Abstract
Hybridization between wild and domestic species is of conservation concern because it can result in the loss of adaptations and/or disappearance of a distinct taxon. Wolves from Vancouver Island, British Columbia (Canada), have been subject to several eradication campaigns during the twentieth century and were considered virtually extirpated between 1950 and 1970. In this study, we use control region mitochondrial DNA sequences and 13 autosomal microsatellite loci to characterize Vancouver Island wolves as well as dogs from British Columbia. We observe a turnover in the haplotypes of wolves sampled before and after the 1950–1970 period, when there was no permanent wolf population on the island, supporting the probable local extinction of wolves on Vancouver Island during this time, followed by re-colonization of the island by wolves from mainland British Columbia. In addition, we report the presence of a domestic dog mtDNA haplotype in three individuals eliminated in 1986 that were morphologically identified as wolves. Here we show that Vancouver Island wolves were also identified as wolves based on autosomal microsatellite data. We attribute the hybridization event to the episodically small size of this population during the re-colonization event. Our results demonstrate that at least one female hybrid offspring, resulting from a cross of a male wolf and a female dog or a female hybrid pet with dog mtDNA, successfully introgressed into the wolf population. No dog mtDNA has been previously reported in a population of wild wolves. Genetic data show that Vancouver Island wolves are distinct from dogs and thus should be recognized as a population of wild wolves. We suggest that the introgression took place due to the Allee effect, specifically a lack of mates when population size was low. Our findings exemplify how small populations are at risk of hybridization.
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Adams JR, Leonard JA, Waits LP (2003) Widespread occurrence of a domestic dog mitochondrial DNA haplotype in southeastern US coyotes. Mol Ecol 12:541–546. doi:10.1046/j.1365-294X.2003.01708.x
Adams JR, Lucash C, Schutte L, Waits LP (2007) Locating hybrid individuals in the red wolf (Canis rufus) experimental population area using a spatially targeted sampling strategy and faecal DNA genotyping. Mol Ecol 16:1823–1834. doi:10.1111/j.1365-294X.2007.03270.x
Allee WC (1931) Animal aggregations. University of Chicago Press, Chicago
Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229
Andersone Z, Lucchini V, Randi E, Ozolins J (2002) Hybridisation between wolves and dogs in Latvia as documented using mitochondrial and microsatellite DNA markers. Mammal Biol 67:79–90. doi:10.1078/1616-5047-00012
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bohomme F (1996–2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France. URL: http://www.genetix.univ-montp2.fr/genetix/genetix.htm, last accessed: 26th January 2009
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300
Bibikov D (1982) Wolf ecology and management in the USSR. In: Harrington FH, Paquet P (eds) Wolves of the world. Noyes, Park Ridge, pp 120–133
Björnerfeldt S, Webster MT, Vilà C (2006) Relaxation of selective constraint on dog mitochondrial DNA following domestication. Genome Res 16:990–994. doi:10.1101/gr.5117706
Boitani L (1982) Wolf management in intensively used areas of Italy. In: Harrington FH, Paquet P (eds) Wolves of the world. Noyes, Park Ridge, pp 158–172
Broquet T, Petit M (2004) Quantifying genotyping errors in non-invasive population genetics. Mol Ecol 13:3601–3608. doi:10.1111/j.1365-294X.2004.02352.x
Charpentier MJE, Williams CV, Drea CM (2008) Inbreeding depression in ring-tailed lemurs (Lemur catta): genetic diversity predicts parasitism, immunocompetence and survivorship. Conserv Genet 9:1605–1615. doi:10.1007/s10592-007-9499-4
