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Natural re-colonization and admixture of wolves (Canis lupus) in the US Pacific Northwest: challenges for the protection and management of rare and endangered taxa

Heredityvolume 122pages133149 (2019) | Download Citation


Admixture resulting from natural dispersal processes can potentially generate novel phenotypic variation that may facilitate persistence in changing environments or result in the loss of population-specific adaptations. Yet, under the US Endangered Species Act, policy is limited for management of individuals whose ancestry includes a protected taxon; therefore, they are generally not protected under the Act. This issue is exemplified by the recently re-established grey wolves of the Pacific Northwest states of Washington and Oregon, USA. This population was likely founded by two phenotypically and genetically distinct wolf ecotypes: Northern Rocky Mountain (NRM) forest and coastal rainforest. The latter is considered potentially threatened in southeast Alaska and thus the source of migrants may affect plans for their protection. To assess the genetic source of the re-established population, we sequenced a ~ 300 bp portion of the mitochondrial control region and ~ 5 Mbp of the nuclear genome. Genetic analysis revealed that the Washington wolves share ancestry with both wolf ecotypes, whereas the Oregon population shares ancestry with NRM forest wolves only. Using ecological niche modelling, we found that the Pacific Northwest states contain environments suitable for each ecotype, with wolf packs established in both environmental types. Continued migration from coastal rainforest and NRM forest source populations may increase the genetic diversity of the Pacific Northwest population. However, this admixed population challenges traditional management regimes given that admixture occurs between an adaptively distinct ecotype and a more abundant reintroduced interior form. Our results emphasize the need for a more precise US policy to address the general problem of admixture in the management of endangered species, subspecies, and distinct population segments.

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  1. Abbott RJ, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N et al. (2013) Hybridization and speciation. J Evol Biol 26:229–246

  2. Abbott RJ, Barton NH, Good JM (2016) Genomics of hybridization and its evolutionary consequences. Mol Ecol 25:2325–2332

  3. Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664

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

  5. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622

  6. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

  7. Arnold ML (2016) Divergence with Genetic Exchange. Oxford University Press. Oxford, UK

  8. Arnold M, Fogarty N (2009) Reticulate evolution and marine organisms: the final frontier? Int J Mol Sci 10:3836–3860

  9. Bailey V (1936) The mammals and life zones of Oregon. North American Fauna No. 55, 272–275.

  10. Berger KM, Gese EM, Berger J (2008) Indirect effects and traditional trophic cascades: a test involving wolves, coyotes, and pronghorn. Ecology 89:818–828

  11. Blair ME, Sterling EJ, Dusch M, Raxworthy CJ, Pearson RG (2013) Ecological divergence and speciation between lemur (Eulemur) sister species in Madagascar. J Evol Biol 26:1790–1801

  12. Boyd DK, Paquet PC, Donelon S, Ream RR, Pletscher DH, White CC (1995) Ecology and conservation of wolves in a changing world. Canadian Circumpolar Institute. Alberta, CA

  13. Callaghan C (2002). The ecology of gray wolf (Canis lupus) habitat use, survival, and persistence in the Central Rocky Mountains, Canada. Carolyn J. Callaghan.

  14. Carmichael LE, Krizan J, Nagy JA, Fuglei E, Dumond M, Johnson D et al. (2007) Historical and ecological determinants of genetic structure in arctic canids. Mol Ecol 16:3466–3483

  15. Chambers SM, Fain SR, Fazio B, Amaral M (2012) An account of the taxonomy of North American wolves from morphological and genetic analyses. North Am Fauna 77:1–67

  16. Chapron G, Kaczensky P, Linnell JDC, Arx von M, Huber D, Andrén H et al. (2014) Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science 346:1517–1519

  17. Cronin MA, Canovas A, Bannasch DL, Oberbauer AM, Medrano JF (2014) Single nucleotide polymorphism (SNP) variation of wolves (Canis lupus) in Southeast Alaska and comparison with wolves, dogs, and coyotes in North America. J Hered 106:26–36

  18. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA et al. (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158

  19. Darimont CT, Paquet PC (2002) Gray wolves, Canis lupus, of British Columbia's Central and North Coast: distribution and conservation assessment Canadian Field-Naturalist 116:416–422

