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Conservation Genetics

, Volume 13, Issue 2, pp 359–371 | Cite as

Dispersal in a plain landscape: short-distance genetic differentiation in southwestern Manitoba wolves, Canada

  • Astrid V. Stronen
  • Graham J. Forbes
  • Paul C. Paquet
  • Gloria Goulet
  • Tim Sallows
  • Marco Musiani
Research Article

Abstract

The effects of human-caused fragmentation require further study in landscapes where physical dispersal barriers and natural ecological transitions can be discounted as causes for population genetic structure. We predict that fragmentation can reduce dispersal across such barrier-free landscapes because dispersal also is limited by a perception of risk. Considerable fragmentation has occurred in the Riding Mountain National Park (RMNP) region in Manitoba, Canada, during the past 60 years. We examine data from 13 autosomal microsatellites to determine whether fragmentation is correlated with genetic population structure in wolves (Canis lupus). Moderate and significant differentiation between RMNP and a genetic cluster identified 30 km farther north (F ST = 0.053, 95% CI [0.031–0.073]) is consistent with predicted effects of fragmentation. The RMNP population cluster represents at least seven wolf packs followed weekly by radio tracking during 2003–2006. Distinct mtDNA haplotypes have been identified in the Park and no successful wolf dispersal from RMNP has been documented in several multi-year tracking studies since 1974. Tracking data also indicate that some wolves might be reluctant to leave RMNP. Although the influence of behaviour and local adaptation require investigation, human-caused fragmentation appears to have caused cryptic genetic structure on fine spatiotemporal scales in a vagile species that is: (1) not influenced by physical movement barriers or historical ecological discontinuities in our study area, and; (2) able to live relatively close to humans. The Great Plains is now an intensely human-managed landscape. Detection of cryptic genetic structure could therefore function as an important indicator in conservation management.

Keywords

Canis lupus Dispersal Fragmentation Gene flow Isolation 

Notes

Acknowledgments

We thank G. Pflueger, S. Jaward, staff from Parks Canada and Manitoba Conservation, the Duck Mountain Trappers’ Association, trappers from northern Manitoba, and other residents for contributing to sample collection and tracking of radio-collared wolves. Microsatellite analyses were done at GenServe Laboratories at the Saskatchewan Research Council, Saskatoon. A. Arndt, D. Berezanski, D. Bergeson, L. Jesson, D. Keppie, B. Mann, A. McDevitt, E. Navid, Y. Plante, S. Woodley, and two anonymous reviewers provided valuable help and advice on analyses and earlier versions of the manuscript. We gratefully acknowledge funding from Parks Canada, World Wildlife Fund Canada, the Sustainable Development Innovations Fund at Manitoba Conservation, and Louisiana Pacific Canada.

Supplementary material

10592_2011_290_MOESM1_ESM.doc (266 kb)
Supplementary material 1 (DOC 256 kb)

