Advertisement

Conservation Genetics

, Volume 19, Issue 6, pp 1487–1503 | Cite as

Characterizing genetic integrity of rear-edge trout populations in the southern Appalachians

  • Kasey C. PreglerEmail author
  • Yoichiro Kanno
  • Daniel Rankin
  • Jason A. Coombs
  • Andrew R. Whiteley
Research Article

Abstract

Vertebrate populations at the periphery of their range can show pronounced genetic drift and isolation, and therefore offer unique challenges for conservation and management. These populations are often candidates for management actions such as translocations that are designed to improve demographic and genetic integrity. This is particularly true of coldwater species like brook trout (Salvelinus fontinalis), whose numbers have declined greatly across its historic range. At the southern margin, remnant wild populations persist in isolated headwater streams, and many have a history of receiving translocated individuals through either stocking of hatchery reared fish, relocation of wild fish, or both during restoration attempts. To determine current genetic integrity and resolve the genetic effects of past management actions for brook trout populations in SC, USA, we genetically assessed all 18 documented remaining brook trout populations along with individuals acquired from six hatcheries with recorded stocking events in SC. Our results indicated that six of the 18 streams showed signs of hatchery admixture (range 57–97%) and restored patches retained genetic signatures from multiple source populations. Populations had among the lowest genetic diversity (min average HE = 0.147) and effective number of breeders (mean Nb = 31.2) estimates observed throughout the native brook trout range. Populations were highly differentiated (mean pair-wise FST = 0.396), and substantial genetic divergence was evident across major river drainages (max pair-wise FST = 0.773). The lowest local genetic diversity and highest genetic differentiation ever reported for this species make its conservation a challenging task, particularly when combined with other threats such as climate change and non-native species. We offer recommendations on managing peripheral populations with depleted genetic characteristics and provide a reference for determining which existing populations will best serve as sources for future translocation efforts aimed at enhancing or restoring wild brook trout genetic integrity.

Keywords

Appalachian mountains Effective population size Genetic drift Admixture Microsatellite Translocation 

Notes

Acknowledgements

This study was financially supported by the Southeast Aquatic Resources Partnership, Trout Unlimited, Duke Energy, and the South Carolina Department of Natural Resources (SC-DNR). We thank a number of SC-DNR fisheries biologists and volunteers who conducted field sampling, as well as the Greenville Water Company for access to field sites. Two anonymous reviewers provided constructive comments that improved an earlier version of this manuscript.

Supplementary material

10592_2018_1116_MOESM1_ESM.docx (1.1 mb)
Supplementary material 1 (DOCX 1177 KB)