  20. Darimont CT, Paquet PC, Reimchen TE (2008) Spawning salmon disrupt tight trophic coupling between wolves and ungulate prey in coastal British Columbia. BMC Ecol 8:14

  21. Darimont CT, Reimchen TE, Paquet PC (2003) Foraging behaviour by gray wolves on salmon streams in coastal British Columbia. Can J Zool 81:349–353

  22. DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837

  23. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43:491–498

  24. Diniz-Filho JAF, Bini LM, Rangel TF, Loyola RD, Hof C, Nogués-Bravo D et al. (2009) Partitioning and mapping uncertainties in ensembles of forecasts of species turnover under climate change. Ecography 32:897–906

  25. Dobzhansky T (1935) A critique of the species concept in biology. Philos Sci 2:344–355

  26. Elith J, Graham CH, Anderson RP, Dudík M, Ferrier S, Guisan A et al. (2006) Novel methods improve prediction of species' distributions from occurrence data. Ecography 29:129–151

  27. Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57

  28. Faircloth BC, Glenn TC (2012) Not all sequence tags are created equal: designing and validating sequence identification tags robust to indels. PLoS ONE 7:e42543

  29. Faircloth BC, Sorenson L, Santini F, Alfaro ME (2013) A phylogenomic perspective on the radiation of ray-finned fishes based upon targeted sequencing of ultraconserved elements (UCEs). PLoS ONE 8:e65923

  30. Fourcade Y, Engler JO, Rödder D, Secondi J (2014) Mapping species distributions with MAXENT using a geographically biased sample of presence data: a performance assessment of methods for correcting sampling bias. PLoS ONE 9:e97122

  31. Frankham R, Ballou JD, Ralls K, Dubash MR, Fenster CB, Sunnucks P (2017) Genetic management of fragmented animal and plant populations. Oxford University Press. Oxford, UK

  32. Fredrickson RJ, Siminski P, Woolf M, Hedrick PW (2007) Genetic rescue and inbreeding depression in Mexican wolves. Proc Biol Sci 274:2365–2371

  33. Freedman AH, Gronau I, Schweizer RM, Ortega-Del Vecchyo D, Han E, Silva PM et al. (2014) Genome sequencing highlights the dynamic early history of dogs. PLoS Genet 10:e1004016–12

  34. Fritts SH (1983) Record dispersal by a wolf from Minnesota. J Mammal 64:166–167

  35. Fritts SH, Bangs EE, Fontaine JA, Brewster WG (1995) Restoring wolves to the northern Rocky Mountains of the United States. In: LN Carbyn, SH Fritts, DR Seip (eds) Ecology and conservation of wolves in a changing world. Edmonton, Alberta, p 107–125

  36. Gray MM, Granka JM, Bustamante CD, Sutter NB, Boyko AR, Zhu L et al. (2009) Linkage disequilibrium and demographic history of wild and domestic canids. Genetics 181:1493–1505

  37. Haight RG, Mladenoff DJ, Wydeven AP (1998) Modeling disjunct gray wolf populations in semi‐wild landscapes. Conserv Biol 12:879–888

  38. Hailer F, Leonard JA (2008) Hybridization among three native North American canis species in a region of natural sympatry. PLoS ONE 3:e3333

  39. Harrigan RJ, Thomassen HA, Buermann W, Smith TB (2014) A continental risk assessment of West Nile virus under climate change. Glob Change Biol 20:2417–2425

  40. Harrigan RJ, Thomassen HA, Buermann W, Cummings RF, Kahn ME, Smith TB (2010) Economic conditions predict prevalence of West Nile virus. PLoS ONE 5:e15437

  41. Hedrick PW (2013) Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol Ecol 22:4606–4618

  42. Hendricks SA, Charruau PC, Pollinger JP, Callas R, Figura PJ, Wayne RK (2015) Polyphyletic ancestry of historic gray wolves inhabiting U.S. Pacific states. Conserv Genet 16:759–764

  43. Hendricks S, Epstein B, Schonfeld B, Wiench C, Hamede R, Jones ME et al. (2017) Conservation implications of limited genetic diversity and population structure in Tasmanian devils (Sarcophilus harrisii). Conserv Genet 18:977–982

  44. Hernandez PA, Graham CH, Master LL, Albert DL (2006) The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography 29:773–785

