Abstract
Conflicting interpretations of the influence of coyote hybridization on wolf recovery in the western Great Lakes (WGL) states have stemmed from disagreement over the systematics of North American wolves. Questions regarding their recovery status have resulted. We addressed these issues with phylogenetic and admixture analysis of DNA profiles of western wolves, WGL states wolves and Wisconsin coyotes developed from autosome and Y-chromosome microsatellites and mitochondrial DNA control region sequence. Hybridization was assessed by comparing the haplotypes exhibited by sympatric wolves and coyotes. Genetic variability and connectivity were also examined. These analyses support the recognition of Canis lycaon as a unique species of North American wolf present in the WGL states and found evidence of hybridization between C. lupus and C. lycaon but no evidence of recent hybridization with sympatric coyotes. The recolonized WGL states wolves are genetically similar to historical wolves from the region and should be considered restored.
Similar content being viewed by others
References
Adams JR, Kelly BT, Waits LP (2003) Using faecal DNA sampling and GIS to monitor hybridization between red wolves (Canis rufus) and coyotes (Canis latrans). Mol Ecol 12:2175–2186
Aggarwal RK, Kivisild T, Ramadevi J, Singh L (2007) Mitochondrial DNA coding region sequences support the phylogenetic distinction of two Indian wolf species. J Zoolog Syst Evol Res 45:163–172
Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Bannasch DL, Bannasch MJ, Ryun JR, Famula TR, Pedersen NC (2005) Y chromosome haplotype analysis in purebred dogs. Mamm Genome 16:273–280
Berger KM, Gese EM (2007) Does interference competition with wolves limit the distribution and abundance of coyotes? J Anim Ecol 76:1075–1085
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170
El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morroco. Theor Appl Genet 92:832–839
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Fain SR, Hamlin BC, Straughan DJ (2000) Genetic variation in the river sturgeon scaphirhynchus (Acipenseridae) as inferred from partial mtDNA sequences of cytochrome b. Final report, pp 1–20. http://www.lab.fws.gov/pdfs/Fain_etal.2000.pdf
Felsenstein J (1989) PHYLIP––phylogeny inference package (version 3.2). Cladistics 5:164–166
Felsenstein J (1995) PHYLIP––phylogeny inference package (version 3.57). http://evolution.genetics.washington.edu/phylip.html. Updated from Felsenstein (1989)
Fish US, Service Wildlife (2007) Proposed rule. Fed Reg 72:6051–6103
Forbes SH, Boyd DK (1996) Genetic variation of naturally colonizing wolves in the central Rocky Mountains. Conserv Biol 10:1082–1090
Forbes SH, Boyd DK (1997) Genetic structure and migration in native and reintroduced Rocky Mountain wolf populations. Conserv Biol 11:1226–1234
Garcia-Moreno J, Roy MS, Geffen E, Wayne RK (1996) Relationships and genetic purity of the endangered Mexican wolf based on analysis of microsatellite loci. Conserv Biol 10:376–387
Gottelli D, Sillero-Zubirl C, Applebaum GD, Roy MS, Girman DJ, Garcia-Moreno J, Ostrander EA, Wayne RK (1994) Molecular genetics of the most endangered canid: the Ethiopian wolf Canis simensis. Mol Ecol 3:301–312
Goudet J (1995) FSTAT (vers. 1.2) a computer program to calculate F-statistics. J Hered 86:485–486
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html. Updated from Goudet (1995)
Grewal SK, Wilson PJ, Kung TK, Sharmi K, Theberge MT, Theberge JB, White BN (2004) A genetic assessment of the eastern wolf (Canis lycaon) in Algonquin Provincial Park. J Mamm 85:625–632
Hailer F, Leonard JA (2008) Hybridization among three native North American Canis species in a region of natural sympatry. PLoS One. doi:10.1371/journal.pone.0003333
