Conservation Genetics

, Volume 7, Issue 2, pp 197–211 | Cite as

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

  • C.C. Cegelski
  • L.P. Waits
  • N.J. Anderson
  • O. Flagstad
  • C. Strobeck
  • C.J. Kyle
Article

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.

Keywords

genetic diversity Gulo gulo population genetic structure wolverine 

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References

  1. Amos W, Balmford A, (2001) When does conservation genetics matter?. Hered ity 87:257–265PubMedCrossRefGoogle Scholar
  2. Archie JW (1985) Statistical analysis of heterozygosity data: Independent sample comparisons. Evolution 39:623–637CrossRefGoogle Scholar
  3. Banci V (1987) Ecology and behavior of wolverine in Yukon. MS thesis, Simon Fraser University, Burnaby, BCGoogle Scholar
  4. 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, COGoogle Scholar
  5. Bryant HN (1987) Wolverine from the Pleistocene of the Yukon: Evolutionary trends and taxonomy of Gulo (Carnivora: Mustelidae). Can. J. Earth Sci. 24:654–663CrossRefGoogle Scholar
  6. Carroll C, Noss RF, Paquet PC (2001) Carnivores as focal species for conservation planning in the Rocky Mountain region. Ecol. Appl. 11:961–980CrossRefGoogle Scholar
  7. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: Models and estimation procedures. Evolution 32:550–570CrossRefGoogle Scholar
  8. Cegelski CC, Waits LP, Anderson NJ (2003) Assessing population structure and gene flow in Montana wolverines (Gulo gulo) using assignment-based approaches. Mol. Ecol. 12:2907–2918PubMedCrossRefGoogle Scholar
  9. 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 5:759–767CrossRefGoogle Scholar
  10. Clement M, Posada D, Crandall KA (2000) TCS, a computer program to estimate gene genealogies. Mol. Ecol. 9:1657–1659PubMedCrossRefGoogle Scholar
  11. 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. 265:803–809CrossRefGoogle Scholar
  12. Copeland J (1998) Biology of the wolverine in central Idaho. MS thesis, University of Idaho, Moscow, IdahoGoogle Scholar
  13. Dallas JF, Piertney SB (1998) Microsatellite primers for the Eurasian otter. Mol. Ecol. 7:1247–1263CrossRefGoogle Scholar
  14. Davis CS, Strobeck C (1998) Isolation, variability, and cross-species amplification of polymorphic microsatellite loci in the family Mustelidae. Mol. Ecol. 7:1771–1788CrossRefGoogle Scholar
  15. Duffy AJ, Landa A, O’Connell M, Stratton C, Wright JM (1998) Four polymorphic microsatellites in wolverine. Gulo gulo. Anim. Genet. 29:63–72PubMedGoogle Scholar
  16. Edelmann F, Copeland J (1999) Wolverine distribution in the Northwestern United States and a survey in the Seven Devils Mountains of Idaho. Northwest Sci. 73:295–304Google Scholar
  17. England PR, Osler GHR (2001) GENELOSS: A computer program for simulating the effects of population bottlenecks on genetic diversity. Mol. Ecol. Notes 1:111–113CrossRefGoogle Scholar
  18. 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 131:479–491PubMedGoogle Scholar
  19. Frankham R (1995) Inbreeding and extinction: A threshold effect. Conserv. Biol. 9:792–799CrossRefGoogle Scholar
  20. 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. 18:676–688CrossRefGoogle Scholar
  21. Guglich EA, Wilson PJ, White BN (1994) Forensic application of repetitive DNA markers to the species identification of animal tissues. J. Forensic Sci. 39:353–361PubMedGoogle Scholar
  22. Haglund B (1966). Winter habits of the Lynx (Lynx lynx L.) and wolverine (Gulo gulo L.) as revealed by tracking in the snow. Vilvetry 4:81–309Google Scholar
  23. Hall ER (1981) The mammals of North America. 2nd ed. 2 vol. John Wiley & Sons, New YorkGoogle Scholar
  24. Hanski I, Gilpin M (eds) (1997) Metapopulation Biology, Ecology, Genetic, and Evolution. Academic press, San DiegoGoogle Scholar
  25. 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. 574–585Google Scholar
  26. Hedrick PW, Miller P (1992) Conservation genetics: Techniques and fundamentals. Ecol. App. 2:30–46CrossRefGoogle Scholar
  27. 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. 55–74Google Scholar
  28. Hornocker MG, Hash HS (1981) Ecology of the wolverine in northwestern Montana. Can. J. Zoo. 59:1286–1301CrossRefGoogle Scholar
  29. 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 ppGoogle Scholar
  30. Knowles LL, Maddison WP (2002) Statistical phylogeography. Mol. Ecol. 11:2623–2635PubMedCrossRefGoogle Scholar
  31. 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 BCGoogle Scholar
  32. Kyle CJ, Strobeck C (2001) Genetic Structure of North American wolverine (Gulo gulo) Populations. Mol. Ecol. 10:337–347PubMedCrossRefGoogle Scholar