References

  1. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell Publishing, MaldenGoogle Scholar
  2. Ashley MV, Wilson MF, Pergarms ORW, O’Dowd DJ, Gende SM, Brown JS (2003) Evolutionary enlightened management. Biol Conserv 111:115–123CrossRefGoogle Scholar
  3. Aspi J, Roininen E, Ruokonen M, Kojola I, Vilà C (2006) Genetic diversity, population structure, effective population size and demographic history of the Finnish wolf population. Mol Ecol 15:1561–1576PubMedCrossRefGoogle Scholar
  4. Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165PubMedCrossRefGoogle Scholar
  5. Belkhir KP, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions. CNRS UMR 5171, Université de Montpellier II, MontpellierGoogle Scholar
  6. Breen M, Jouquand S, Renier C et al (2001) Chromosome-specific single-locus FISH probes allow anchorage of an 1800-marker integrated radiation-hybrid/linkage map of the domestic dog genome to all chromosomes. Genome Res 11:1784–1795PubMedCrossRefGoogle Scholar
  7. Carbyn LN (1980) Ecology and management of wolves in Riding Mountain National Park, Manitoba. Final report, Large Mammal System Studies, Report No. 10, September 1975–March 1979. Canadian Wildlife Service, EdmontonGoogle Scholar
  8. Carbyn LN (1982) Incidence of disease and its potential role in the population dynamics of wolves in Riding Mountain National Park, Manitoba. In: Harrington FH, Paquet PC (eds) Wolves of the world: perspectives of behaviour, ecology and conservation. Noyes Publications, Park Ridge, pp 106–115Google Scholar
  9. Carmichael LE, Nagy JA, Carter NC, Strobeck C (2001) Prey specialization may influence patterns of gene flow in wolves of the Canadian Northwest. Mol Ecol 10:2787–2798PubMedGoogle Scholar
  10. Carroll C, Philips MK, Lopez-Gonzales CA, Schumaker NH (2006) Defining recovery goals and strategies for endangered species: the wolf as a case study. Bioscience 56:25–37CrossRefGoogle Scholar
  11. Cegelski CC, Waits LP, Anderson NJ (2003) Assessing population structure and gene flow in Montana wolverines (Gulo gulo) using assignment approaches. Mol Ecol 12:2907–2918PubMedCrossRefGoogle Scholar
  12. Coulon A, Guillot G, Cousson J-F et al (2006) Genetic structure is influenced by landscape features: empirical evidence from a roe deer population. Mol Ecol 15:1669–1679PubMedCrossRefGoogle Scholar
  13. Environment Canada (1993) Canada: terrestrial ecoregions. http://atlas.nrcan.gc.ca/site/english/maps/archives/5thedition/environment/ecology/mcr4164#download. Accessed May 2007
  14. Eppley SM, Taylor PJ, Jesson LK (2007) Self-fertilization in mosses: a comparison of heterozygosity deficiency between species with combined versus separate sexes. Heredity 98:38–44PubMedCrossRefGoogle Scholar
  15. Ernest HB, Boyce WM, Bleich VC, May B, Stiver SJ, Torres SG (2003) Genetic structure of mountain lion (Puma concolor) populations in California. Conserv Genet 4:353–366CrossRefGoogle Scholar
  16. Evanno G, Regaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  17. Fain SR, Straughan DJ, Taylor BF (2010) Genetic outcomes of wolf recovery in the western Great Lakes states. Conserv Genet 11:1747–1765CrossRefGoogle Scholar
  18. Falush D, Stephens M, Pritchard JK (2003) Inference on population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  19. Flagstad Ø, Walker CW, Vilà C, Sundqvist A-K, Fernholm B, Hufthammer AK, Wiig Ø, Kojola I, Ellegren H (2003) Two centuries of the Scandinavian wolf population: patterns of genetic variability and migration during an era of dramatic decline. Mol Ecol 12:869–880PubMedCrossRefGoogle Scholar
  20. Forbes GJ, Theberge JB (1996) Response by wolves to prey variation in central Ontario. Can J Zool 74:1511–1520CrossRefGoogle Scholar
  21. Franklin JF (1993) Preserving biodiversity: species, ecosystems, or landscapes? Ecol Appl 32:202–205CrossRefGoogle Scholar
  22. Fritts SH (1983) Record dispersal by a wolf from Minnesota. J Mammal 64:166–167CrossRefGoogle Scholar
  23. Fritts SH, Carbyn LN (1995) Population viability, nature reserves, and the outlook for gray wolf conservation in North America. Restor Ecol 3(1):26–38CrossRefGoogle Scholar