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660. doi:10.1046/j.1365-294x.2000.01020.x
Darimont CT, Paquet PC (2002) The gray wolves, Canis lupus, of British Columbia’s central and north coast: distribution and conservation assessment. Can Field Nat 116:416–422
Francisco LV, Langston AA, Mellersh CS, Neal CL, Ostrander EA (1996) A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mamm Genome 7:359–362. doi:10.1007/s003359900104
Gottelli D, Sillerozubiri C, Applebaum GD, Roy MS, Girman DJ, García-Moreno J, Ostrander EA, Wayne RK (1994) Molecular genetics of the most endangered canid - the Ethiopian wolf Canis simensis. Mol Ecol 3:301–312. doi:10.1111/j.1365-294X.1994.tb00070.x
Hebert DH, Youds J, Davies R, Langin H, Janz D, Smith GW (1982) Preliminary investigations of the Vancouver Island wolf (Canis lupus crassodon) prey relationships. In: Harrington FH, Paquet P (eds) Wolves of the world. Noyes, Park Ridge, pp 54–68
Hedrick PW, Fredrickson RJ (2008) Captive breeding and the reintroduction of Mexican and red wolves. Mol Ecol 17:344–350. doi:10.1111/j.1365-294X.2007.03400.x
Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189. doi:10.1111/j.1471-8286.2004.00845.x
Leonard JA, Wayne RK, Wheeler J, Valádez R, Guillén S, Vilà C (2002) Ancient DNA evidence for old world origin of new world dogs. Science 298:1613–1616. doi:10.1126/science.1076980
Mendelssohn H (1982) Wolves in Israel. In: Harrington FH, Paquet P (eds) Wolves of the world. Noyes, Park Ridge, pp 173–194
Muñoz-Fuentes V, Vilà C, Green AJ, Negro JJ, Sorenson M (2007) Hybridization between white-headed ducks and introduced ruddy ducks in Spain. Mol Ecol 16:629–638. doi:10.1111/j.1365-294X.2006.03170.x
Muñoz-Fuentes V, Darimont CT, Wayne RK, Paquet P, Leonard JA (2009) Ecological factors drive differentiation in wolves from British Columbia. J Biogeogr 36:1516–1531. doi:10.1111/j.1365-2699.2008.02067.x
Ostrander EA, Sprague GF Jr, Rine J (1993) Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in the dog. Genomics 16:207–332. doi:10.1006/geno.1993.1160
Paquet PC, Alexander SM, Swan PL, Darimont CT (2006) The influence of natural landscape fragmentation and resource availability on connectivity and distribution of marine gray wolf (Canis lupus) populations on the Central Coast, British Columbia, Canada. In: Crooks K, Sanjayan MAE (eds) Connectivity conservation. Society for Conservation Biology. Cambridge University Press, Cambridge, pp 130–156
Park SDE (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. Ph. D. Thesis, University of Dublin, Dublin, Ireland. URL: http://www.animalgenomics.ucd.ie/sdepark/ms-toolkit/, last accessed: 26th January 2009
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rambaut A (1996) Se-Al: Sequence alignment editor. Department of Zoology, University of Oxford, UK. URL: http://tree.bio.ed.ac.uk/software/seal/, last accessed: 26th January 2009
Randi E (2008) Detecting hybridization between wild species and their domesticated relatives. Mol Ecol 17:285–293. doi:10.1111/j.1365-294X.2007.03417.x
Randi E, Lucchini V (2002) Detecting rare introgression of domestic dog genes into wild wolf (Canis lupus) populations by Bayesian admixture analyses of microsatellite variation. Conserv Genet 3:31–45. doi:10.1023/A:1014229610646
Randi E, Lucchini V, Christensen MF, Mucci N, Funk SM, Dolf G, Loeschcke V (2000) Mitochondrial DNA variability in Italian and East European wolves: detecting the consequences of small population size and hybridization. Conserv Biol 14:464–473. doi:10.1046/j.1523-1739.2000.98280.x
Raymond M, Rousset F (1995) Genepop (Version-1.2)—population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reid R, Janz D (1995) Economic evaluation of Vancouver Island wolf control. In: Carbyn L, Fritts S, Seip D (eds) Ecology and conservation of wolves in a changing world. Canadian Circumpolar Institute, Occasional Publication No. 35, University of Alberta, Edmonton, Alberta, Canada