References

  1. Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoobiology 5:181–190Google Scholar
  2. Allendorf FW, Phelps SR (1981) Use of allelic frequencies to describe population structure. Can J Fish Aquat Sci 38:1507–1514Google Scholar
  3. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622Google Scholar
  4. Anderson EC, Dunham KK (2008) The influence of family groups on inferences made with the program STRUCTURE. Mol Ecol Resour 8:1219–1229PubMedGoogle Scholar
  5. Angermeier PL, Karr JR (1994) Biological integrity versus biological diversity as policy directives: protecting biotic resources. In: Ecosystem Management. Springer, New York, NY, pp. 264–275Google Scholar
  6. Annett B, Gerlach G, King TL, Whiteley AR (2012) Conservation genetics of remnant coastal brook trout populations at the southern limit of their distribution: population structure and effects of stocking. Trans Am Fish Soc 141:1399–1410Google Scholar
  7. Araki H, Cooper B, Blouin MS (2007) Genetic effects of captive breeding cause a rapid cumulative fitness decline in the wild. Science 318:100–103PubMedGoogle Scholar
  8. Armstrong DP, Seddon PJ (2007) Directions in reintroduction biology. Trends Ecol Evol 23:20–25PubMedGoogle Scholar
  9. Belmar-Lucero S, Wood SLA, Scott S, Harbicht AB, Hutchings JA, Fraser DJ (2012) Concurrent habitat and life history influences on effective/census population size ratios in stream-dwelling brook trout. Ecol Evol 2:562–573PubMedPubMedCentralGoogle Scholar
  10. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188Google Scholar
  11. Bernatchez L, Wilson CC (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Mol Ecol 7:431–452Google Scholar
  12. Bodkin JL, Ballachey BE, Cronin MA, Scribner KT (1999) Population demographics and genetic diversity in remnant and translocated populations of sea otters. Conserv Biol 13:1378–1385Google Scholar
  13. Brichieri-Colombi TA, Moehrenschlager A (2016) Alignment of threat, effort, and perceived success in North American conservation translocations. Conserv Biol 30:1159–1172PubMedGoogle Scholar
  14. Burkhead NM (2012) Extinction rates in North America freshwater fishes, 1900–2010. Bioscience 62:798–808Google Scholar
  15. Cada GF, Loar JM, Sale MJ (1987) Evidence of food limitation of rainbow and brown trout in southern Appalachian soft-water streams. Trans Am Fish Soc 116:692–702Google Scholar
  16. Castric V, Bonney F, Bernatchez L (2001) Landscape structure and hierarchical genetic diversity in the brook charr, Salvelinus fontinalis. Evolution 55:1016–1028PubMedGoogle Scholar
  17. Coombs JA (2010) Reproduction in the wild: the effect of individual life history strategies on population dynamics and persistence. University of Massachusetts Amherst, DissertationGoogle Scholar
  18. Currens KP, Hemmingsen AR, French RA, Buchanan DV, Schreck CB, Li HW (1997) Introgression and susceptibility to disease in a wild population of rainbow trout. N Am J Fish Manag 17:1065–1078Google Scholar
  19. Currie DJ (2001) Projected effects of climate change on patterns of vertebrate and tree species richness in the coterminous United States. Ecosystems 4:216–225Google Scholar
  20. Curry RA, MacNeill WS (2004) Population-level responses to sediment during early life in brook trout. J N Benthol Soc 23:140–150Google Scholar
  21. Danzmann RG, Morgan IIRP, Jones MW, Bernatchez L, Ihssen PE (1998) A major sextet of mitochondrial DNA phylogenetic assemblages extant in eastern North American brook trout (Salvelinus fontinalis): distribution and postglacial dispersal patterns. Can J Zool 76:1300–1318Google Scholar
  22. Davis MB, Shaw RG (2001) Range shifts and adaptive responses to quaternary climate change. Science 292:673–679PubMedGoogle Scholar
  23. Dewald L, Wilzbach MA (1992) Interactions between native brook trout and hatchery brown trout: effects on habitat use, feeding, and growth. Trans Am Fish Soc 121:287–296Google Scholar
