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Detecting rare introgression of domestic dog genes into wild wolf (Canis lupus) populations by Bayesian admixture analyses of microsatellite variation

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Abstract

Hybridization with free-ranging dogs isthought to threat the genetic integrity ofwolves in Europe, although available mtDNA dataevidenced only sporadic cases of crossbreeding.Here we report results of population assignmentand genetic admixture analyses in 107wild-living Italian wolves, 95 dogs including30 different breeds and feral dogs, andcaptive-reared wolves of unknown or hybridorigins, which were genotyped at 18microsatellites. Two Italian wolves showedunusually dark coats (``black wolves''), and oneshowed a spur in both hindlegs (``fifth fingerwolf''), suggesting hybridization. Italianwolves showed significant deficit ofheterozygotes, positive FIS values anddeviations from Hardy-Weinberg equilibrium.Genetic variability was significantlypartitioned between groups, suggesting thatwolves and dogs represent distinct gene pools.Multivariate ordination of individual genotypesand clustering of inter-individual geneticdistances split wolves and dogs into twodifferent clusters congruent with the priorphenotypic classification, but hybrids andwolves of unknown origin were not identifiedfrom genetic information alone. By contrast, aBayesian admixture analysis assigned all theItalian wolves and dogs to two differentclusters, independent of any prior phenotypicinformation, and simultaneously detected theadmixed gene composition of the hybrids, whichwere assigned to more than one cluster.Captive-reared wolves of unknown origin wereprevalently assigned to the Italian wolfpopulation. Admixture analyses showed that one``black wolf'' had mixed ancestry in the dog genepool and could be a hybrid, while the other twowolves with unusual phenotypes were assigned tothe Italian wolf population.

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References

  • Andersone Z, Lucchini V, Randi E, Ozolins J (submitted) Relationships between wolves and free-ranging dogs in Latvia.

  • Blanco JC, Reig S, de la Cuesta L (1992) Distribution, status and conservation problems of the wolf Canis lupus in Spain. Biol. Conserv., 60, 73–80.

    Google Scholar 

  • Boitani L (1982) Wolf management in intensively used areas in Italy. In: Wolves of the World: Perspectives of Behavior, Ecology and Conservation (eds. Harrington FH, Paquet PC), pp. 158–172. Noyes, Park Ridge, New York.

  • Boitani L (1983) Wolf and dog competition in Italy. Acta Zool. Fennica, 174, 259–264.

    Google Scholar 

  • Boitani L (1984) Genetic considerations on wolf conservation in Italy. Boll. Zool., 51, 367–373.

    Google Scholar 

  • Boitani L (1986) Dalla parte del lupo. Mondadori, Milano, Italy.

  • Boitani L (1995) Ecological and cultural diversities in the evolution of wolf-human relationships. In: Ecology and Conservation of Wolves in a Changing World (eds. Carbyn LN, Fritts SH, Seip DR), pp. 3–11. Canadian Circumpolar Institute, Occasional Pubblication No. 35. Edmonton, Alberta, Canada.

  • Boitani L (1999) Final Draft Action Plan for the Conservation of Wolves (Canis lupus) in Europe. Council of Europe, Strasbourg.

    Google Scholar 

  • Boitani L, Fabbri L (1983) Strategia nazionale di conservazione per il lupo (Canis lupus). Ric. Biol. Selv., 72, 1–31.

    Google Scholar 

  • Boitani L, Francisci F, Ciucci P, Andreoli P (1995) Population biology and ecology of feral dogs in central Italy. In: The domestic dog (ed. Serpell J), pp. 218–244. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforza LL (1994) High resolution human evolutionary trees with polymorphic microsatellites. Nature, 368, 455–457.

    Google Scholar 

  • Breitenmoser U (1998) Large predators in the Alps: The fall and rise of man's competitors. Biol. Conser., 83, 279–289.

    Google Scholar 

  • Brewster WG, Fritts SH (1995) Taxonomy and genetics of the gray wolf in western North America: A review. In: Ecology and Conservation of Wolves in a Changing World (eds. Carbyn LN, Fritts SH, Seip DR), pp. 353–373. Canadian Circumpolar Institute, Occasional Pubblication No. 35. Edmonton, Alberta, Canada.

  • Butler D (1994) Bid to protect wolves from genetic pollution. Nature, 370, 497.

    Google Scholar 

  • Colson I, Goldstein DB (1999) Evidence for complex mutations at microsatellite loci in Drosophila. Genetics, 152, 617–627.

    Google Scholar 

  • Cornuet J-M, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 2001–2014.

    Google Scholar 

  • Cornuet J-M, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics, 153, 1989–2000.

    Google Scholar 

  • Corsi F, Duprè E, Boitani L (1999) A large-scale model of wolf distribution in Italy for conservation planning. Cons. Biol., 13, 150–159.

    Google Scholar 

  • Delibes M (1990) Status and conservation needs of the wolf in the Council of Europe member States. Nature and Environment Series, Strasbourg, 47, 1–46.

