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Genetic diversity and population structure of wolverine (Gulo gulo) populations at the southern edge of their current distribution in North America with implications for genetic viability

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Abstract

The current range of wolverines (Gulo gulo) within the lower 48 states includes small, remnant populations in Idaho, Washington, Wyoming and Montana. The size and trend of each of these populations and connectivity to adjacent populations in the contiguous United States and Canada are poorly understood. In this study, levels of genetic diversity and population genetic structure were examined in three states (Idaho, Wyoming, and Montana) and two Canadian provinces (Alberta and British Columbia) using both mitochondrial (mtDNA) and nuclear microsatellite DNA. Restricted levels of gene flow were detected among these populations with mitochondrial and nuclear DNA and our observations suggest a pattern of male-mediated gene flow. Populations in the United States appear to be receiving migrants from Canada, however, substantial genetic differentiation suggests that gene flow may not be high enough to prevent genetic drift. Our analyses suggest that at least 400 breeding pairs or 1–2 effective migrants per generation would be needed to ensure genetic viability in the long-term for each of the populations in the United States. Significant matrilineal structuring and restricted female gene flow indicates that demographic viability will depend upon the movement of female wolverines into new territories. Results from this study provide guidelines for conservation and management and indicate the need for more ecological data.

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References

  • Amos W, Balmford A, (2001) When does conservation genetics matter?. Hered ity 87:257–265

    Article  PubMed  CAS  Google Scholar 

  • Archie JW (1985) Statistical analysis of heterozygosity data: Independent sample comparisons. Evolution 39:623–637

    Article  Google Scholar 

  • Banci V (1987) Ecology and behavior of wolverine in Yukon. MS thesis, Simon Fraser University, Burnaby, BC

  • Banci V (1994) Wolverine. In: The Scientific Basis for Conserving Forest Carnivores, American Marten, Fisher Lynx, and Wolverine in the Western United States (eds. Ruggiero LF, Aubry KB, Buskirk SW, Lyon LJ, Zielinski WJ). USDA For. Env. Rocky Mt. For and Range. Exp. Stn., Gen Tech Rep. RM-254 1-184, Fort Collins, CO

  • Bryant HN (1987) Wolverine from the Pleistocene of the Yukon: Evolutionary trends and taxonomy of Gulo (Carnivora: Mustelidae). Can. J. Earth Sci. 24:654–663

    Article  Google Scholar 

  • Carroll C, Noss RF, Paquet PC (2001) Carnivores as focal species for conservation planning in the Rocky Mountain region. Ecol. Appl. 11:961–980

    Article  Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: Models and estimation procedures. Evolution 32:550–570

    Article  Google Scholar 

  • Cegelski CC, Waits LP, Anderson NJ (2003) Assessing population structure and gene flow in Montana wolverines (Gulo gulo) using assignment-based approaches. Mol. Ecol. 12:2907–2918

    Article  PubMed  CAS  Google Scholar 

  • Chappell DE, Van Den Bussche RA, Kriza J, Patterson B (2004) Contrasting levels of genetic differentiation among populations of wolverines (Gulo gulo) from northern Canada revealed by nuclear and mitochondrial loci. Conserv. Genetics 5:759–767

    Article  CAS  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS, a computer program to estimate gene genealogies. Mol. Ecol. 9:1657–1659

    Article  PubMed  CAS  Google Scholar 

  • Coltman DW, Bowen DW, Wright JM (1998) Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc. R. Soc. Lond. B. Biol. Sci. 265:803–809

    Article  CAS  Google Scholar 

  • Copeland J (1998) Biology of the wolverine in central Idaho. MS thesis, University of Idaho, Moscow, Idaho

  • Dallas JF, Piertney SB (1998) Microsatellite primers for the Eurasian otter. Mol. Ecol. 7:1247–1263

    Article  Google Scholar 

  • Davis CS, Strobeck C (1998) Isolation, variability, and cross-species amplification of polymorphic microsatellite loci in the family Mustelidae. Mol. Ecol. 7:1771–1788

    Article  Google Scholar 

  • Duffy AJ, Landa A, O’Connell M, Stratton C, Wright JM (1998) Four polymorphic microsatellites in wolverine. Gulo gulo. Anim. Genet. 29:63–72

    PubMed  CAS  Google Scholar 

  • Edelmann F, Copeland J (1999) Wolverine distribution in the Northwestern United States and a survey in the Seven Devils Mountains of Idaho. Northwest Sci. 73:295–304

    Google Scholar 

  • England PR, Osler GHR (2001) GENELOSS: A computer program for simulating the effects of population bottlenecks on genetic diversity. Mol. Ecol. Notes 1:111–113