  24. Do C, Waples RS, Peel D, Macbeth GM, Tillet BJ, Ovenden JR (2013) NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214PubMedGoogle Scholar
  25. Dudgeon D, Arthington AH, Gessner MO, Kawabata ZI, Knowler DJ, Lévêque C, Naiman RJ, Prieur-Richard AH, Soto D, Stiassny ML, Sullivan CA (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182Google Scholar
  26. Eastern Brook Trout Joint Venture (EBTJV) (2016) Range-wide assessment of brook trout at the catchment scale: a summary of findings. https://www.easternbrooktrout.org. Accessed Jan 2017
  27. Evans DM, Che-Castaldo JP, Crouse D, Davis FW, Epachin-Niell R, Flather CH, Frohlich RK, Goble DD, Li YW, Male TD, Master LL, Moskwik MP, Neel MC, Noon BR, Parmesan C, Schwartz MW, Scott JM, Williams BK (2016) Species recovery in the United States: increasing the effectiveness of the endangered species act. Issues Ecol 20:1–28Google Scholar
  28. Fausch KD, Rieman BE, Dunham JB, Young MK, Peterson DP (2009) Invasion versus isolation: trade-offs in managing native salmonids with barriers to upstream movement. Conserv Biol 23:859–870PubMedGoogle Scholar
  29. Fischer J, Lindenmayer DB (2000) An assessment of the published results of animal translocations. Biol Conserv 96:1–11Google Scholar
  30. Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475PubMedGoogle Scholar
  31. Fraser DJ, Debes PV, Bernatchez L, Hutchings JA, Fraser DJ (2014) Population size, habitat fragmentation, and the nature of adaptive variation in a stream fish. Proc R Soc B 281:1–8Google Scholar
  32. Gozlan RE, Britton JR, Cowx I, Copp GH (2010) Current knowledge on non-native freshwater fish introductions. J Fish Biol 76:751–786Google Scholar
  33. Griffith B, Scott MJ, Carpenter JW, Reed C (1989) Translocation as a species conservation tool: status and strategy. Science 245:477–480PubMedGoogle Scholar
  34. Guffey SZ (1993) Allozyme genetics of South Carolina brook trout. South Carolina Department of Natural Resources, ColumbiaGoogle Scholar
  35. Haak AL, Williams JE, Neville HM, Dauwalter DC, Colyer WT (2010) Conserving peripheral trout populations: the values and risks of life on the edge. Fisheries 35:530–549Google Scholar
  36. Habera J. Moore S (2005) Managing southern Appalachian brook trout: a position statement. Fisheries 30(7):10–20Google Scholar
  37. Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467PubMedGoogle Scholar
  38. Hayes JP, Guffey SZ, Kriegler FJ, McCracken GF, Parker CR (1996) The genetic diversity of native, stocked, and hybrid populations of brook trout in the southern Appalachians. Conserv Biol 10:1403–1412Google Scholar
  39. Heber S, Varsani A, Kuhn S, Girg A, Kempenaers B, Briskie J (2013) The genetic rescue of two bottlenecked South Island robin populations using translocations of inbred donors. Proc R Soc B 280:1–8Google Scholar
  40. Hedrick PW (1995) Gene flow and genetic restoration: the Florida panther as a case study. Conserv Biol 9:996–1007Google Scholar
  41. Hedrick PW (2005) “Genetic restoration”: a more comprehensive perspective than “genetic rescue”. Trends Ecol Evol 20:109PubMedGoogle Scholar
  42. Hoffmann M, Brooks TM, Butchart SHM, Carpenter KE, Chanson J et al (2010) The impact of conservation on the status of the world’s vertebrates. Science 330:1503–1509PubMedGoogle Scholar
  43. Hoxmeier RJH, Dieterman DJ, Miller LM (2015) Brook trout distribution, genetics and population characteristics in the driftless area of Minnesota. N Am J Fish Manag 35:632–648Google Scholar
  44. 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 Manag 28:1069–1085Google Scholar
  45. Huff DD, Miller LM, Vondracek B (2010) Patterns of ancestry and genetic diversity in reintroduced populations of the slimy sculpin: implications for conservation. Conserv Genet 11:2379–2391Google Scholar
