Differentiation of tundra/taiga and boreal coniferous forest wolves: Genetics, coat colour and association with migratory caribou

Molecular Ecology

Volumn 16, Issue 19, 2007, Pages 4149-4170

  Musiani, Marco ^a   Leonard, Jennifer A ^b,c,d   Cluff, H Dean ^e   Gates, C Cormack ^a   Mariani, Stefano ^f   Paquet, Paul C ^a   Vilà, Carles ^d   Wayne, Robert K ^b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DEPARTMENT OF PALEOBIOLOGY   (United States)

^d UPPSALA UNIVERSITY   (Sweden)

^e DEPARTMENT OF ENVIRONMENT AND NATURAL RESOURCES   (Canada)

^f UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Canis lupus; Foraging ecology; Gene flow; Grey wolf; Migratory behaviour; Phylogeography

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; CHEMISTRY; COLOR; DNA SEQUENCE; FEMALE; GENE FLOW; GENETIC SELECTION; GENETICS; GEOGRAPHY; HAIR; HISTOLOGY; MALE; PHENOTYPE; PHYSIOLOGY; POPULATION MIGRATION; PREDATION; REINDEER; SEX DIFFERENCE; TERRITORIALITY; TREE; WOLF; Y CHROMOSOME;

ANIMAL MIGRATION; ANIMALS; COLOR; DNA, MITOCHONDRIAL; FEMALE; GENE FLOW; GEOGRAPHY; HAIR; MALE; MICROSATELLITE REPEATS; PHENOTYPE; PREDATORY BEHAVIOR; REINDEER; SELECTION (GENETICS); SEQUENCE ANALYSIS, DNA; SEX FACTORS; TERRITORIALITY; TREES; WOLVES; Y CHROMOSOME;

CANIDAE; CANIS FAMILIARIS; CANIS LUPUS; MAMMALIA; RANGIFER TARANDUS;

EID: 34748919495     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2007.03458.x     Document Type: Article

References (128)