    Article  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Frankham R (1995) Inbreeding and extinction: A threshold effect. Conserv. Biol. 9:792–799

    Article  Google Scholar 

  • Flagstad O, Hedmark E, Landa A, Broseth H, Persson J, Andersen R, Segerstrom P, Ellegren H (2004) Colonization history and noninvasive monitoring of a reestablished wolverine population. Conserv. Biol. 18:676–688

    Article  Google Scholar 

  • Guglich EA, Wilson PJ, White BN (1994) Forensic application of repetitive DNA markers to the species identification of animal tissues. J. Forensic Sci. 39:353–361

    PubMed  CAS  Google Scholar 

  • Haglund B (1966). Winter habits of the Lynx (Lynx lynx L.) and wolverine (Gulo gulo L.) as revealed by tracking in the snow. Vilvetry 4:81–309

    Google Scholar 

  • Hall ER (1981) The mammals of North America. 2nd ed. 2 vol. John Wiley & Sons, New York

    Google Scholar 

  • Hanski I, Gilpin M (eds) (1997) Metapopulation Biology, Ecology, Genetic, and Evolution. Academic press, San Diego

    Google Scholar 

  • Hash HS (1987) Wolverine. In: Nowak M, Baker J, Obbard M, Malloch B (eds) Wild Furbearer Management and Conservation in North America. Ministry of Natural Resources, Ontario, pp. 574–585

    Google Scholar 

  • Hedrick PW, Miller P (1992) Conservation genetics: Techniques and fundamentals. Ecol. App. 2:30–46

    Article  Google Scholar 

  • Holsinger KE (2000) Demography and extinction in small populations. In: Young A, Clarke G (eds) Genetics, demography, and the viability of fragmented populations. Cambridge University Press, Cambridge, pp. 55–74

    Google Scholar 

  • Hornocker MG, Hash HS (1981) Ecology of the wolverine in northwestern Montana. Can. J. Zoo. 59:1286–1301

    Article  Google Scholar 

  • Inman KH, Inman RM, Wigglesworth RR, McCue AJ, Brock BL, Rieck JD, Harrower W (2003) Greater Yellowstone Wolverine Study, CumulativeProgress Report December 2003, Wildlife Conservation Society General Technical Report. 36 pp

  • Knowles LL, Maddison WP (2002) Statistical phylogeography. Mol. Ecol. 11:2623–2635

    Article  PubMed  Google Scholar 

  • Krebs JA, Lewis D (1999) Wolverine Ecology and habitat use in the North Columbia Mountains: Progress Report. Proceedings of Biology and Management of Species at Risk, Kamloops BC

  • Kyle CJ, Strobeck C (2001) Genetic Structure of North American wolverine (Gulo gulo) Populations. Mol. Ecol. 10:337–347

    Article  PubMed  CAS  Google Scholar 

  • Kyle CJ, Strobeck C (2002) Connectivity of peripheral and core populations of North American wolverines. J. Mamm. 83:1141–1150

    Article  Google Scholar 

  • Krott P (1960) Ways of the wolverine. Nat. Hist. 69:136–150

    Google Scholar 

  • Langella O (2001) Populations 1.2.24. Population genetic structure (individuals or populations distances, phylogenetic␣trees). http://www.pge.cnrs.gif.fr/bioinfo/populations/ (March 2005)

  • Madsen T, Shine R, Olsson M, Wittzell H (1999) Restoration of an inbred adder population. Nature 404:34–35

    Article  CAS  Google Scholar 

  • Magoun AJ (1985) Population characteristics, ecology and management of wolverines in northwestern Alaska. PhD thesis, University of Alaska, Fairbanks, Alaska

  • Mantel N (1967) The detection of disease clustering and generalized regression approach. Cancer Res. 27:209–220

    PubMed  CAS  Google Scholar 

  • Miller CR, Waits LP (2003) The history of effective population size and genetic diversity in the Yellowstone grizzly (Ursus arctos): Implications for conservation. Proc. Natl. Acad. Sci. 7:4334–4339

    Article  CAS  Google Scholar 

  • Murray JA (1987) Wildlife in Peril: The Endangered Mammals of Colorado: River Otter, Black-footed Ferret, Wolverine, Lynx, Grizzly Bear, Gray Wolf. Roberts Rinchart Publishers, Boulder, Colorado

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  Google Scholar 

  • Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York

    Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: A simulation-based exploration of accuracy and power. Mol. Ecol. 13:55–65

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall KA, Templeton AR (2000) GeoDis, a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol. Ecol. 9:487–488