  45. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

  46. Hoffmann AA, Sgrò CM, Kristensen TN (2017) Revisiting adaptive potential, population size, and conservation. Trends Ecol Evol 32:506–517

  47. Hohenlohe PA, Amish SJ, Catchen JM, Allendorf FW, Luikart G (2011) Next‐generation RAD sequencing identifies thousands of SNPs for assessing hybridization between rainbow and westslope cutthroat trout. Mol Ecol Resour 11:117–122

  48. Jackiw RN, Mandil G, Hager HA (2015) A framework to guide the conservation of species hybrids based on ethical and ecological considerations. Conserv Biol 29:1040–1051

  49. Jimenez MD, Bangs EE, Boyd DK, Smith DW, Becker SA, Ausband DE et al. (2017) Wolf dispersal in the Rocky Mountains, Western United States: 1993–2008. J Wild Mgmt 81:581–592

  50. Jordan MI, Ng AY (2002). On discriminative vs. generative classifiers: a comparison of logistic regression and naive bayes. Adv Neural Information Process Syst. 1-8

  51. Koblmüller S, NORD M, Wayne RK, Leonard JA (2009) Origin and status of the Great Lakes wolf. Mol Ecol 18:2313–2326

  52. Kurtz S, Narechania A, Stein JC, Ware D (2008) A new method to compute K-mer frequencies and its application to annotate large repetitive plant genomes. BMC Genomics 9:517

  53. Lehman N, Eisenhawer A, Hansen K, Mech LD, Peterson RO, Gogan PJP et al (1991) Introgression of coyote mitochondrial DNA into sympatric North American gray wolf populations. Evolution 45:104

  54. Leonard JA, Vilà C, Wayne RK (2005) Legacy lost: genetic variability and population size of extirpated US grey wolves (Canis lupus). Mol Ecol 14:9–17

  55. Leonard JA, Wayne RK, Wheeler J, Valadez R, Guillén S, Vilà C (2002) Ancient DNA evidence for Old World origin of New World dogs. Science 298:1613–1616

  56. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

  57. Liberg O, Andrén H, Pedersen H-C, Sand H, Sejberg D, Wabakken P et al. (2005) Severe inbreeding depression in a wild wolf (Canis lupus) population. Biol Lett 1:17–20

  58. Licht DS, Millspaugh JJ, Kunkel KE, Kochanny CO, Peterson RO (2010) Using small populations of wolves for ecosystem restoration and stewardship. Bioscience 60:147–153

  59. Littell JS, Oneil EE, McKenzie D, Hicke JA, Lutz JA (2010) Forest ecosystems, disturbance, and climatic change in Washington State, USA. Clim Change 102:129–158

  60. Love Stowell SM, Pinzone CA, Martin AP (2017) Overcoming barriers to active interventions for genetic diversity. Biodivers Conserv 26:1753–1765

  61. Lv W, Li Z, Wu X, Ni W, Qv W (2011) Maximum entropy niche-based modeling (Maxent) of potential geographical distributions of Lobesia botrana (Lepidoptera: Tortricidae) in China. Paper presented at the International Conference on Computer and Computing Technologies in Agriculture V, Beijing, China, 29–31 October, 2011.

  62. Manichaikul A, Mychaleckyj JC, Rich SS, Daly K, Sale M, Chen W-M (2010) Robust relationship inference in genome-wide association studies. Bioinformatics 26:2867–2873

  63. Mayr E (1947) Systematics and the origin of species. Columbia University Press. New York, USA

  64. Mech LD (1970) The Wolf. American Museum of Natural History by the Natural History Press. New York, USA

  65. Merrill SB, Mech LD (2000) Details of extensive movements by Minnesota wolves (Canis lupus). USGS Northern Prairie Wildlife Research Center, Paper 76.