  24. Fuller TK, Mech LD, Cochrane JF (2003) Wolf population dynamics. In: Mech LD, Boitani L (eds) Wolves: behaviour, ecology and conservation. University of Chicago Press, Chicago, pp 161–191Google Scholar
  25. Geffen E, Anderson MJ, Wayne RK (2004) Climate and habitat barriers to dispersal in the highly mobile grey wolf. Mol Ecol 13:2481–2490PubMedCrossRefGoogle Scholar
  26. Gese EM, Mech LD (1991) Dispersal of wolves (Canis lupus) in northeastern Minnesota, 1969–1989. Can J Zool 69:2946–2955CrossRefGoogle Scholar
  27. Goulet GD (1993) Comparison of temporal and geographical skull variation among Nearctic modern, Holocene and Late Pleistocene gray wolves (Canis lupus) (and selected Canis). MSc Thesis, University of Manitoba, WinnipegGoogle Scholar
  28. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162CrossRefGoogle Scholar
  29. Guertin DS, Easterling WE, Brandle JR (1997) Climate change and forests in the Great Plains. Bioscience 47:287–295CrossRefGoogle Scholar
  30. Guillot G, Estoup A, Mortier F, Cosson J-F (2005) A spatial statistical model for landscape genetics. Genetics 170:1261–1280PubMedCrossRefGoogle Scholar
  31. Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372PubMedCrossRefGoogle Scholar
  32. Guyon R, Lorentzen TD, Hitte C et al (2003) A 1-Mb resolution radiation hybrid map of the canine genome. Proc Natl Acad Sci USA 100:5296–5301PubMedCrossRefGoogle Scholar
  33. Haight RG, Mladenoff DL, Wydeven AP (1998) Modeling disjunct gray wolf populations in semi-wild landscapes. Conserv Biol 12:879–888CrossRefGoogle Scholar
  34. Hedrick PW (1999) Highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318CrossRefGoogle Scholar
  35. Hoelzel AR, Dahlheim M, Stern SJ (1998) Low genetic variation among killer whales (Orcinus orca) in the eastern north Pacific and genetic differentiation between foraging specialists. J Hered 89:121–128PubMedCrossRefGoogle Scholar
  36. Koblmüller S, Nord M, Wayne RK, Leonard JA (2009) Origin and status of the Great Lakes wolf. Mol Ecol 18:2313–2326PubMedCrossRefGoogle Scholar
  37. Kramer-Schadt S, Revilla E, Wiegand T, Breitenmoser U (2004) Fragmented landscapes, road mortality and patch connectivity: modelling influences on the dispersal of Eurasian lynx. J Appl Ecol 41:711–723CrossRefGoogle Scholar
  38. Lambin X, Yoccoz NG (1998) The impact of population kin-structure on nestling survival in Townsend voles (Microtus townsendii). J Anim Ecol 67:1–16CrossRefGoogle Scholar
  39. Lehman N, Eisenhawer A, Hansen K, Mech D, Peterson RO, Gogan PJP, Wayne RK (1991) Introgression of coyote mitochondrial DNA into sympatric North American gray wolf populations. Evolution 45:104–119CrossRefGoogle Scholar
  40. Leonard JA, Vilà C, Wayne RK (2005) Legacy lost: genetic variability and population size of extirpated US grey wolves (Canis lupus). Mol Ecol 14:9–17PubMedCrossRefGoogle Scholar
  41. Loveless K (2010) Foraging strategies of eastern wolves in relation to migratory prey and hybridization. MSc Thesis, Trent University, PeterboroughGoogle Scholar
  42. Lucchini V, Fabri E, Marucco F, Ricci S, Boitani L, Randi E (2002) Noninvasive molecular tracking of colonizing wolf (Canis lupus) packs in the western Alps. Mol Ecol 11:857–868PubMedCrossRefGoogle Scholar
  43. Manitoba Conservation (2004) Duck Mountain Provincial Park. http://www.gov.mb.ca/conservation/parks/popular_parks/duck_mtn/info.html. Accessed June 2007
  44. McNamee K (1993) From wild places to endangered spaces: a history of Canada’s national parks. In: Dearden P, Rollins R (eds) Parks and protected areas in Canada: planning and management. Oxford University Press, Toronto, pp 17–44Google Scholar
  45. Mech LD, Boitani L (2003) Introduction. In: Mech LD, Boitani L (eds) Wolves: behaviour, ecology and conservation. University of Chicago Press, Chicago, pp xv–xviiGoogle Scholar
  46. Muñoz-Fuentes V, Darimont CT, Wayne RK, Paquet PC, Leonard JA (2009) Ecological factors drive genetic differentiation in British Columbia gray wolves. J Biogeogr 31:1516–1531CrossRefGoogle Scholar
  47. Neff MW, Broman KW, Mellersh CS et al (1999) A second-generation genetic linkage map of the domestic dog, Canis familiaris. Genetics 151:803–820. doi: 10.1073/pnas.0831002100 PubMedGoogle Scholar