  46. Huff DD, Miller LM, Chizinski CJ, Vondracek B (2011) Mixed-source reintroductions lead to outbreeding depression in second-generation descendants of a native North American fish. Mol Ecol 20:4246–4258PubMedGoogle Scholar
  47. IUCN (1987) IUCN position statement on translocation of living organisms: introductions, re-introductions and re-stocking. IUCN, GlandGoogle Scholar
  48. Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405PubMedPubMedCentralGoogle Scholar
  49. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BioMed Cent Genet 11(94):1–15Google Scholar
  50. Kanno Y, Vokoun JC, Letcher BH (2011) Fine-scale population structure and riverscape genetics of brook trout (Salvelinus fontinalis) distributed along headwater channel networks. Mol Ecol 20:3711–3729PubMedGoogle Scholar
  51. Kanno Y, Kulp MA, Moore SE (2016) Recovery of native brook trout populations following the eradication of nonnative rainbow trout in southern Appalachian mountains streams. N Am J Fish Manag 36:1325–1335Google Scholar
  52. Kazyak DC, Hilderbrand RH, Keller SR, Colaw MC, Holloway AE, Morgan IIRP, King TL (2015) Spatial structure of morphological and neutral genetic variation in brook trout. Trans Am Fish Soc 144:480–490Google Scholar
  53. Kazyak DC, Rash J, Lubinski BA, King TL (2018) Assessing the impact of stocking northern-origin hatchery brook trout on the genetics of wild populations in North Carolina. Conserv Genet 19:207–219Google Scholar
  54. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649PubMedPubMedCentralGoogle Scholar
  55. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241Google Scholar
  56. Kelson SJ, Kapuscinski AR, Timmins D, Ardren WR (2015) Fine-scale genetic structure of brook trout in a dendritic stream network. Conserv Genet 16:31–42Google Scholar
  57. King TL, Julian SE, Coleman RL, Burnham Curtis MK (2003) Isolation and characterization of novel tri-and tetranucleotide microsatellite DNA markers for Brook trout Salvelinus fontinalis: GenBank submission numbers AY168187, AY168188, AY168189, AY168191, AY168192, AY 168193, AY168194, AY168195, AY168196, AY168197, AY168198, AY168199. https://www.ncbi.nlm.nih.gov/nucleotide/. Accessed Nov 2014
  58. King TL, Eackles MS, Letcher BH (2005) Microsatellite DNA markers for the study of Atlantic salmon (Salmo salar) kinship, population structure, and mixed-fishery analyses. Mol Ecol Notes 5:130–131Google Scholar
  59. Kirchner F, Robert A, Colas B (2006) Modelling the dynamics of introduced populations in the narrow-endemic Centaurea corymbosa: a demo-genetic integration. J Appl Ecol 43:1011–1021Google Scholar
  60. Kriegler FJ, McCracken GF, Habera JW, Strange RJ (1995) Genetic characterization of Tennessee brook trout populations and associated management implications. N Am J Fish Manag 15:804–813Google Scholar
  61. Krueger CC, Menzel BW (1979) Effects of stocking on genetics of wild brook trout populations. Trans Am Fish Soc 108:277–287Google Scholar
  62. Kulp MA, Moore SE (2005) A case history in fishing regulations in Great Smoky Mountains National Park: 1934–2004. N Am J Fish Manag 25:510–524Google Scholar
  63. Laikre L, Schwartz MK, Waples RS, Ryman N, GeM Working Group (2010) Compromising genetic diversity in the wild: unmonitored large-scale release of plants and animals. Trends Ecol Evol 25:520–529PubMedGoogle Scholar
  64. 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 21:2877–2895PubMedGoogle Scholar
  65. Lande R, Barrowclough GF (1987) Effective population size, genetic variation, and their use in population management. In: Soulé ME (ed) Viable populations for conservation. Cambridge University Press, Cambridge, pp 87–123Google Scholar
  66. Larson GL, Moore SE (1985) Encroachment of exotic rainbow trout into stream populations of native brook trout in the southern Appalachian mountains. Trans Am Fish Soc 114:195–203Google Scholar