1. Anderson MJ (2004) distlm Version 5. A FORTRAN Computer Program to Calculate a Distance-Based Multivariate Analysis for a Linear Model. Department of Statistics. University of Auckland, New Zealand. Available at URL: http://www.stat.auckland.ac.nz/∼mja.
2. Anderson MJ, Legendre P (1999) An empirical comparison of permutation methods for tests of partial regression coefficients in a linear model. Journal of Statistical Computation and Simulation, 62, 271 303.
3. Avise JC (2000) Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, Massachusetts.
4. Ballard WB, Ayres LA, Krausman PR, Reed DJ, Fancy SG (1997) Ecology of wolves in relation to a migratory caribou herd in northwest Alaska. Wildlife Monograph, 135, 1 47.
5. Barton NH, Keightley PD (2002) Understanding quantitative genetic variation. Nature Genetics, 3, 11 21.
6. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) genetix Version 4. 05 Logiciel sous Windows pour la génétique des Populations. Laboratoire Génome, Populations, Interactions. CNRS UMR 5000, Université de Montpellier II, Montpellier, France.
7. Birch LL (1999) Development of food preferences. Annual Review of Nutrition, 19, 41 62.
8. Bliss LC (1988) Arctic tundra and polar desert biome. In : North American Terrestrial Vegetation (eds Barbour MG, Billings WD), pp. 1 32. Cambridge University Press, Cambridge, UK.
9. Calef G (1981) Caribou and the Barren-Lands. Canadian Arctic resources Committee, Ottawa, Firefly Books Limited, Toronto, Canada.
10. Carmichael LE, Nagy JA, Larter NC, Strobeck C (2001) Prey specialization may influence patterns of gene flow in wolves of the Canadian Northwest. Molecular Ecology, 10, 2787 2798.
11. Carmichael LE, Krizan J, Nagy JA et al 2007) Historical and Ecological Determinants of Genetic Structure in Arctic Canids. Molecular Ecology, 16, 3466 3483.
12. Caughley G, Gunn A (1993) Dynamics of large herbivores in deserts: kangaroos and caribou. Oikos, 67, 47 55.
13. Clement M, Posada D, Crandall K (2000) tcs: a computer program to estimate gene genealogies. Molecular Ecology, 9, 167 1660.
14. Cluff D, Musiani M, Frame P, Paquet P, Gates C (2003) Multiple litters at den sites. Northwest Territories Wolf Notes, 7, 1 8.
15. Cook SJ, Norris DR, Theberge JB (1999) Spatial dynamics of a migratory wolf population in winter, south-central Ontario (1990-1995). Canadian Journal of Zoology, 77, 1740 1750.
16. Coulon A, Cosson JF, Angibault JM et al 2004) Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: an individual-based approach. Molecular Ecology, 13, 2841 2850.
17. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution, 15, 290 295.
18. Davis JM, Stamps JA (2004) The effect of natal experience on habitat preferences. Trends in Ecology & Evolution, 19, 411 416.
19. Delaney KS, Wayne RK (2005) Adaptive units for conservation: population distinction and historic extinctions in the island scrub-jay. Conservation Biology, 19, 523 533.
20. Doncaster CP (1990) Non-parametric estimates of interaction from radio-tracking data. Journal of Theoretical Biology, 143, 431 443.
21. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Molecular Ecology, 11, 2571 2581.
22. Elliot-Fisk DL (1988) The boreal forest. In : North American Terrestrial Vegetation (eds Barbour MG, Billings WD), pp. 33 62. Cambridge University Press, London.
23. Estes JA, Riedman ML, Staedle MM, Tinker MT, Lyon BE (2003) Individual variation in prey selection by sea otters: patterns, causes and implications. Journal of Animal Ecology, 72, 144 155.
24. ESWG (Ecological Stratification Working Group 1995) A National Ecological Framework for Canada. Environment Canada, State of the Environment Directorate, Ottawa/Hull, Canada.
25. Excoffier L, Heckel G (2006) Computer programs for population genetics data analysis: a survival guide. Nature Reviews Genetics, 7, 745 758.
26. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479 491.
27. Excoffier L, Laval G, Schneider S (2005) arlequin, version 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47 50.
28. FAO (2001) Global Forest Resources Assessment 2000. Main Report. FAO Forestry Paper, Rome, Italy.
29. Favre L, Balloux F, Goudet J, Perrin N (1997) Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field and microsatellite patterns. Proceedings of the Royal Society of London. Series B, Biological Sciences, 269, 127 132.
30. Felsenstein J (1995) phylip (Phylogeny Inference Package) Version 3.57c. University of Washington, Seattle, Washington.
31. Forbes SH, Boyd DK (1997) Genetic structure and migration in native and reintroduced Rocky Mountain wolf populations. Conservation Biology, 11, 1226 1234.
32. Francisco LV, Langston AA, Mellersh CS, Neal CL, Ostrander EA (1996) A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mammalian Genome, 7, 359 362.
33. Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology, 10, 2741 2752.
34. Freedman D, Lane D (1983) A nonstochastic interpretation of reported significance levels. Journal of Business and Economic Statistics, 1, 292 298.
35. Fritts SH (1982) Record dispersal by a wolf from Minnesota. Journal of Mammalogy, 64, 166 167.
36. Geffen E, Anderson MJ, Wayne RK (2004) Climate and habitat barriers to dispersal in the highly mobile gray wolf. Molecular Ecology, 13, 2481 2490.
37. Gipson PS, Bangs EE, Bailey TN et al 2002) Color patterns among wolves in western North America. Wildlife Society Bulletin, 30, 821 830.
38. Goldman EA (1944) The wolves of North America. Part 2. Classification of wolves. In : The Wolves of North America (eds Young SP, Goldman EA), pp. 389 636. Dover, New York /American Wildlife Institute, Washington, DC.
39. Guillot G, Mortier F, Estoup A (2005) geneland: a computer package for landscape genetics. Molecular Ecology Notes, 5, 708 711.
40. Gunn A, Dragon J, Boulanger J (2002) Seasonal Movements of Satellite-Collared Caribou from the Bathurst Herd. Final Report to the West Kitikmeot Slave Study Society. Government of the Northwest Territories, Yellowknife, Northwest Territories.
41. Guthrie RD (1990) Frozen Fauna of the Mammoth Steppe: The Story of Blue Babe. University of Chicago Press, Chicago.
42. Haber GC (1977) Socio-ecological Dynamics of Wolves and Prey in a Subarctic Ecosystem. PhD Thesis. University of British Columbia, Vancouver, Canada.
43. Hall ER (1981) The Mammals of North America. John Wiley and Sons, New York.
44. Hansen AJ, Neilson RP, Dale VH et al 2001) Global change in forests: response of species, communities, and biomes. Bioscience, 51, 765 779.
45. Harrington FH, Paquet PC, Ryon J, Fentress JC (1982) Monogamy in wolves: a review of the evidence. In : Wolves of the world (eds Harrington FH, Paquet PC), pp. 209 22. Noyes Publication, Park Ridge, New Jersey.
46. Hartl DL, Clark AG (1989) Principles of Population Genetics, 2nd edn. Sinauer & Associates, Sunderland, Massachusetts.
47. Heard DC, Williams TM (1992) Distribution of wolf dens on migratory caribou ranges in the Northwest Territories, Canada. Canadian Journal of Zoology, 70, 1504 1510.
48. Hedrick PW (1999) Highly variable loci and their interpretation in evolution and conservation. Evolution, 53, 313 318.
49. Hoelzel AR (1994) Genetics and ecology of whales and dolphins. Annual Review of Ecology and Systematics, 25, 377 399.
50. Hoelzel AR (1998) Genetic structure of cetacean populations in sympatry, parapatry, and mixed assemblages: implications for conservation policy. Journal of Heredity, 89, 451 458.
51. Hofer H, East ML (1993) The commuting system of Serengeti spotted hyenas: how a predator copes with migratory prey. I. Social organization. Animal Behaviour, 46, 547 557.
52. Hofer H, East ML (1995) Population dynamics, population size, and the commuting system of Serengeti spotted hyenas. In : Serengeti II. Dynamics, Management, and Conservation of an Ecosystem (eds Sinclair ARE, Arcese P), pp. 332 363. University of Chicago Press, Chicago.
53. Hooge PN, Eichenlaub B (1997) Animal Movement Extension to arcview, Ver. 1.1. Alaska Science Center - Biological Science Office, U.S. Geological Survey, Anchorage, Alaska.
54. Kelsall JP (1968) The Migratory Barren-ground Caribou of Canada. Canadian Wildlife Service, Queens Printer, Ottawa, Canada.
55. Kittel TGF, Steffen WL, Chapin FS III (2000) Global and regional modelling of arctic-boreal vegetation distribution and its sensitivity to altered forces. Global Change Biology, 6, 1 18.
56. Klein DR (1991) Caribou in the changing North. Applied Animal Behavior Sciences, 29, 279 291.
57. Kurtén B, Anderson E (1980) Pleistocene Mammals of North America. Columbia University Press, New York.
58. Kuyt E (1972) Food habits and ecology of wolves on the barren-ground caribou range in the Northwest Territories. Canadian Wildlife Service Report Series, 21, 1 36.
59. Lank DB, Butler RW, Ireland J, Ydenberg RC (2003) Effects of predation danger on migration strategies of sandpipers. Oikos, 103, 303 320.
60. Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multi-species responses in multi-factorial ecological experiments. Ecological Monographs, 69, 1 24.
61. Lehman N, Eisenhawer A, Hansen K et al 1991) Introgression of coyote mitochondrial DNA into sympatric North American grey wolf populations. Evolution, 45, 104 119.
62. Lenormand T (2002) Gene flow and the limits to natural selection. Trends in Ecology & Evolution, 17, 183 189.
63. Leonard JA, Vilà C, Wayne RK (2005) Legacy lost: genetic variability and population size of extirpated US gray wolves (Canis lupus). Molecular Ecology, 14, 9 17.
