hilborn R, Chasco B, Boatright CP, Quinn TP, Rogers LA, Webster MS (2010) Population diversity and the portfolio effect in an exploited species. Nature 465:609–612CrossRefPubMedGoogle Scholar
  70. Scott WB, Crossman EJ (1973) Freshwater fishes of Canada. Bull Fish Res Board Can 184:1–966Google Scholar
  71. Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65CrossRefGoogle Scholar
  72. Takezaki N, Nei M, Tamura K (2010) POPTREE2: software for constructing population trees from allele frequency data and computing other populations statistics with windows Interface. Mol Biol Evol 27:747–752CrossRefPubMedCentralPubMedGoogle Scholar
  73. Vähä JP, Erkinaro J, Niemela E, Primmer CR (2007) Life-history and habitat features influence the within-river genetic structure of Atlantic salmon. Mol Ecol 16:2638–2654CrossRefPubMedGoogle Scholar
  74. 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 Quebec, Canada. Evol Appl 7:625–644CrossRefPubMedCentralPubMedGoogle Scholar
  75. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  76. Ward RD (2006) The importance of identifying spatial population structure in restocking and stock enhancement programmes. Fish Res 80:9–18CrossRefGoogle Scholar
  77. Waters J, Epifanio J, Gunter T, Brown B (2000) Homing behaviour facilitates subtle genetic differentiation among river populations of Alosa sapidissima: microsatellites and mtDNA. J Fish Biol 5:622–636CrossRefGoogle Scholar
  78. Weir B, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  79. Wilcove DS, Wikelski M (2008) Going, going, gone: is animal migration disappearing? PLoS Biol 6:e188CrossRefPubMedCentralPubMedGoogle Scholar
  80. Willis TV (2009) How policy, politics, and science shaped a 25-year conflict over alewife in the St. Croix river, New Brunswick Maine. In: Haro A, Smith KL, Rulifson RA, Moffitt CM, Klauda RJ, Dadswell MJ, Cunjak RA, Cooper JE, Beal KL, Avery TS (eds) Challenges for Diadrmous fishes in a dynamic global environment. American Fisheries Society, Bethesda, pp 739–811Google Scholar
  81. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Meghan C. McBride
    • 1
  • Daniel J. Hasselman
    • 2
  • Theodore V. Willis
    • 3
  • Eric P. Palkovacs
    • 2
  • Paul Bentzen
    • 1
  1. 1.Marine Gene Probe Laboratory, Biology DepartmentDalhousie UniversityHalifaxCanada
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaSanta CruzUSA
  3. 3.Department of Environmental ScienceUniversity of Southern MaineGorhamUSA

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