  67. Lennon RE (1967) Brook trout of Great Smoky Mountains National Park. U.S. Fish and Wildlife Service, Washington, DCGoogle Scholar
  68. Lesica P, Allendorf FW (1995) When are peripheral populations viable for conservation? Conserv Biol 9:753–760Google Scholar
  69. Letcher BH, Coombs JA, Nislow KH (2011) Maintenance of phenotypic variation: repeatability, heritability, and size-dependent processes in a brook trout population. Evol Appl 4:602–615PubMedPubMedCentralGoogle Scholar
  70. Maillett E, Aiken R (2015) Trout fishing in 2011: a demographic description and economic analysis. Addendum to the 2011 nation survey of fishing, hunting and wildlife-associated recreation. United States Fish & Wildlife Service, Washington, DCGoogle Scholar
  71. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Can Res 27:209–220Google Scholar
  72. Marie AD, Bernatchez L, Garant D (2010) Loss of genetic integrity correlates with stocking intensity in brook charr (Salvelinus fontinalis). Mol Ecol 19:2025–2037PubMedGoogle Scholar
  73. McCracken GF, Parker CR, Guffey SZ (1993) Genetic differentiation and hybridization between stocked hatchery and native brook trout in Great Smoky Mountains National Park. Trans Am Fish Soc 122:533–542Google Scholar
  74. Meisner JD (1990) Effect of climatic warming on the southern margins of the native range of brook trout, Salvelinus fontinalis. Can J Fish Aquat Sci 47:1065–1070Google Scholar
  75. Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787Google Scholar
  76. Nathan LR, Kanno Y, Vokoun JC (2017) Population demographics influence genetic responses to fragmentation: a demogenetic assessment of the ‘one migrant per generation’ rule of thumb. Biol Conserv 210:261–272Google Scholar
  77. 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 17:3428–3447PubMedGoogle Scholar
  78. Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet 2:2074–2093Google Scholar
  79. Pavlova A, Beheregaray LB, Coleman R, Gilligan D, Harrisson KA, Ingram BA, Kearns J, Lamb AM, Lintermans M, Lyon J, Nguyen TT, Sasaki M, Tonkin Z, Yen JDL, Sunnucks P (2017) Severe consequences of habitat fragmentation on genetic diversity of an endangered Australian freshwater fish: a call for assisted gene flow. Evol Appl 10:531–550PubMedPubMedCentralGoogle Scholar
  80. Peacock MM, Dochtermann NA (2012) Evolutionary potential but not extinction risk of Lahonton cutthroat trout (Oncorhynchus clarkia henshawi) is associated with stream characteristics. Can J Fish Aquat Sci 69:615–626Google Scholar
  81. Peakall R, Smouse PE (2005) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol 6:288–295Google Scholar
  82. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  83. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  84. Ramasamy RK, Ramasamy S, Bindroo BB, Naik VG (2014) STRUCTURE PLOT: a program for drawing elegant STRUCTURE bar plots in user friendly interface. Springerplus.  https://doi.org/10.1186/2193-1801-3-431 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249Google Scholar
  86. Redford KH, Amato G, Baillie J, Beldomenico P, Bennett EL, Clum N, Cook R, Fonseca G, Hedges S, Launay F, Lieberman S, Mace GM, Murayama A, Putnam A, Robinson JG, Rosenbaum H, Sanderson EW, Stuart SN, Thomas P, Thorbjarnarson J (2011) What does it mean to successfully conserve a (vertebrate) species? BioScience 61:39–48Google Scholar
  87. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109Google Scholar
  88. Robinson ZL, Coombs JA, Hudy M, Nislow KH, Letcher BH, Whiteley AR (2017) Experimental test of genetic rescue in isolated populations of brook trout. Mol Ecol 26:4418–4433PubMedGoogle Scholar
  89. Rodriguez-Ramilo ST, Wang J (2012) The effect of close relatives on unsupervised Bayesian clustering algorithms in population genetic structure analysis. Mol Ecol Resour 12:873–884PubMedGoogle Scholar
