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Confirmation of a unique and genetically diverse ‘heritage’ strain of brook trout (Salvelinus fontinalis) in a remote Adirondack watershed

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Abstract

In fisheries management, understanding anthropogenic impacts on fish population genetic structure is essential because genetic diversity is a fundamental attribute contributing to a species’ evolutionary capacity. An extended history of supplemental stocking has led to the introgression of genes from non-local, hatchery-reared brook trout (Salvalinus fontinalis) into natural Adirondack populations in the state of New York. Managers have therefore gone to great lengths to protect known or suspected pristine “heritage” populations, but the genetic integrity of most populations is unknown. We used 11 microsatellite loci to examine a putative, but as yet unconfirmed “heritage” population in Dix Pond (Essex County, New York), in an effort to confirm its genetic uniqueness, quantify genetic diversity, and determine the geographic extent of the population. No spatial population structure was found within the Dix Pond/Elk Lake watershed, with minimal signs of introgression from historical stocking. The Dix/Elk population showed allelic richness, and effective population size comparable to the highest diversity heritage population among the four that we used for comparison. These patterns support continued heritage status for the Dix Pond population and recognition of the entire Dix-Elk watershed as habitat for this strain. We conclude this study by discussing how the genetic techniques employed here may help to inform future management decisions associated with the conservation and protection of imperiled populations throughout the globe.

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References

  • Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709

    Article  CAS  PubMed  Google Scholar 

  • Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a F ST-outlier method. BMC Bioinform 9:1

    Article  Google Scholar 

  • Aprahamian MW, Smith KM, McGinnity P, McKelvey S, Taylor J (2003) Restocking of salmonids: opportunities and limitations. Fish Res 62:211–227

    Article  Google Scholar 

  • Aunins AW, Petty JT, King TL, Schilz M, Mazik PM (2015) River mainstem thermal regimes influence population structuring within an appalachian brook trout population. Conserv Genet 16:15–29

    Article  Google Scholar 

  • Baker JP, Gherini SA, Munson RK, Christensen SW, Driscoll CT, Gallagher J, Newton RM, Reckhow KH, Schofield CL (1990) Adirondack lakes survey: an interpretive analysis of fish communities and water chemistry, 1984–1987. Adirondack Lakes Survey Corporation, Ray Brook

    Google Scholar 

  • Bassar RD, Letcher BH, Nislow KH, Whiteley AR (2016) Changes in seasonal climate outpace compensatory density-dependence in eastern brook trout. Global Change Biol 22:577–593

    Article  Google Scholar 

  • Bourret V, O’reilly PT, Carr JW, Berg PR, Bernatchez L (2011) Temporal change in genetic integrity suggests loss of local adaptation in a wild Atlantic salmon (Salmo salar) population following introgression by farmed escapees. Heredity 106:500–510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chadwick JG, Nislow KH, McCormick SD (2015) Thermal onset of cellular and endocrine stress responses correspond to ecological limits in brook trout, an iconic cold-water fish. Conserv Physiol 3:cov017

    Article  PubMed  PubMed Central  Google Scholar 

  • Christie MR, Marine ML, French RA, Waples RS, Blouin MS (2012) Effective size of a wild salmonid population is greatly reduced by hatchery supplementation. Heredity 109:254–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cianfrani C, Satizábal HF, Randin C (2015) A spatial modelling framework for assessing climate change impacts on freshwater ecosystems: response of brown trout (Salmo trutta L.) biomass to warming water temperature. Ecol Model 313:1–12

    Article  Google Scholar 

  • Comte L, Buisson L, Daufresne M, Grenouillet G (2013) Climate-induced changes in the distribution of freshwater fish: observed and predicted trends. Freshw Biol 58:625–639

    Article  Google Scholar 

  • Daniels RA (2011) Legacy of New York State’s Watershed surveys, 1926–1939. Fisheries 36:179–189

    Article  Google Scholar 

  • 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 14:209–214

    Article  CAS  PubMed  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Ehlinger NF (1977a) Selective breeding of trout to furunculosis. N Y Fish Game J 24:25–36