  66. Mladenoff DJ, Haight RG, Sickley TA, Wydeven AP (1997) Causes and implications of species restoration in altered ecosystems. Bioscience 47:21–31

  67. Mladenoff DJ, Sickley TA (1998) Assessing potential gray wolf restoration in the Northeastern United States: a spatial prediction of favorable habitat and potential population levels. J Wild Mgmt 62:1

  68. Mladenoff DJ, Sickley TA, Haight RG, Wydeven AP (1995) A regional landscape analysis and prediction of favorable gray wolf habitat in the Northern Great Lakes Region. Conserv Biol 9:279–294

  69. Mladenoff DJ, Sickley TA, Wydeven AP (1999) Predicting gray wolf landscape recolonization: logistic regression models vs. new field data. Ecol Appl 9:37–44

  70. Muhlfeld CC, Kalinowski ST, McMahon TE, Taper ML, Painter S, Leary RF et al (2009) Hybridization rapidly reduces fitness of a native trout in the wild. Biol Lett 5:328–331

  71. Muñoz Fuentes V, Darimont CT, Paquet PC, Leonard JA (2010) The genetic legacy of extirpation and re-colonization in Vancouver Island wolves. Conserv Genet 11:547–556

  72. Muñoz Fuentes V, Darimont CT, Wayne RK, Paquet PC, Leonard JA (2009) Ecological factors drive differentiation in wolves from British Columbia. J Biogeogr 36:1516–1531

  73. Muscarella R, Galante PJ, Soley Guardia M, Boria RA, Kass JM, Uriarte M et al. (2014) ENMeval: an R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods Ecol Evol 5:1198–1205

  74. Paquet PC, Alexander SM, Swan PL, Darimont CT (2006) The influence of natural landscape fragmentation and resource availability on connectivity and distribution of marine gray wolf (Canis lupus) populations on Central Coast, BC. Page 726. In: Crooks K, Sanjayan MA (eds) Connectivity Conservation. Cambridge University Press. Cambridge, UK

  75. Paquet PC, Wierczhowski J, Callaghan C (1996) Summary report on the effects of human activity on gray wolves in the Bow River Valley, Banff National Park, Alberta. Pages 74– 120. In: Green J., Pacas, C, Bayley, S, and Cornwell, L (eds) A cumulative effects assessment and futures outlook for the Banff Bow Valley. Department of Canadian Heritage, Ottawa, CA

  76. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Modell 190:231–259

  77. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909

  78. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575

  79. Räikkönen J, Vucetich JA, Peterson RO, Nelson MP (2009) Congenital bone deformities and the inbred wolves (Canis lupus) of Isle Royale. Biol Conserv 142:1025–1031

  80. Rhymer J, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

  81. Ripple WJ, Beschta RL, Painter LE (2015) Trophic cascades from wolves to alders in Yellowstone. For Ecol Manag 354:254–260

  82. Rodríguez Soto C, Monroy Vilchis O, Maiorano L, Boitani L, Faller JC, Briones MÁ et al. (2011) Predicting potential distribution of the jaguar (Panthera onca) in Mexico: identification of priority areas for conservation. Divers Distrib 17:350–361

  83. Roy MS, Geffen E, Smith D, Ostrander EA, Wayne RK (1994) Patterns of differentiation and hybridization in North American wolflike canids, revealed by analysis of microsatellite loci. Mol Biol Evol 11:553–570

  84. Rödder D, Schmidtlein S, Veith M, Lötters S (2009) Alien invasive slider turtle in unpredicted habitat: a matter of niche shift or of predictors studied? PLoS ONE 4:e7843

  85. Rutledge LY, Patterson BR, Mills KJ, Loveless KM, Murray DL, White BN (2010) Protection from harvesting restores the natural social structure of eastern wolf packs. Biol Conserv 143:332–339

  86. Schweizer RM, Durvasula A, Smith J, Vohr SH, Stahler DR, Galaverni M, Thalmann O, Smith D, Randi E, Ostrander EA, Lohmueller K, Green RE, Novembre J, Wayne RK (2018) Natural selection and origin of a melanistic allele in North American gray wolves. Mol Biol Evol.

  87. Schweizer RM, Robinson JA, Harrigan RJ, Silva P, Galverni M, Musiani M et al. (2016a) Targeted capture and resequencing of 1040 genes reveal environmentally driven functional variation in grey wolves. Mol Ecol 25:357–379

  88. Schweizer RM, vonHoldt BM, Harrigan RJ, Knowles JC, Musiani M, Coltman D et al. (2016b) Genetic subdivision and candidate genes under selection in North American grey wolves. Mol Ecol 25:380–402

  89. Sesink Clee PR, Abwe EE, Ambahe RD, Anthony NM, Fotso R, Locatelli S et al. (2015) Chimpanzee population structure in Cameroon and Nigeria is associated with habitat variation that may be lost under climate change. BMC Evol Biol 15:2

  90. Shafer ABA, Wolf JBW, Alves PC, Bergström L, Bruford MW, Brännström I et al. (2015) Genomics and the challenging translation into conservation practice. Trends Ecol Evol 30(2):78–87.

