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Conservation Genetics

, Volume 3, Issue 1, pp 29–43 | Cite as

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

  • Ettore Randi
  • Vittorio Lucchini
Article

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.

admixture analysis assignment test Bayesian clustering Canis lupus dog wolf 

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References

  1. Andersone Z, Lucchini V, Randi E, Ozolins J (submitted) Relationships between wolves and free-ranging dogs in Latvia.Google Scholar
  2. 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
  3. 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.Google Scholar
  4. Boitani L (1983) Wolf and dog competition in Italy. Acta Zool. Fennica, 174, 259–264.Google Scholar
  5. Boitani L (1984) Genetic considerations on wolf conservation in Italy. Boll. Zool., 51, 367–373.Google Scholar
  6. Boitani L (1986) Dalla parte del lupo. Mondadori, Milano, Italy.Google Scholar
  7. 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.Google Scholar
  8. Boitani L (1999) Final Draft Action Plan for the Conservation of Wolves (Canis lupus) in Europe. Council of Europe, Strasbourg.Google Scholar
  9. Boitani L, Fabbri L (1983) Strategia nazionale di conservazione per il lupo (Canis lupus). Ric. Biol. Selv., 72, 1–31.Google Scholar
  10. 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
  11. 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
  12. Breitenmoser U (1998) Large predators in the Alps: The fall and rise of man's competitors. Biol. Conser., 83, 279–289.Google Scholar
  13. 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.Google Scholar
  14. Butler D (1994) Bid to protect wolves from genetic pollution. Nature, 370, 497.Google Scholar
  15. Colson I, Goldstein DB (1999) Evidence for complex mutations at microsatellite loci in Drosophila. Genetics, 152, 617–627.Google Scholar
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. DogMap Consortium (1999) DogMap: An international collaboration toward a low-resolution canine genetic marker map. J. Heredity, 90, 3–6.Google Scholar
  22. 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
  23. 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
  24. 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
  25. Forbes SH, Boyd DK (1997) Genetic structure and migration in native and reintroduced Rocky Mountain wolf populations. Cons. Biol., 11, 1226–1234.Google Scholar
  26. 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
  27. 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
  28. 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.Google Scholar
  29. 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
  30. 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
  31. 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
  32. 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
  33. 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
  34. Goudet J (1995) Fstat Version 1.2 A computer program to calculate F-statistics. J. Heredity, 86, 485–486.Google Scholar
  35. Guo S, Thompson E (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics, 48, 361–372.Google Scholar
  36. Hartl DL, Clark AG (1989) Principles of Population Genetics, Second Edition.Google Scholar
  37. Sinauer, MA. Lariviere S, Crete M (1993) The size of eastern coyotes (Canis latrans): A comment. J. Mammal., 74, 1072–1074.Google Scholar
  38. 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
  39. 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
  40. 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
  41. 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
  42. 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.Google Scholar
  43. Mengel RM (1971) A study of dog-coyote hybrids and implications concerning hybridization in Canis. J. Mammal., 52, 316–336.Google Scholar
  44. 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
  45. 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
  46. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.Google Scholar
  47. 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
  48. 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
  49. 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
  50. Ostrander EA, Galibert F and Patterson D (2000). Canine genetics comes of age. TIG, 16, 117–124.Google Scholar
  51. 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
  52. 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
  53. 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
  54. 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
  55. Pritchard, JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.Google Scholar
  56. 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
  57. 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
  58. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc. Nat. Acad. Sci. U.S.A., 94, 9197–9201.Google Scholar
  59. Raymond M, Rousset F (1995) Genepop (version 1.2): Population genetics software for exact tests and ecumenicism. J. Heredity, 86, 248–249.Google Scholar
  60. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu. Rev. Eco. Syst., 27, 83–109.Google Scholar
  61. Rice WR (1989) Analyzing tables of statistical tests. Evolution, 43, 223–225.Google Scholar
  62. 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
  63. Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol., 4, 406–425.Google Scholar
  64. 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
  65. 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
  66. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139, 457–462.Google Scholar
  67. 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
  68. Sneath PH, Sokal RR (1973) Numerical Taxonomy. WH Freeman and Co., San Francisco.Google Scholar
  69. 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
  70. 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
  71. Vilà C, Wayne RK (1999) Hybridization between wolves and dogs. Cons. Biol., 13, 195–198.Google Scholar
  72. 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
  73. 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.Google Scholar
  74. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.Google Scholar
  75. Zimen E, Boitani L (1975) Number and distribution of Wolves in Italy. Zeitsch. Säugetierk., 40, 102–112.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  1. 1.Istituto Nazionale per la Fauna SelvaticaOzzano dell'Emilia (BO)Italy

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