    Google Scholar 

  • Ehlinger NF (1977b) Selective breeding of trout for resistance to furunculosis. NY Fish Game 24:.25–36

    Google Scholar 

  • EPA (2015) Climate Change in the United States: benefits of global action. United States environmental protection agency. Office of atmospheric programs. EPA 430-R-15-001

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Filipe AF, Markovic D, Pletterbauer F, Tissueil C, De Weever A, Schmutz S, Bonada N, Freyhof J (2013) Forecasting fish distribution along stream networks: brown trout (Salmo trutta) in Europe. Diversity Distrib 19:1059–1071

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics, 1st edn. Cambridge University Press, New York

    Book  Google Scholar 

  • Frumhoff PC, McCarthy JJ, Melillo JM, Moser SC, Wuebbles DJ (2007) Confronting climate change in the US Northeast. A report of the northeast climate impacts assessment. Union of Concerned Scientists, Cambridge

    Google Scholar 

  • Garcia de Leaniz C, Fleming IA, Einum S, Verspoor E, Jordan WC, Consuegra S, Aubin-Horth N (2007) A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation. Biol Rev 82:173–211

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www2.unil.ch/popgen/softwares/fstat.htm. Updated from Goudet. 1995. Accessed 6 May 2016

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  CAS  PubMed  Google Scholar 

  • Harbicht AB, Alshamlih M, Wilson CC, Fraser DJ (2014) Anthropogenic and habitat correlates of hybridization between hatchery and wild brook trout. Can J Fish Aquat Sci 71:688–697

    Article  Google Scholar 

  • Harding JS, Benfield EF, Bolstad PV, Helfman GS, Jones EBD (1998) Stream biodiversity: the ghost of land use past. Proc Natl Acad Sci 95:14843–14847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genet Res 38:209–216

    Article  Google Scholar 

  • Hindar K, Ryman N, Utter F (1991) Genetic effects of cultured fish on natural fish populations. Can J Fish Aquat Sci 48:945–957

    Article  Google Scholar 

  • Hudy M, Thieling TM, Gillespie N, Smith EP (2008) Distribution, status, and land use characteristics of subwatersheds within the native range of brook trout in the eastern United States. N Am J Fish Manage 28:1069–1085

    Article  Google Scholar 

  • Isaak DJ, Young MK, Nagel DE, Horan DL, Groce MC (2015) The cold-water climate shield: delineating refugia for preserving salmonid fishes through the 21st century. Global Change Biol 21:2540–2553

    Article  Google Scholar 

  • 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 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Jombart T (2008) adegenet: an R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11(1):94

    Article  PubMed  PubMed Central  Google Scholar 

  • Keller WT (1979) Management of wild and hybrid brook trout in New York lakes, ponds and coastal streams. Report from the bureau of fisheries, division of fish and wildlife. New York State Department of Environmental Conservation, Albany

    Google Scholar 

  • Kelson SJ, Kapuscinski AR, Timmins D, Ardren WR (2015) Fine-scale genetic structure of brook trout in a dendritic stream network. Conserv Genet 16:31–42

    Article  Google Scholar 

  • King TL, Lubinski BA, Burnham-Curtis MK, Stott W, Morgan II RP (2012) Tools for the management and conservation of genetic diversity in brook trout (Salvelinus fontinalis): tri-and tetranucleotide microsatellite markers for the assessment of genetic diversity, phylogeography, and historical demographics. Conserv Genet Resour 4:539–543

    Article  Google Scholar 

  • Kovach RP, Muhlfeld CC, Al-Chokhachy R, Dunham JB, Letcher BH, Kershner JL (2016) Impacts of climatic variation on trout: a global synthesis and path forward. Rev Fish Biol Fish 26:135–151

    Article  Google Scholar 

  • Lachance S, Magnan P (1990) Performance of domestic, hybrid, and wild strains of brook trout, Salvelinus fontinalis, after stocking: the impact of intra-and interspecific competition. Can J Fish Aquat Sci 47:2278–2284