  90. Rohde FC, Arndt RG, Foltz JW, Quattro JM (2009) Freshwater fishes of South Carolina. University of South Carolina Press, Columbia, pp 13–28Google Scholar
  91. Ruzzante DE, McCracken GR, Parmelee S, Hill K, Corrigan A, MacMillan J, Walde SJ (2016) Effective number of breeders, effective population size and their relationship with census size in an iteroparous species, Salvelinus fontinalis. R Soc B 283:1–9Google Scholar
  92. Stoneking M, Wagner DJ, Hildebrand AC (1981) Genetic evidence suggesting subspecific differences between northern and southern populations of brook trout (Salvelinus fontinalis). Copeia 4:810–819Google Scholar
  93. Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496PubMedGoogle Scholar
  94. Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979PubMedPubMedCentralGoogle Scholar
  95. Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Mol Ecol 14:3335–3352PubMedGoogle Scholar
  96. Waples RS, Anderson EC (2017) Purging putative siblings from population genetic data sets: a cautionary view. Mol Ecol 26:1211–1224PubMedGoogle Scholar
  97. 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 3:244–262PubMedGoogle Scholar
  98. Weeks AR, Sgro CM, Young AG, Frankham R, Mitchell NJ, Miller KA, Byrne M, Coates DJ, Eldridge MDB, Sunnucks P, Breed MF, James EA, Hoffmann AA (2011) Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evol Appl 4:709–725PubMedPubMedCentralGoogle Scholar
  99. Wenger SJ, Isaak DJ, Luce CH, Neville HM, Fausch KD, Dunham JB, Dauwalter DC, Young MK, Elsner MM, Rieman BE, Hamlet AF, Williams JE (2011) Flow regime, temperature, and biotic interactions drive differential declines of trout species under climate change. Proc Natl Acad Sci 108:14175–14180PubMedGoogle Scholar
  100. Whiteley AR, Hastings K, Wenburg JK, Frissell CA, Martin JC, Allendorf FW (2010) Genetic variation and effective population size in isolated populations of coastal cutthroat trout. Conserv Genet 11:1929–1943Google Scholar
  101. Whiteley AR, Coombs JA, Hudy M, Robinson Z, Nislow KH, Letcher BH (2012) Sampling strategies for estimating brook trout effective population size. Conserv Genet 13:577–593Google Scholar
  102. Whiteley AR, Coombs JA, Hudy M, Robinson Z, Colton AR, Nislow KH (2013) Fragmentation and patch size shape genetic structure of brook trout populations. Can J Fish Aquat Sci 70:678–688Google Scholar
  103. Whiteley AR, Coombs JA, Letcher BH, Nislow KH (2014a) Simulation and empirical analysis of novel sibship-based genetic determination of fish passage. Can J Fish Aquat Sci 71:1667–1679Google Scholar
  104. Whiteley AR, Hudy M, Robinson ZL, Coombs JA, Nislow KH (2014b) Patch-based metrics: a cost effective method for short- and long-term monitoring of EBTJV wild brook trout populations? In: Carline RF, LoSapio C (eds) Wild Trout XI: looking back and moving forward. Wild Trout Symposium, West YellowstoneGoogle Scholar
  105. Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends Ecol Evol 30:42–49PubMedGoogle Scholar
  106. Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354PubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Kasey C. Pregler
    • 1
    • 2
    Email author
  • Yoichiro Kanno
    • 1
    • 2
  • Daniel Rankin
    • 3
  • Jason A. Coombs
    • 4
    • 5
  • Andrew R. Whiteley
    • 6
  1. 1.Department of Forestry and Environmental ConservationClemson UniversityClemsonUSA
  2. 2.Department of Fish, Wildlife, and Conservation BiologyColorado State UniversityFort CollinsUSA
  3. 3.South Carolina Department of Natural ResourcesClemsonUSA
  4. 4.Department of Environmental ConservationUniversity of Massachusetts AmherstAmherstUSA
  5. 5.USDA Forest ServiceNorthern Research Station, University of MassachusettsAmherstUSA
  6. 6.Wildlife Biology Program, Department of Ecosystem and Conservation SciencesUniversity of MontanaMissoulaUSA

Personalised recommendations