  33. Kyle CJ, Strobeck C (2002) Connectivity of peripheral and core populations of North American wolverines. J. Mamm. 83:1141–1150CrossRefGoogle Scholar
  34. Krott P (1960) Ways of the wolverine. Nat. Hist. 69:136–150Google Scholar
  35. 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)
  36. Madsen T, Shine R, Olsson M, Wittzell H (1999) Restoration of an inbred adder population. Nature 404:34–35CrossRefGoogle Scholar
  37. Magoun AJ (1985) Population characteristics, ecology and management of wolverines in northwestern Alaska. PhD thesis, University of Alaska, Fairbanks, AlaskaGoogle Scholar
  38. Mantel N (1967) The detection of disease clustering and generalized regression approach. Cancer Res. 27:209–220PubMedGoogle Scholar
  39. 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. 7:4334–4339CrossRefGoogle Scholar
  40. 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, ColoradoGoogle Scholar
  41. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  42. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New YorkGoogle Scholar
  43. 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. 13:55–65PubMedCrossRefGoogle Scholar
  44. Posada D, Crandall KA, Templeton AR (2000) GeoDis, a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol. Ecol. 9:487–488PubMedCrossRefGoogle Scholar
  45. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  46. Pulliainen E (1968) Breeding biology of the wolverine (Gulo gulo L.) in Finland. Ann. Zool. Fenni. 5:338–344Google Scholar
  47. Raymond M, Rousset F (1995) GENEPOP (version 1.2): Population genetic software for exact tests and ecumenicism. J. Hered. 86:248–249Google Scholar
  48. Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103PubMedGoogle Scholar
  49. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv. Biol. 17:230–237CrossRefGoogle Scholar
  50. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  51. 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, SwitzerlandGoogle Scholar
  52. 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, SwitzerlandGoogle Scholar
  53. Storfer A (1999) Gene flow and endangered species translocations: a topic revisited. Biol. Conserv. 87:173–180CrossRefGoogle Scholar
  54. Swafford DL (1998) PAUP* Phylogenetic Analysis Using Parsimony (*and other methods), Version 3, Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  55. Taylor H (2000) IUCN Red List of Threatened Species. IUCN. Gland, Switzerland and CambridgeGoogle Scholar
  56. Templeton AR (1998) Nested clade analysis of phylogeographic data: Testing hypotheses about gene flow and population history. Mol. Ecol. 7:381–397PubMedCrossRefGoogle Scholar
  57. Templeton AR (2004) Statistical phlogeography: Methods of evaluating and minimizing inference errors. Mol. Ecol. 13:789–809PubMedCrossRefGoogle Scholar
  58. 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 134:659–669PubMedGoogle Scholar
  59. 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 132:619–633PubMedGoogle Scholar
  60. 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 140:767–782PubMedGoogle Scholar
  61. Tomasik E, Cook JA (2005) Mitochondrial phylogeography and conservation genetics of wolverine (Gulo gulo) of northwestern North America. J. Mammal. 86:386–396CrossRefGoogle Scholar
  62. 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. 60:19567–19568Google Scholar
  63. 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. 68:60112–60115Google Scholar
  64. Vangen KM, Persson J, Landa A, Anderson R, Segerstrom P (2001) Characteristics of dispersal in wolverines. Can. J. Zool. 79:1641–1649CrossRefGoogle Scholar
  65. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370CrossRefGoogle Scholar
  66. 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 282:1695–1698PubMedCrossRefGoogle Scholar
  67. 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. 81:186–196CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • C.C. Cegelski
    • 1
  • L.P. Waits
    • 2
  • N.J. Anderson
    • 3
  • O. Flagstad
    • 4
  • C. Strobeck
    • 5
  • C.J. Kyle
    • 6
  1. 1.Idaho Department of Fish and GameEagleUSA
  2. 2.Department of Fish and Wildlife ResourcesUniversity of IdahoMoscowUSA
  3. 3.Montana Fish, Wildlife, and ParksBozemanUSA
  4. 4.Center for Ecological and Evolutionary SynthesisDepartment of BiologyBlindernNorway
  5. 5.Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  6. 6.Natural Resources DNA Profiling and Forensics CentreTrent UniversityPeterboroughCanada

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