  48. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  49. Noss RF (1995) Maintaining ecological integrity in representative networks. World Wildlife Fund Canada and World Wildlife Fund United StatesGoogle Scholar
  50. Noss RF, Quigley HB, Hornocker MG, Merrill T, Paquet PC (1996) Conservation biology and carnivore conservation in the Rocky Mountains. Conserv Biol 10:949–963CrossRefGoogle Scholar
  51. Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354PubMedCrossRefGoogle Scholar
  52. Paquet PC (1992) Prey use strategies of sympatric wolves and coyotes in Riding Mountain National Park, Manitoba. J Mammal 73:337–343CrossRefGoogle Scholar
  53. Paquet PC, Alexander S, Donelon S, Callaghan C (2010) Influence of anthropogenically modified snow conditions on movement and predatory behaviour of gray wolves. In: Musiani M, Boitani L, Paquet PC (eds) The world of wolves: new perspectives on ecology behaviour and policy. University of Calgary Press, Calgary, pp 157–173Google Scholar
  54. Parks Canada (2004) Riding Mountain National Park: ecological integrity statement. http://www2.parkscanada.gc.ca/pn-np/mb/riding/plan/plan3_e.asp. Accessed June 2007
  55. Parks Canada (2006) Riding Mountain National Park: natural heritage. http://www2.parkscanada.gc.ca/pn-np/mb/riding/natcul/natcul1_E.asp. Accessed June 2007
  56. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  57. Pilot M, Jedrzejewski W, Branicki W et al (2006) Ecological factors influence population genetic structure of European grey wolves. Mol Ecol 15:4533–4553PubMedCrossRefGoogle Scholar
  58. Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  59. Pritchard JK, Stephens M, Donnely P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  60. Raymond M, Rousset F (1995) Genepop (version 1.2): population genetics software for exact tests and ecumeniscism. J Hered 86:248–249Google Scholar
  61. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  62. Riley SPD, Pollinger JP, Sauvajot RM et al (2006) A southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15:1733–1741PubMedCrossRefGoogle Scholar
  63. Roques S, Sevigny J-M, Bernatchez L (2001) Evidence for broadscale introgressive hybridization between two redfish (genus Sebastes) in the North-west Atlantic: a rare marine example. Mol Ecol 10:149–165PubMedCrossRefGoogle Scholar
  64. Roy MS, Geffen E, Smith D, Ostrander EA, Wayne RK (1994) Patterns of differentiation and hybridization in North American wolf like canids, revealed by analysis of microsatellite loci. Mol Biol Evol 11:553–570PubMedGoogle Scholar
  65. Rueness EK, Stenseth NC, O’Donoghue M et al (2003) Ecological and genetic spatial structuring in the Canadian lynx. Nature 425:69–72PubMedCrossRefGoogle Scholar
  66. Sacks BN, Brown SK, Ernest HB (2004) Population structure of California coyotes corresponds to habitat-specific breaks and illuminate species history. Mol Ecol 13:1265–1275PubMedCrossRefGoogle Scholar
  67. Sacks BN, Mitchell BR, Williams CL, Ernest HB (2005) Coyote movements and social structure along a cryptic genetic subdivision. Mol Ecol 14:1241–1249PubMedCrossRefGoogle Scholar
  68. Sancristobal-Gaudy M, Renand G, Amigues Y, Boscher M-Y, Levéziel H, Bibé B (2000) Traçabilité individuelle des viands bovines à l’aide de marqueurs génétiques. INRA Prod Anim 13:269–276Google Scholar
  69. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.00: a software for population genetics data analyses. Genetics and Biometry Laboratory, University of Geneva, GenevaGoogle Scholar
  70. Stronen AV (2009) Dispersal in a plain landscape: wolves in southwestern Manitoba, Canada. PhD Dissertation, University of New Brunswick, FrederictonGoogle Scholar
  71. Stronen AV, Brook RK, Paquet PC, McLachlan SM (2007) Farmer attitudes toward wolves: implications for the role of predators in managing disease. Biol Conserv 135:1–10CrossRefGoogle Scholar
  72. Stronen AV, Forbes GJ, Sallows T, Goulet G, Musiani M, Paquet PC (2010) Wolf body mass, skull morphology, and mitochondrial DNA haplotypes in the Riding Mountain National Park region of Manitoba, Canada. Can J Zool 88:496–507CrossRefGoogle Scholar