    Google Scholar 

  • 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. U.S.A., 91, 3166–3170.

    Google Scholar 

  • DogMap Consortium (1999) DogMap: An international collaboration toward a low-resolution canine genetic marker map. J. Heredity, 90, 3–6.

    Google Scholar 

  • Dolf G, Schläpfer J, Gaillard C, Randi E, Lucchini V, Breitenmoser U, Stahlberger-Saitbekova N (2000) Differentiation between Italian wolf and domestic dog based on microsatellite analysis. Genet. Sel. Evol., 32, 533–541.

    Google Scholar 

  • Ellegren H, Savolainen P, Rosén B (1996) The genetical history of an isolated population of the endangered grey wolf Canis lupus: A study of nuclear and mitochondrial polymorphism. Phil. Trans. Roy. Soc. London B, 351, 1661–1669.

    Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: Applications to human mitochondrial DNA restriction data. Genetics, 131, 479–491.

    Google Scholar 

  • Forbes SH, Boyd DK (1997) Genetic structure and migration in native and reintroduced Rocky Mountain wolf populations. Cons. Biol., 11, 1226–1234.

    Google Scholar 

  • 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.

    Google Scholar 

  • Fredholm M, Winteroe AK (1995) Variation of short tandem repeats within and between species belonging to the Canidae family. Mamm. Genome, 6, 11–18.

    Google Scholar 

  • Funk SM, Lucchini V, Randi E (submitted) Microsatellite analysis reveals significant genetic differentiation between fragmented wolf populations in Europe and the Near East but no evidence for distinct management units.

  • Genovesi P, Dupré E (2000) Strategia nazionale di conservazione del lupo (Canis lupus): Indagine sulla presenza e la gestione di cani vaganti in Italia. Biol. Cons. Fauna, 104, 1–36.

    Google Scholar 

  • Gerloff U, Schlotterer C, Rassmann K et al. (1995) Amplification of hypervariable simple sequence repeats (microsatellites) from excremental DNA of wild living Bonobos (Pan paniscus). Mol. Ecol., 4, 515–518.

    Google Scholar 

  • Goldstein DB, Ruiz-Linares A, Feldman M, Cavalli-Sforza LL (1995) An evaluation of genetic distances for use with microsatellite loci. Genetics, 139, 463–471.

    Google Scholar 

  • Goodman SJ, Barton NH, Swanson G, Abernethy K, Pemberton JM (1999) Introgression through rare hybridization: A genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll, Scotland. Genetics, 152, 355–371.

    Google Scholar 

  • Gottelli D, Sillero-Zubiri C, Applebaum GD, Roy MS, Girman DJ, Garcia-Moreno J et al. (1994) Molecular genetics of the most endangered canid – the Ethiopian wolf Canis simensis. Mol. Ecol., 3, 301–312.

    Google Scholar 

  • Goudet J (1995) Fstat Version 1.2 A computer program to calculate F-statistics. J. Heredity, 86, 485–486.

    Google Scholar 

  • Guo S, Thompson E (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics, 48, 361–372.

    Google Scholar 

  • Hartl DL, Clark AG (1989) Principles of Population Genetics, Second Edition.

  • Sinauer, MA. Lariviere S, Crete M (1993) The size of eastern coyotes (Canis latrans): A comment. J. Mammal., 74, 1072–1074.

    Google Scholar 

  • Lehman N, Clarckson P, Mech LD, Meyer TJ and Wayne RK (1992). A study of the genetic relationships within and among wolf packs using DNA fingerprinting and mitochondrial DNA. Behav. Ecol. Sociobiol., 30, 83–94.

    Google Scholar 

  • Lehman N, Eisenhawer A, Hansen K, Mech LD, Peterson RO, Wayne RK (1991) Introgression of coyote mitochondrial DNA into sympatric North American gray wolf populations. Evolution, 45, 104–119.

    Google Scholar 

  • Longmire JL, Lewis AK, Brown NC et al. (1988) Isolation and molecular characterization of a highly polymorphic centromeric tandem repeat in the family Falconidae. Genomics, 2, 14–24.

    Google Scholar 

  • Maruyama T, Fuerst PA (1985) Population bottlenecks and non equilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics, 111, 675–689.

    Google Scholar 

  • Mendelssohn M (1982) Wolves in Israel. In: Wolves of the World: Perspectives of Behavior, Ecology and Conservation (eds. Harrington FH, Paquet PC), pp. 173–195. Noyes, Park Ridge, New Jork.

  • Mengel RM (1971) A study of dog-coyote hybrids and implications concerning hybridization in Canis. J. Mammal., 52, 316–336.

    Google Scholar 

  • Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference to microsatellite loci. Genetics, 142, 1061–1064.

    Google Scholar 

  • Miller SA, Dykes DD, Poleski HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. NAR, 16, 12–15.

    Google Scholar 

  • Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.