64. Lessa EP (1990) Multidimensional analysis of geographic genetic structure. Systematic Zoology, 39, 242 252.
65. Long AD, Lyman RF, Morgan AH, Langley CH, Mackay TFC (2000) Both naturally occurring insertions of transposable elements and intermediate frequency polymorphisms at the achaete-scute complex are associated with variation in bristle number in Drosophila melanogaster. Genetics, 154, 1255 1269.
66. Macdonald DW, Ball FG, Hough NG (1980) The evaluation of home-range size and configuration using radiotracking data. In : A Handbook on Biotelemetry and Radio Tracking (eds Amlaner CJ, Macdonald DW), pp. 405 424. Pergamon Press, Oxford, UK.
67. Magurran AE (1986) Individual differences in fish behavior. In : The Behavior of Teleost Fishes (ed. Pitcher TJ), pp. 338 365. Croon Helm Press, London.
68. Mardia KV, Kent JT, Bibby JM (1979) Multivariate Analysis. Academic Press, London.
69. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology, 82, 290 297.
70. McBride RT (1980) The Mexican Wolf (Canis lupus baileyi): A Historical Review and Observations on its Status and Distribution. Endangered Species Report, US Fish and Wildlife Service, Albuquerque, New Mexico.
71. Mech LD (1970) The Wolf : The Ecology and Behavior of an Endangered Species. University of Minnesota Press, Minneapolis, Minnesota.
72. Mech LD (1977) Productivity, mortality and population trend of wolves in northeastern Minnesota. Journal of Mammalogy, 58, 559 574.
73. Mech LD (1988) The Arctic Wolf : Living with the Pack. Voyageur Press, Stillwater, Minnesota.
74. Mech LD (2004) Is climate change affecting wolves in the High Arctic? Climatic Change, 67, 87 93.
75. Mech LD, Adams LG, Meier TJ, Burch JW, Dale BW (1998) The Wolves of Denali. University of Minnesota Press, Minneapolis, Minnesota.
76. Merrill SB, Mech LD (2000) Details of extensive movements by Minnesota wolves (Canis lupus). American Midland Naturalist, 144, 428 433.
77. Miller FL (1982) Caribou. In : Wild Mammals of North America (eds Chapman JA, Feldhamer GA), pp. 923 959. Johns Hopkins University Press, Baltimore, Maryland.
78. Minch E (1997) microsat 1.5d. Department of Genetics, University of Stanford, Stanford, California.
79. Morneau C, Payette S (2000) Long-term fluctuations of a caribou population revealed by tree-ring data. Canadian Journal of Zoology, 78, 1784 1790.
80. Murie A (1944) The Wolves of Mount McKinley. US National Park Service Fauna Series Number 5, Washington, DC.
81. Musiani M (2003) Conservation Biology and Management of Wolves and Wolf-human Conflicts in Western North America. PhD Thesis. University of Calgary, Alberta, Canada.
82. Musiani M, Paquet PC (2004) The practices of wolf persecution, protection and restoration in Canada and the USA. Bioscience, 54, 50 60.
83. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583 590.
84. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.
85. Nowak RM (1995) Another look at wolf taxonomy. In : Ecology and Conservation of Wolves in a Changing World (eds Carbyn LN, Fritts SH, Seip DR), pp. 375 397. Canadian Circumpolar Institute, Occasional Publication no. 35, Edmonton, Canada.
86. Obbard ME (1987) Fur grading and pelt identification, In : Wild Furbearer Management and Conservation in North America (eds Novak M, Baker JA, Obbard ME, Malloch B), pp. 717 826. Ontario Trappers Association, North Bay, Ontario, Canada.
87. van Oosterhout C, William F, Hutchinson DP, Wills M, Shipley P (2004) micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535 538.
88. Ostrander EA, Sprague GF Jr., Rine J (1993) Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. Genomics, 16, 207 213.
89. Overpeck J, Hughen K, Hardy D et al 1997) Arctic environmental change of the last four centuries. Science, 278, 1251 1256.
90. Paetkau D, Waits LP, Clarkson PL, Craighead L, Strobeck C (1997) An empirical evaluation of genetic distance statistics using microsatellite data from bear (Ursidae) populations. Genetics, 147, 1943 1957.
91. Parker GR (1973) Distribution and densities of wolves within barren-ground caribou range in northern mainland Canada. Journal of Mammalogy, 5, 341 348.
92. Partridge L, Green P (1985) Intraspecific feeding specializations and population dynamics. In : Behavioral Ecology (eds Sibley RM, Smith RH), pp. 207 226. Blackwell Press, Oxford, UK.
93. Peterson RO, Ciucci P (2003) The wolf as a carnivore. In : Wolves: Behavior, Ecology and Conservation (eds Mech LD, Boitani L), pp. 104 130. University of Chicago Press, Chicago.
94. Peterson RO, Page RE (1988) The rise and fall of the Isle Royale wolves 1975-1986. Journal of Mammalogy, 69, 89 99.
95. Petit E, Balloux F, Excoffier L (2002) Mammalian population genetics: why not Y? Trends in Ecology & Evolution, 17, 28 33.