    Article  Google Scholar 

  • Lamaze FC, Sauvage C, Marie A, Garant D, Bernatchez L (2012) Dynamics of introgressive hybridization assessed by SNP population genomics of coding genes in stocked brook charr (Salvelinus fontinalis). Mol Ecol 21:2877–2895

    Article  CAS  PubMed  Google Scholar 

  • 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 6:393–407

    Article  PubMed  Google Scholar 

  • Marie AD, Bernatchez L, Garant D (2012) Environmental factors correlate with hybridization in stocked brook charr (Salvelinus fontinalis). Can J Fish Aquat Sci 69:884–893

  • Mason JW, Brynildson OM, Degurse PE (1967) Comparative survival of wild and domestic strains of brook trout in streams. T Am Fish Soc 96:313–319

    Article  Google Scholar 

  • Moore MV, Pace ML, Mather JR (1997) Potential effects of climate change on freshwater ecosystems of the New England/Mid-Atlantic region. Hydrol Process 2:925–947

    Article  Google Scholar 

  • Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170

  • Neville HM, Bernatchez L (2013) Coding gene single nucleotide polymorphism population genetics of nonnative brook trout: the ghost of introductions past. T Am Fish Soc 142:1215–1231

    Article  CAS  Google Scholar 

  • Newman LE, DuBois RB, Halpern TN (2003) A brook trout rehabilitation plan for Lake Superior. Great Lakes Fishery Commission, Miscellaneous Publication, Ann Arbor

    Google Scholar 

  • Nomura T (2008) Estimation of effective number of breeders from molecular coancestry of single cohort sample. Evol Appl 1:462–474

    Article  PubMed  PubMed Central  Google Scholar 

  • Perkins DL, Krueger CC, May B (1993a) Heritage brook trout in northeastern USA: genetic variability within and among populations. T Am Fish Soc 122:515–532

    Article  Google Scholar 

  • Perkins DL, Krueger CC, May B (1993b) Heritage brook trout project summary report to the New York State department of environmental conservation. Return a gift to wildlife project. 29-19-19, F-02

  • Pilgrim BL, Perry RC, Keefe DG, Perry EA, Dawn Marshall H (2012) Microsatellite variation and genetic structure of brook trout (Salvelinus fontinalis) populations in Labrador and neighboring Atlantic Canada: evidence for ongoing gene flow and dual routes of post-Wisconsinan colonization. Ecol Evol 2:885–898

    Article  PubMed  PubMed Central  Google Scholar 

  • Poplar-Jeffers IO, Petty JT, Anderson JT, Kite SJ, Strager MP, Fortney RH (2009) Culvert replacement and stream habitat restoration: implications from brook trout management in an Appalachian watershed, USA. Restor Ecol 17:404–413

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Wen X, Falush D (2009). Documentation for structure software: version 2.3. Department of Statistics University, Oxford

    Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Roberts JJ, Faush KD, Peterson DP, Hooten MB (2013) Fragmentation and thermal risks from climate change interact to affect persistence of native trout in the Colorado River basin. Global Change Biol 19:1383–1398

    Article  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schofield CL, Keleher C (1996) Comparison of brook trout reproductive success and recruitment in an acidic Adirondack lake following whole lake liming and watershed liming. Biogeochemistry 32:323–337

    Article  CAS  Google Scholar 

  • Schofield CL, Trojnar JR (1980) Aluminum toxicity to brook trout (Salvelinus Fontinalis) in acidified waters. Environ Sci Res Series Pollut Rain 341–366

  • Schreiner DR, Ostazeski JJ, Halpern TN, Geving SA (2006) Fisheries management plan for the Minnesota waters of Lake Superior. Minnesota Department of Natural Resources, St. Paul

    Google Scholar 

  • Stitt BC, Burness G, Burgomaster KA, Currie S, McDermid JL, Wilson CC (2014) Intraspecific variation in thermal tolerance and acclimation capacity in brook trout (Salvelinus fontinalis): physiological implications for climate change*. Physiol Biochem Zool 87:15–29