  73. Sundquist AK, Ellegren H, Olivier M, Vilà C (2001) Y-chromosome haplotyping in Scandinavian wolves (Canis lupus) based on microsatellite markers. Mol Ecol 10:1959–1966CrossRefGoogle Scholar
  74. Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203PubMedCrossRefGoogle Scholar
  75. Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson J-F (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464PubMedCrossRefGoogle Scholar
  76. Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. Trends Ecol Evol 14:323–327PubMedCrossRefGoogle Scholar
  77. Temple HJ, Hoffman I, Amos W (2006) Dispersal, philopatry and intergroup relatedness: fine-scale genetic structure in the white-breasted thrasher (Ramphocinclus branchyurus). Mol Ecol 15:3449–3458PubMedCrossRefGoogle Scholar
  78. Thiessen CD (2007) Population structure and dispersal of wolves in the Canadian Rocky Mountains. MSc Thesis, Department of Biology, University of Alberta, EdmontonGoogle Scholar
  79. Vilà C, Amorim IR, Leonard JA et al (1999) Mitochondrial DNA phylogeography and population history of the grey wolf Canis lupus. Mol Ecol 8:2089–2103PubMedCrossRefGoogle Scholar
  80. vonHoldt BM, Stahler DR, Smith DW et al (2008) The genealogy and genetic viability of reintroduced Yellowstone grey wolves. Mol Ecol 17:252–274PubMedCrossRefGoogle Scholar
  81. vonHoldt BM, Pollinger JP, Earl DA et al (2011) A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids. Genome Res. Advance online publication 12 May 2011. doi: 10.1101/gr.116301.110
  82. Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256PubMedCrossRefGoogle Scholar
  83. Walker DJ (2001) Landscape complexity and vegetation dynamics in Riding Mountain National Park, Canada. PhD Dissertation, University of Manitoba, WinnipegGoogle Scholar
  84. Waser PM, Strobeck C (1998) Genetic signatures of interpopulation dispersal. Trends Ecol Evol 13:43–44PubMedCrossRefGoogle Scholar
  85. Watson A, Moss R, Parr R, Mountford MD, Rothery P (1994) Kin landownership, differential aggression between kin and non-kin, and population fluctuations in red grouse. J Anim Ecol 63:39–50CrossRefGoogle Scholar
  86. Weaver JL, Paquet PC, Ruggiero LF (1996) Resilience and conservation of large carnivores in the Rocky Mountains. Conserv Biol 10:964–976CrossRefGoogle Scholar
  87. 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 14:917–931PubMedCrossRefGoogle Scholar
  88. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analyses of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  89. Wheeldon TJ, Patterson BR, White BN (2010) Sympatric wolf and coyote populations of the western Great Lakes region are reproductively isolated. Mol Ecol 19:4428–4440PubMedCrossRefGoogle Scholar
  90. Whittington J, Cassady St. Clair C, Mercer G (2005) Spatial responses of wolves to roads and trails in mountain valleys. Ecol Appl 15:533–543CrossRefGoogle Scholar
  91. Wilson PJ, Grewal S, Lawford ID et al (2000) DNA profiles of the eastern Canadian wolf and the red wolf provide evidence for a common evolutionary history independent of the gray wolf. Can J Zool 78:2156–2166CrossRefGoogle Scholar
  92. Wilson PJ, Grewal SK, Mallory FF, White BN (2009) Genetic characterization of hybrid wolves across Ontario. J Hered 100:S80–S89CrossRefGoogle Scholar
  93. Wydeven AP, Schultz RN, Thiel RP (1995) Monitoring of a recovering gray wolf population in Wisconsin, 1979–1991. In: Carbyn LN, Fritts SH, Seip DR (eds) Ecology and conservation of wolves in a changing world. Canadian Circumpolar Institute, Occasional Publication No. 35, pp 147–156Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Astrid V. Stronen
    • 1
    • 2
  • Graham J. Forbes
    • 1
  • Paul C. Paquet
    • 3
  • Gloria Goulet
    • 4
  • Tim Sallows
    • 5
  • Marco Musiani
    • 6
  1. 1.Department of BiologyUniversity of New BrunswickFrederictonCanada
  2. 2.Mammal Research InstitutePolish Academy of SciencesBiałowieżaPoland
  3. 3.Raincoast Conservation FoundationDenny IslandCanada
  4. 4.Canadian Wildlife Service, Environment CanadaWinnipegCanada
  5. 5.Riding Mountain National ParkWasagamingCanada
  6. 6.Faculty of Environmental DesignUniversity of CalgaryCalgaryCanada

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