96. Pilot M, Jedrzejewski W, Branicki W et al 2006) Ecological factors influence population genetic structure of European grey wolves. Molecular Ecology, 15, 4533 4553.
97. Posada D, Crandall KA (1998) modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817 818.
98. Post E, Stenseth NC (1999) Climatic variability, plant phenology, and northern ungulates. Ecology, 80, 1322 1339.
99. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945 959.
100. Prugnolle F, de Meeus T (2002) Inferring sex-biased dispersal from population genetic tools: a review. Heredity, 88, 161 165.
101. Pruitt WO (1959) Snow as a factor in the winter ecology of barren-ground caribou. Arctic, 12, 159 179.
102. Raymond M, Rousset F (1995) genepop (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248 249.
103. Rowe SJ (1972) Forest Regions of Canada. Publication No. 1300. Canadian Forestry Service, Ottawa, Canada.
104. 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. Molecular Biology and Evolution, 11, 553 570.
105. Sacks BN, Brown SK, Ernest HB (2004) Population structure of California coyotes corresponds to habitat-specific breaks and illuminates species history. Molecular Ecology, 13, 1265 1275.
106. Sacks BN, Mitchell BR, Williams CL, Ernest HB (2005) Coyote movements and social structure along a cryptic population genetic subdivision. Molecular Ecology, 14, 1241 1249.
107. Seaman DE, Powell RA (1996) An evaluation of the accuracy of kernel density estimators for home range analysis. Ecology, 77, 2075 2085.
108. Shibuya H, Collins BK, Huang TH-M, Johnson GS (1994) A polymorphic (AGGAAT)n tandem repeat in an intron of the canine von Willebrand factor gene. Animal Genetics, 25, 122.
109. Smith TB, Skúlason S (1996) Evolutionary significance of resource polymorphisms in fishes, amphibians and birds. Annual Review of Ecology and Systematics, 27, 111 133.
110. Sorenson MD, Sefc KM, Payne RB (2003) Speciation by host switch in parasitic indigobirds. Nature, 424, 928 931.
111. Stamps JA (2001) Habitat selection by dispersers: integrating proximate and ultimate approaches. In : Dispersal (eds Clobert J et al.), pp. 230 242. Oxford University Press, Oxford, UK.
112. Sundqvist AK, Ellegren H, Olivier M, Vilà C (2001) Y-chromosome haplotyping in Scandinavian wolves (Canis lupus) based on microsatellite markers. Molecular Ecology, 10, 1959 1966.
113. Sundqvist A-K, Bjornerfeldt S, Leonard JA et al 2006) Unequal contribution of sexes in the origin of dog breeds. Genetics, 172, 1121 1128.
114. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512 526.
115. Tew TE, Macdonald DW (1994) Dynamics of space use and male vigour amongst wood mice, Apodemus sylvaticus, in the cereal ecosystem. Behavioral Ecology and Sociobiology, 34, 337 345.
116. Theurillat J-P, Guisan A (2001) Potential impact of climate change on vegetation in the European Alps: a review. Climatic Change, 50, 77 109.
117. Trinkel M, Fleischmann PH, Steindorfer AF, Kastberger G (2004) Spotted hyenas (Crocuta crocuta) follow migratory prey. Seasonal expansion of a clan territory in Etosha, Namibia. Journal of Zoology, 264, 125 133.
118. Urquhart DR (1981) The Bathurst Herd: a Review and Analysis of Information Concerning the Bathurst Herd of Barren-Ground Caribou in the N.W.T. For the Period 6000 bc to 1980 ad, p. 204. NWT Wildlife Service, Yellowknife, Canada.
119. Vilà C, Amorim IR, Leonard JA et al 1999) Mitochondrial DNA phylogeography and population history of the grey wolf Canis lupus. Molecular Ecology, 8, 2089 2103.
120. Vilà C, Sundqvist AK, Flagstad Ø et al 2003) Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proceedings of the Royal Society of London. Series B, Biological Sciences, 270, 91 98.
121. Wakeley J (1993) Substitution rate variation among sites in hypervariable region 1 of human mitochondrial DNA. Journal of Molecular Evolution, 37, 613 623.
122. Walton LR, Cluff HD, Paquet PC, Ramsay MA (2001a) Movement patterns of barren-ground wolves in the central Canadian arctic. Journal of Mammalogy, 82, 867 876.
123. Walton LR, Cluff HD, Paquet PC, Ramsay MA (2001b) Performance of 2 models of satellite collars for wolves. Wildlife Society Bulletin, 29, 180 186.
124. Waser PM, Strobeck C (1998) Genetic signatures of interpopulation dispersal. TREE, 13, 43 44.
125. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358 1370.
126. Weladji RB, Klein DR, Holand Ø, Mysterud A (2002) Comparative response of Rangifer tarandus and other northern ungulates to climatic variability. Rangifer, 22, 33 50.
127. Wright S (1951) The genetical structure of populations. Annales Eugenics, 15, 323 354.
128. Young SP, Goldman EA (1944) The Wolves of North America. Dover, New York.