    Article  PubMed  Google Scholar 

  • Stott W, Quinlan HR, Gorman OT, King TL (2010) Genetic structure and diversity among brook trout from Isle Royale, Lake Nipigon, and three Minnesota tributaries of Lake Superior. N Am J Fish Manage 30:400–411

    Article  Google Scholar 

  • Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tishkoff SA, Reed FA, Friedlaender FR, Ehret C, Ranciaro A, Froment A, Hirbo JB, Awomoyi AA, Bodo JM, Doumbo O, Ibrahim M (2009) The genetic structure and history of Africans and African Americans. Science 324:1035–1044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torterotot JB, Perrier C, Bergeron NE, Bernatchez L (2014) Influence of forest road culverts and waterfalls on the fine-scale distribution of Brook Trout genetic diversity in a boreal watershed. Trans Am Fish Soc 143:1577–1591

    Article  CAS  Google Scholar 

  • 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 7:625–644

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genoty** errors in microsatellite data. Mol Ecol Resour 4:535–538

    Article  Google Scholar 

  • Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci*. Conserv Genet 7:167–184

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Waples RS, Antao T, Luikart G (2014) Effects of overlap** generations on linkage disequilibrium estimates of effective population size. Genetics 197:769–780

    Article  PubMed  PubMed Central  Google Scholar 

  • Warren DR, Robinson JM, Josephson DC (2012) Elevated summer temperatures delay spawning and reduce redd construction for resident brook trout (Salvelinus fontinalis). Global Change Biol 18(6):1804–1811

  • Webster DA, Flick WA (1981) Performance of indigenous, exotic, and hybrid strains of brook trout (Salvelinus fontinalis) in waters of the Adirondack Mountains, New York. Can J Fish Aquat Sci 38:1701–1707

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Wenger SJ, Isaak DJ, Luce CH, Neville HM, Fausch KD, Dunham JB, Dauwalter DC, Young MK, Elsner MM, Rieman BE, Hamlet AF (2011) Flow regime, temperature, and biotic interactions drive differential declines of trout species under climate change. Proc Natl Acad Sci 108:14175–14180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wofford JE, Gresswell RE, Banks MA (2005) Influence of barriers to movement on within-watershed genetic variation of coastal cutthroat trout. Ecol Appl 15:628–637

    Article  Google Scholar 

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Acknowledgements

This research was carried out with IACUC approval (protocol #13008) from the University at Albany—State University of New York. We thank Rich Preall and the NYSDEC for their input and support related to the conception of this project. We thank Mike Sheridan and Elk Lake lodge for allowing us access, and providing us with additional samples. We are grateful to Tim King for sharing genotype data and M. Bartram for providing samples and data that facilitated determination of genotype cross-comparability. Thanks to Harmony Borchardt-Wier for microsatellite genoty** in the Hare Lab. We also thank Mary Katherine Gonder and Gary Kleppel for their helpful comments and input on earlier versions of this work. Funding from the UAlbany foundation through the Biodiversity, Conservation and Policy program helped to support this work.

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Authors and Affiliations

  1. Department of Biological Sciences, University at Albany – State University of New York, Albany, NY, 12222, USA

    Spencer A. Bruce & Matthew W. Mitchell

  2. New York State Museum, 3140 Cultural Education Center, Albany, NY, 12230, USA

    Spencer A. Bruce & Jeremy J. Wright

  3. Department of Natural Resources, Cornell University, Ithaca, NY, 14853, USA

    Matthew P. Hare

  4. Department of Biology, Drexel University, Philadelphia, PA, 19104, USA

    Matthew W. Mitchell

  5. 113 Hill St, Troy, NY, 12180, USA

    Spencer A. Bruce

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  1. Spencer A. Bruce
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Correspondence to Spencer A. Bruce or Matthew P. Hare.

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Bruce, S.A., Hare, M.P., Mitchell, M.W. et al. Confirmation of a unique and genetically diverse ‘heritage’ strain of brook trout (Salvelinus fontinalis) in a remote Adirondack watershed. Conserv Genet 19, 71–83 (2018). https://doi.org/10.1007/s10592-017-1019-6

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