Hellborg L, Ellegren H (2004) Low levels of nucleotide diversity in mammalian Y chromosomes. Mol Biol Evol 21:158–163
Hope J (1994) Wolves and wolf hybrids as pets are big business––but a bad idea. Smithsonian 25:34–45
Ito H, Nara H, Inoue-Muayama M, Shimada MK, Koshimura A, Ueda Y, Kitagawa H, Takeuchi Y, Mori Y, Murayama Y, Morita M, Iwasaki T, Ota K, Tanabe Y, Ito S (2004) Allele frequency distribution of the canine dopamine receptor D4 gene exon III and I in 23 breeds. J Vet Med Sci 66:815–820
Jobling MA, Heyer E, Dieltjes P, deKnijff P (1999) Y-chromosome-specific microsatellite mutation rates re-examined using a minisatellite, MSY1. Hum Mol Genet 8:2117–2120
Koblmüller S, Nord M, Wayne RK, Leonard JA (2009) Origin and status of the Great Lakes wolf. Mol Ecol 18:2313–2326
Kolenosky GB, Stanfield R (1975) Morphological and ecological variation among gray wolves (Canis lupus) of Ontario. In: Fox MW (ed) The wild canids––their systematics, behavioral ecology and evolution. Van Nostrand, New York
Kyle CJ, Johnson AR, Patterson BR, Wilson PJ, Shami K, Grewal SK, White BN (2006) Genetic nature of eastern wolves: past, present and future. Conserv Genet 7:273–287
Kyle CJ, Johnson AR, Patterson BR, Wilson PJ, White BN (2008) The conspecific nature of eastern and red wolves: conservation and management implications. Conserv Genet. doi:10.1007/s10592-007-9380-5
Lehman N, Eisenhawer A, Hansen K, Mech LD, Peterson RO, Gogan PJP, Wayne RK (1991) Introgression of coyote mitochondrial DNA into sympatric North American gray wolf populations. Evolution 45:104–119
Leonard JA, Wayne RK (2008a) Wishful thinking: imagining that the current Great Lakes wolf is the same entity that existed historically. Biol Lett. doi:10.1098/rsbl.2008.0533
Leonard JA, Wayne RK (2008b) Native Great Lakes wolves were not restored. Biol Lett 4:95–98
Lucchini V, Galov A, Randi E (2004) Evidence of genetic distinction and long-term population decline in wolves (Canis lupus) in the Italian Apennines. Mol Ecol 13:523–536
Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237
Mech LD (1974) Canis lupus. Mammalian Species 37:1–6
Mech LD (2008) Crying wolf: concluding that wolves were not restored. Biol Lett. doi:10.1098/rsbl.2008.0440
Mech LD, Federoff NE (2002) Alpha1-antitrypsin polymorphism and systematics of eastern North American wolves. Can J Zool 80:961–963
Mech LD, Fritts SH, Radde G, Paul WJ (1988) Wolf distribution in Minnesota relative to road density. Wildlife Soc B 16:85–88
Mech LD, Fritts SH, Wagner D (1995) Minnesota wolf dispersal to Wisconsin and Michigan. Am Mid Nat 133:368–370
Mladenoff DJ, Sickley TA, Haight RG, Wydevan AP (1995) A regional landscape analysis and prediction of favorable gray wolf habitat in the northern Great Lakes Region. Conserv Biol 9:279–294
Muñoz-Fuentes V, Darimont CT, Wayne RK, Paquet PC, Leonard J (2009a) Ecological factors drive differentiation in wolves from British Columbia. J Biogeograp. doi:10.1111/j.1365-2699.2008.02067.x
Muñoz-Fuentes V, Darimont CT, Paquet PC, Leonard J (2009b) The genetic legacy of extirpation and re-colonization in Vancouver Island wolves. Conserv Genet. doi:10.1007/s10592-009-9974-1
Musiani M, Leonard J, Cluff HD, Gates CC, Mariani S, Paquet PC, Vilas C, Wayne RK (2007) Differentiation of tundra/taiga and boreal coniferous forest wolves: genetics, coat color and association with migratory caribou. Mol Ecol 16:4149–4170
Natanaelsson C, CR Oskarsson M, Angleby H, Lundeberg J, Kirkness E, Savilainen P (2006) Dog Y chromosomal DNA sequence: identification, sequencing and SNP discovery. BMC Genet 7:45. doi:10.1186/1471-2156-7-45
Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Nowak RM (1983) A perspective on the taxonomy of wolves in North America. In: Carbyn LN (ed) Wolves in Canada and Alaska: their status, biology, and management. Report series, no. 45. Canadian Wildlife Service, Edmonton, Alberta, pp 10–19
Nowak RM (1995) Another look at wolf taxonomy. In: Carbyn LN, Fritts SH, Seip DR (eds) Ecology and conservation of wolves in a changing world. Canadian Circumpolar Institute, Edmonton, Alberta, pp 375–397
Nowak RM (2002) The original status of wolves in eastern North America. Southeast Nat 1:95–130
Nowak RM (2003) Wolf evolution and taxonomy. In: Mech LD, Boitani L (eds) Wolves, behavior, ecology, and conservation. Chicago, University of Chicago Press, pp 239–258
Nowak RM (2009) Chapter 15, taxonomy, morphology, and genetics of wolves in the Great Lakes region. In: Wydeven AP, Van Deelen TR, Heske E (eds) Recovery of wolves in the great lakes region. New York, Springer, pp 233–250
Ostrander EA, Sprague GF, Rine J (1993) Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. Genomics 16:207–213
Pacquet PC (1992) Prey use strategies of sympatric wolves and coyotes in Riding Mountain National Park, Manitoba. J Mamm 73:337–343
Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci. 12:357–358. http://taxonomy.zoology.gla.ac.uk/rod/treeview.html
Pilgrim KL, Boyd DK, Forbes SH (1998) Testing for wolf-coyote hybridization in the Rocky Mountains using mitochondrial DNA. J Wildl Manag 62:683–686
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 90:502–503
Primmer CR, Saino N, Moller AP, Ellegren H (1998) Unravelling the processes of microsatellite evolution through analysis of germ line mutations in Barn Swallows Hirundo rustica. Mol Biol Evol 15:1047–1054
Pritchard JK, Wen W (2003) Documentation for STRUCTURE software: version 2. http://pritch.bsd.uchicago.edu
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Randi E, Lucchini V (2002) Detecting rare introgression of domestic dog genes into wild wolf (Canis lupus) populations by Bayesian admixture analysis of microsatellite variation. Conserv Genet 3:31–45
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenism. J Hered 86:248–249. http://kimura.univ-montp2.fr/~rousset/Genepop.htm
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Roy MS, Geffen E, Smith D, Ostrander EA (1994) Patterns of differentiation and hybridization in North American wolflike canids, revealed by analysis of microsatellite loci. Mol Biol Evol 11:553–570
Sacks BN, Brown SK, Ernest HB (2004) Population structure of California coyotes corresponds to habitat-specific breaks and illuminates species history. Mol Ecol 13:1265–1275
Saetre P, Lindberg J, Leonard JA, Olsson K, Pettersson U, Ellegren H, Bergstrom TF, Vila C, Jazin E (2004) From wild wolf to domestic dog: gene expression changes in the brain. Mol Brain Res 126:198–206
Schneider S, Kueffer JM, Roessli D, Excoffier L (2000) Arlequinn ver 2000: a software for population genetics data analysis. Genetics and Biometry Lab, University of Geneva, Geneva
Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452
Shami K (2002) Evaluating the change in distribution of the eastern timber wolf (Canis lycaon) using the Y-chromosome. M.Sc. Thesis, McMaster University, 73 pp
Skeel MA, Carbyn LN (1977) The morphological relationship of gray wolves (Canis lupus) in national parks of central Canada. Can J Zool 55:737–747
Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65
Sundqvist A-K, Ellegren H, Olivier M, Vila C (2001) Y chromosome haplotyping in Scandinavian wolves (Canis lupus) based on microsatellite markers. Mol Ecol 10:1959–1966
Sundqvist A-K, Björnerfeldt S, Leonard JA, Hailer F, Hedhammar Å, Ellegren H, Vila C (2006) Unequal contribution of sexes in the origin of dog breeds. Genetics 172:1121–1128
Thiel RP, Hammill JH (1988) Wolf specimens in Upper Michigan, 1960–1986. Jack-Pine Warbler 66:153–179