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Pulliainen E (1968) Breeding biology of the wolverine (Gulo gulo L.) in Finland. Ann. Zool. Fenni. 5:338–344

    Google Scholar 

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

    Google Scholar 

  • Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103

    PubMed  CAS  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv. Biol. 17:230–237

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.0: A software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland

    Google Scholar 

  • Schreiber A, Wirth R, Riffel M, Van Rompaey H (1989) Weasels, civets, mongooses, and their relatives: An action plan for the conservation of mustelids and viverrids. IUCN. Gland, Switzerland

    Google Scholar 

  • Storfer A (1999) Gene flow and endangered species translocations: a topic revisited. Biol. Conserv. 87:173–180

    Article  Google Scholar 

  • Swafford DL (1998) PAUP* Phylogenetic Analysis Using Parsimony (*and other methods), Version 3, Sinauer Associates, Sunderland, Massachusetts

  • Taylor H (2000) IUCN Red List of Threatened Species. IUCN. Gland, Switzerland and Cambridge

    Google Scholar 

  • Templeton AR (1998) Nested clade analysis of phylogeographic data: Testing hypotheses about gene flow and population history. Mol. Ecol. 7:381–397

    Article  PubMed  CAS  Google Scholar 

  • Templeton AR (2004) Statistical phlogeography: Methods of evaluating and minimizing inference errors. Mol. Ecol. 13:789–809

    Article  PubMed  Google Scholar 

  • Templeton AR, Sing CF (1993) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. Genetics 134:659–669

    PubMed  CAS  Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    PubMed  CAS  Google Scholar 

  • Templeton AR, Routman E, Philips C (1995) Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the Tiger Salamander. Ambystoma tigrinum. Genetics 140:767–782

    PubMed  CAS  Google Scholar 

  • Tomasik E, Cook JA (2005) Mitochondrial phylogeography and conservation genetics of wolverine (Gulo gulo) of northwestern North America. J. Mammal. 86:386–396

    Article  Google Scholar 

  • USFWS (1995) Endangered and threatened wildlife and plants: 90 day finding for a petition to list as endangered or threatened the contiguous United States population of the North American wolverine. Fed. Regist. 60:19567–19568

    Google Scholar 

  • USFWS (2003) Endangered and threatened wildlife and plants: 90 day finding for a petition to list as endangered or threatened wolverine in the contiguous United States. Fed. Regist. 68:60112–60115

    Google Scholar 

  • Vangen KM, Persson J, Landa A, Anderson R, Segerstrom P (2001) Characteristics of dispersal in wolverines. Can. J. Zool. 79:1641–1649

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Westemeier RJ, Brawn S, Simpson T, Esker J, Jansen J, Walk J, Kershner E, Bouzat J, Paige K (1998) Tracking the long-term decline and recovery of an isolated population. Science 282:1695–1698

    Article  PubMed  CAS  Google Scholar 

  • Wilson GM, Van Den Bussche RA, Kennedy PK, Gunn A, Poole K (2000) Genetic variability of wolverines (Gulo gulo) from the Northwest Territories, Canada: Conservation implications. J. Mammal. 81:186–196

    Article  Google Scholar 

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Authors and Affiliations

  1. Idaho Department of Fish and Game, 1800 Trout Rd., Eagle, ID, 83616, USA

    C.C. Cegelski

  2. Department of Fish and Wildlife Resources, University of Idaho, Moscow, ID, 83844-1136, USA

    L.P. Waits

  3. Montana Fish, Wildlife, and Parks, Bozeman, MT, 59717, USA

    N.J. Anderson

  4. Center for Ecological and Evolutionary Synthesis, Department of Biology, P.O. Box 1066, Blindern, N-0316, Oslo, Norway

    O. Flagstad

  5. Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada, T6G 2E9

    C. Strobeck

  6. Natural Resources DNA Profiling and Forensics Centre, Trent University, Peterborough, Ontario, Canada, K9J 8N8

    C.J. Kyle

Authors
  1. C.C. Cegelski
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  2. L.P. Waits
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  3. N.J. Anderson
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  4. O. Flagstad
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  5. C. Strobeck
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  6. C.J. Kyle
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Correspondence to L.P. Waits.

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Cegelski, C., Waits, L., Anderson, N. et al. Genetic diversity and population structure of wolverine (Gulo gulo) populations at the southern edge of their current distribution in North America with implications for genetic viability. Conserv Genet 7, 197–211 (2006). https://doi.org/10.1007/s10592-006-9126-9

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  • DOI: https://doi.org/10.1007/s10592-006-9126-9

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