Scott BMV, Shackleton DM (1982) A preliminary study of the social organization of the Vancouver Island wolf. In: Harrington FH, Paquet P (eds) Wolves of the world. Noyes, Park Ridge, pp 12–25
Sefc KM, Payne RB, Sorenson MD (2003) Microsatellite amplification from museum feather samples: effects of fragment size and template concentration on genotyping errors. Auk 120:982–989. doi:10.1642/0004-8038(2003)120[0982:MAFMFS]2.0.CO;2
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. Anim Genet 25:122
Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264. doi:10.1073/pnas.0403809101
Stephens PA, Sutherland WJ, Freckleton RP (1999) What is the Allee effect? Oikos 87:185–190. doi:10.2307/3547011
Sundqvist A-K, Björnerfeldt S, Leonard JA, Hailer F, Hedhammar Å, Ellegren H, Vilà C (2006) Unequal contribution of sexes in the origin of dog breeds. Genetics 172:1121–1128
Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very los DNA quantities using PCR. Nucleic Acids Res 24:3189–3194. doi:10.1093/nar/24.16.3189
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. doi:10.1111/j.1471-8286.2004.00684.x
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
Vilà C, Wayne RK (1999) Hybridization between wolves and dogs. Conserv Biol 13:195–198. doi:10.1046/j.1523-1739.1999.97425.x
Vilà C, Savolainen P, Maldonado JE, Amorim IR, Rice JE, Honeycutt RL, Crandall KA, Lundeberg J, Wayne RK (1997) Multiple and ancient origins of the domestic dog. Science 276:1687–1689. doi:10.1126/science.276.5319.1687
Vilà C, Amorim IR, Leonard JA, Posada D, Castroviejo J, Petrucci-Fonseca F, Crandall KA, Ellegren H, Wayne RK (1999) Mitochondrial DNA phylogeography and population history of the grey wolf Canis lupus. Mol Ecol 8:2089–2103. doi:10.1046/j.1365-294x.1999.00825.x
Vilà C, Sundqvist A-K, Flagstad Ø, Seddon J, Björnerfeldt S, Kojola I, Casulli A, Sand H, Wabakken P, Ellegren H (2003a) Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proc R Soc Lond B Biol Sci 270:91–97. doi:10.1098/rspb.2002.2184
Vilà C, Walker C, Sundqvist AK, Fagstad Ø, Andersone Z, Casulli A, Kojola I, Valdmann H, Halverson J, Ellegren H (2003b) Combined use of maternal, paternal and bi-parental genetic markers for the identification of wolf-dog hybrids. Heredity 90:17–24. doi:10.1038/sj.hdy.6800175
Yang DY, Eng B, Waye JS, Saunders SR (1998) Technical note: improved DNA extraction from ancient bones using silica-based spin columns. Am J Phys Anthropol 105:539–543. doi:10.1002/(SICI)1096-8644(199804)105:4<539:AID-AJPA10>3.0.CO;2-1
Young SP, Goldman EA (1944) The wolves of North America. Dover, New York
Acknowledgments
We thank Heather Bryan for sharing dog samples with us and to Helen Schwantje of the British Columbia Ministry of Environment for providing contemporary wolf samples. We thank Rex Kenner of the University of British Columbia Cowan Vertebrate Museum and Jim Cosgrove from the Royal British Columbia Museum for access to samples in collections. We are also thankful to Carles Vilà and Robert K. Wayne for a critical reading of the manuscript. Funding was provided by the European Union Marie Curie Fellowship programme, the National Science and Engineering Research Council of Canada Postdoctoral Fellowship programme, the National Science Foundation, USA (OPP-0352634), the Spanish Ministry of Education, the Swedish Research Council, Raincoast Conservation Foundation, Wilburforce Foundation and World Wildlife Fund—Canada. The Center for Conservation & Evolutionary Genetics, National Zoological Park, Smithsonian Institution, USA, provided logistical support.
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Muñoz-Fuentes, V., Darimont, C.T., Paquet, P.C. et al. The genetic legacy of extirpation and re-colonization in Vancouver Island wolves. Conserv Genet 11, 547–556 (2010). https://doi.org/10.1007/s10592-009-9974-1
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DOI: https://doi.org/10.1007/s10592-009-9974-1