Treves A (2008) Beyond recovery: Wisconsin’s wolf policy 1980–2008. Hum Dimens Wild 13:329–338. doi:10.1080/1087200802277716
U.S. Fish and Wildlife Service (1992) Recovery plan for the eastern timber wolf. Twin Cities, Minnesota, 73 pp
Valdes AM, Slatkin M, Freimer NB (1993) Allele frequencies at microsatellite loci: the stepwise mutation model revisited. Genetics 133:737–749
Van den Berg L, Kwant L, Hestand MS, van Oost BA, Leegwater PAJ (2005) Structure and variation of three canine genes involved in serotonin binding and transport: the serotonin receptor IA gene (htrIA), serotonin receptor 2A gene (htr2A), and serotonin transporter gene (slc6A4). J Hered 96:786–796
Verardi A, Lucchini V, Randi E (2006) Detecting introgressive hybridization between free-ranging domestic dogs and wild wolves (Canis lupus) by admixture linkage disequilibrium analysis. Mol Ecol 15:2845–2855
Vila C, Wayne RK (1999) Hybridization between wolves and dogs. Conserv Biol 13:195–198
Vila C, Walker C, Sundqvist A-K, Flagstad Ø, Andersone Z, Casulli A, Kojola I, Valdmann H, Halverson J, Ellegren H (2003) Combined use of maternal, paternal and bi-parental genetic markers for the identification of wolf–dog hybrids. Heredity 90:17–24
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wheeldon T, White BN (2009) Genetic analysis of historic western Great Lakes region wolf samples reveals early Canis lupus/lycaon hybridization. Biol Lett. doi:10.1098/rsbl.2008.0516
Wilson PJ, Grewal S, Lawford ID, Heal JNM, Granacki AG, Pennock D, Theberge JB, Theberge MT, Voigt DR, Waddell W, Chambers RC, Paquet PC, Goulet G, Cluff D, White BN (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 78:2156–2166
Wilson PJ, Grewal S, McFadden T, Chambers RC, White BN (2003) Mitochondrial DNA extracted from eastern North American wolves killed in the 1800 s is not of gray wolf origin. Can J Zool 81:936–940
Wilson PJ, Grewal SK, Mallory FF, White BN (2009) Genetic characterization of hybrid wolves across Ontario. J Hered 100(Supplement 1):S80–S89
Wisconsin Department of Natural Resources (WIDNR) 1999 wolf management plan. http://dnr.wi.gov/org/land/er/publications/wolfplan/toc.htm. Madison, WI
Wydevan 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, Edmonton, pp 147–156
Wydeven AP, Weidenhoeft JE, Kohn BE, Thiel RP, Schultz RN, Boales SR (1999) Progress report of wolf population monitoring in Wisconsin for the period April–September 1999. Wisconsin Department of Natural Resources. http://www.timberwolfinformation.org/updates/oct201999/october1999wolfprogressreport.pdf
Young SP, Goldman GE (1944) The wolves of North America. American Wildlife Institute, Washington, DC
Acknowledgements
We are grateful for the help of the many colleagues who have provided the wolf samples that this work is based upon, particularly Adrian Wydevan (WIDNR), Peter Gogan (NPS), Thomas Cooley (MIDNR), Dave Duncan (USFWS) and Ed Spoon (USFWS). We also thank Thomas Cooley (MIDNR), Paula Holahan (Univ of WI) and Nancy Thomas (WIDNR) for morphological characterization of some of the wolves in this study and Jennifer Leonard (Uppsala Univ) for providing sequence data that was invaluable for the confirmation of some of the haplotypes we identified. We also would like to thank Brian Hamlin and Doina Voin (USFWS) for laboratory and analytical assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service.
Appendix
Appendix
Rights and permissions
About this article
Cite this article
Fain, S.R., Straughan, D.J. & Taylor, B.F. Genetic outcomes of wolf recovery in the western Great Lakes states. Conserv Genet 11, 1747–1765 (2010). https://doi.org/10.1007/s10592-010-0068-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-010-0068-x