  91. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15:1034–1050

  92. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

  93. Smith D, Meier T, Geffen E, Mech LD, Burch JW, Adams LG et al. (1997a) Is incest common in gray wolf packs? Behav Ecol 8:384–391

  94. Smith DW, Peterson RO, Houston D (2003) Yellowstone after wolves. Bioscience 53:330–340

  95. Smith TB, Wayne RK, Girman DJ, Bruford MW. (1997b) A role for ecotones in generating rainforest biodiversity. Science 276:1855–1857

  96. Staples J, Nickerson DA, Below JE (2013) Utilizing graph theory to select the largest set of unrelated individuals for genetic analysis. Genet Epidemiol 37:136–141

  97. Stronen AV, Navid EL, Quinn MS, Paquet PC, Bryan HM, Darimont CT (2014) Population genetic structure of gray wolves (Canis lupus) in a marine archipelago suggests island-mainland differentiation consistent with dietary niche. BMC Ecol 14:11

  98. Toppenberg J, Beebe D, Scott, G, Edwards L, Noblin R, Hanson J (2015). Petition to list on an emergency basis the Alexander Archipelago wolf (Canis Lupus Ligoni) as threatened or endangered under the Endangered Species Act.

  99. Thomson HS (2016) Bill 2 – 2016- Great Bear Rainforest (Forest Management) Act.

  100. Twyford AD, Ennos RA (2012) Next-generation hybridization and introgression. Heredity 108:179–189

  101. Verts BJ, Carraway LN (1998) Land mammals of Oregon. University of California Press, Berkeley.

  102. Vilà C, Amorim IR, Leonard JA, Posada D, Castroviejo J, Petrucci Fonseca F et al. (1999) Mitochondrial DNA phylogeography and population history of the grey wolf (Canis lupus). Mol Ecol 8:2089–2103

  103. vonHoldt BM, Brzeski KE, Wilcove DS, Rutledge LY (2017) Redefining the role of admixture and genomics in species conservation. Conserv Lett 16:613

  104. vonHoldt BM, Cahill JA, Fan Z, Gronau I, Robinson J, Pollinger JP et al. (2016) Whole-genome sequence analysis shows that two endemic species of North American wolf are admixtures of the coyote and gray wolf. Sci Adv 2:e1501714–e1501714

  105. vonHoldt BM, Pollinger JP, Earl DA, Knowles JC, Boyko AR, Parker H et al. (2011) A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids. Genome Res 21:1294–1305

  106. vonHoldt BM, Pollinger JP, Earl DA, Parker HG, Ostrander EA, Wayne RK (2013) Identification of recent hybridization between gray wolves and domesticated dogs by SNP genotyping. Mamm Genome 24:80–88

  107. vonHoldt BM, Stahler DR, Bangs EE, Smith DW, Jimenez MD, Mack CM et al. (2010) A novel assessment of population structure and gene flow in grey wolf populations of the Northern Rocky Mountains of the UnitedStates. Mol Ecol 19:4412–4427

  108. vonHoldt BM, Stahler DR, Smith DW, Earl DA, Pollinger JP, Wayne RK (2008) The genealogy and genetic viability of reintroduced Yellowstone grey wolves. Mol Ecol 17:252–274

  109. Wall JD, Cox MP, Mendez FL, Woerner A, Severson T, Hammer MF (2008) A novel DNA sequence database for analyzing human demographic history. Genome Research 18:1354–1361

  110. Wayne RK, Hedrick PW (2011) Genetics and wolf conservation in the American West: lessons and challenges. Heredity 107:16–19

  111. Wayne RK, Jenks SM (1991) Mitochondrial DNA analysis implying extensive hybridization of the endangered red wolf (Canis rufus). Nature 351:565–568

  112. Wayne RK, Shaffer HB (2016) Hybridization and endangered species protection in the molecular era. Mol Ecol 25:2680–2689