    Google Scholar 

  • Newton JM, Wilkie AL, He L, Jordan SA, Metallinos DL, Holmes NG, Jackson IJ, Barsh GS (2000) Melanocortin 1 receptor variation in the domestic dog. Mamm. Genome, 11, 24–30.

    Google Scholar 

  • Ohta T, Kimura K (1973) The model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a genetic population. Genet. Res., 22, 201–204.

    Google Scholar 

  • Okumura N, Ishiguro N, Nakano M, Matsui A, Sahara M (1996) Intra-and interbreed genetic variations of mitochondrial DNA major non-coding regions in Japanese native dog breeds (Canis familiaris). Anim. Genet., 27, 397–405.

    Google Scholar 

  • Ostrander EA, Galibert F and Patterson D (2000). Canine genetics comes of age. TIG, 16, 117–124.

    Google Scholar 

  • Ostrander EA, Sprague GF, Rine J (1993) Identification and characterization of dinucleotide repeat (CA)n markers for geneticmapping in dog. Genomics, 16, 207–213.

    Google Scholar 

  • Paetkau D, Calvert W, Stirling I and Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol. Ecol. 4, 347–354.

    Google Scholar 

  • Paetkau D, Shields GF, Strobeck C (1998) Gene flow between insular, coastal and interior populations of brown bears in Alaska. Mol. Ecol., 7, 1283–1292.

    Google Scholar 

  • Pemberton JM, Slate J, Bancroft DR, Barret JA (1995) Nonamplifying alleles at microsatellite loci: A caution for parentage and population studies. Mol. Ecol., 4, 249–252.

    Google Scholar 

  • Pritchard, JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

    Google Scholar 

  • Randi E, Francisci F, Lucchini V (1995) Mitochondrial DNA restriction-fragment-length monomorphism in the Italian wolf (Canis lupus) population. J. Zool. Syst. Evol. Res., 33, 97–100.

    Google Scholar 

  • Randi E, Lucchini V, Christensen MF, Mucci N, Funk SM, Dolf G, Loeschke V (2000) Mitochondrial DNA variability in Italian and east European wolves: Detecting the consequences of small population size and hybridization. Cons. Biol., 14, 464–473.

    Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc. Nat. Acad. Sci. U.S.A., 94, 9197–9201.

    Google Scholar 

  • Raymond M, Rousset F (1995) Genepop (version 1.2): Population genetics software for exact tests and ecumenicism. J. Heredity, 86, 248–249.

    Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu. Rev. Eco. Syst., 27, 83–109.

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution, 43, 223–225.

    Google Scholar 

  • 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, 553–570.

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol., 4, 406–425.

    Google Scholar 

  • She JX, Autem M, Kotulas G, Pasteur N, Bonhomme F (1987) Multivariate analysis of genetic exchanges between Solea aegyptiaca and Solea senegalensis (Teleosts, Soleidae). Biol. J. Linn. Soc., 32, 357–371.

    Google Scholar 

  • Shibuya H, Collins BK, Huang THM, Johnson GS (1994) A polymorphic (AGGAAT)n tandem repeat in an intron of the canine von Willebrand factor gene. Anim. Genet., 25, 122.

    Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139, 457–462.

    Google Scholar 

  • Smith D, Meier T, Geffen E, Mech LD, Burch JW, Adams LG, Wayne RK (1997) Is incest common in gray wolf packs? Behav. Ecol., 8, 384–391.

    Google Scholar 

  • Sneath PH, Sokal RR (1973) Numerical Taxonomy. WH Freeman and Co., San Francisco.

    Google Scholar 

  • Thurber JM, Peterson RO (1991) Changes in body size asociated with range expansion in the coyote (Canis latrans). J. Mamm., 72, 750–755.

    Google Scholar 

  • 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.

    Google Scholar 

  • Vilà C, Wayne RK (1999) Hybridization between wolves and dogs. Cons. Biol., 13, 195–198.

    Google Scholar 

  • Wayne RK, Geffen E, Girman DJ, Koepfli KP, Lau LM, Marshall CR (1997) Molecular systematics of the Canidae. Syst. Biol., 46, 622–653.

    Google Scholar 

  • Wayne RK, Lehman N, Fuller TK (1995) Conservation genetics of the Gray Wolf. In: Ecology and Conservation of Wolves in a Changing World (eds. Carbyn LN, Fritts SH, Seip DR), pp. 399–407. Canadian Circumpolar Institute, Occasional Pubblication No. 35. Edmonton, Alberta, Canada.

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.

    Google Scholar 

  • Zimen E, Boitani L (1975) Number and distribution of Wolves in Italy. Zeitsch. Säugetierk., 40, 102–112.

    Google Scholar 

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Randi, E., Lucchini, V. Detecting rare introgression of domestic dog genes into wild wolf (Canis lupus) populations by Bayesian admixture analyses of microsatellite variation. Conservation Genetics 3, 29–43 (2002). https://doi.org/10.1023/A:1014229610646

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