  113. Weckworth BV, Dawson NG, Talbot SL, Cook JA (2015) Genetic distinctiveness of Alexander Archipelago wolves (Canis lupus ligoni). J Hered 106:412–414

  114. Weckworth BV, Dawson NG, Talbot SL, Flamme MJ, Cook JA (2011) Going coastal: shared evolutionary history between Coastal British Columbia and Southeast Alaska wolves (Canis lupus). PLoS ONE 6:e19582–8

  115. Weckworth BV, Talbot SL, Cook JA (2010) Phylogeography of wolves (Canis lupus) in the Pacific Northwest. J Mammal 91:363–375

  116. Weckworth BV, Talbot S, Sage GK, Person DK, Cook J (2005) A signal for independent coastal and continental histories among North American wolves. Mol Ecol 14:917–931

  117. Weeks AR, Stoklosa J, Hoffmann AA (2016) Conservation of genetic uniqueness of populations may increase extinction likelihood of endangered species: the case of Australian mammals. Front Zool 13:31

  118. Weir B, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

  119. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

  120. Wisz MS, Hijmans RJ, Li J, Peterson AT (2008) Effects of sample size on the performance of species distribution models. Divers Distrib 14:763–773

  121. Wright S (1951) Genetical structure of populations. Annu Eugen 166:247–249

  122. Young S, Goldman EA (1944) The Wolves of North America, vols 1 and 2. American Wildlife Institute, Washington.

  123. Zhang W, Fan Z, Han E, Hou R, Zhang L, Galaverni M et al (2014) Hypoxia adaptations in the grey wolf (Canis lupus chanco) from Qinghai-Tibet Plateau. PLoS Genet 10:e1004466–13

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We are grateful to Kristin Mansfield and Roblyn Brown for samples and insight into Washington and Oregon wolves, respectively. Laboratory and data processing assistance was completed by Sarah Wenner, Daniel Greenfield and Jacqueline Robinson. We thank Brendan Epstein for helpful discussions concerning methods' implementation and Kim Andrews for discussions regarding data interpretation within this study. This work was supported by the Wilburforce Foundation and the National Science Foundation (NSF; DEB-1021397, OPP-0733033). Additional support was provided to SAH by the National Institute of Health (P30GM103324), NSF (DEB-1316549) and the Bioinformatics and Computational Biology program at the University of Idaho; to RMS by the NSF (DGE-1144087, DGE-0707424, 1612859); and to RJH by the NSF (PD-08-1269). This work used the Vincent J. Coates Genomics Sequencing Laboratory at UC Berkeley, supported by NIH (S10RR029668, S10RR027303).

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  1. These authors contributed equally: Sarah A. Hendricks, Rena M. Schweizer.


  1. Department of Biological Sciences and Institute of Bioinformatics and Evolutionary Studies, University of Idaho, 875 Perimeter Drive, Moscow, ID, 83844, USA

    • Sarah A. Hendricks
    •  & Paul A. Hohenlohe
  2. Division of Biological Sciences, University of Montana, 32 Campus Drive, Missoula, MT, 59812, USA

    • Rena M. Schweizer
  3. Center for Tropical Research, Institute of the Environment and Sustainability, University of California, Los Angeles, 300 LaKretz Hall, Los Angeles, CA, 90095, USA

    • Ryan J. Harrigan
    •  & John P. Pollinger
  4. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, 610 Charles E. Young Drive East, Los Angeles, CA, 90095, USA

    • John P. Pollinger
    •  & Robert K. Wayne
  5. Raincoast Conservation Foundation, Sidney, BC, V8L 3Y3, Canada

    • Paul C. Paquet
    •  & Chris T. Darimont
  6. Department of Geography, University of Victoria, Box 1700, Stn CSC, Victoria, BC, V8W 2Y2, Canada

    • Paul C. Paquet
    •  & Chris T. Darimont
  7. Department of Fish and Wildlife Sciences, University of Idaho, 875 Perimeter Drive, Moscow, ID, 83844, USA

    • Jennifer R. Adams
    •  & Lisette P. Waits
  8. Department of Ecology and Evolutionary Biology, Princeton University, M151 Guyot Hall, Princeton, NJ, 08544, USA

    • Bridgett M. vonHoldt


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