Multiple and ancient origins of the domestic dog

Science

Volumn 276, Issue 5319, 1997, Pages 1687-1689

  Vilà, Carles ^a   Savolainen, Peter ^b   Maldonado, Jesús E ^a   Amorim, Isabel R ^a   Rice, John E ^c   Honeycutt, Rodney L ^c   Crandall, Keith A ^d   Lundeberg, Joakim ^b   Wayne, Robert K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^c TEXAS A AND M UNIVERSITY   (United States)

^d BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; BREEDING; DOG; EVOLUTION; EXTRACHROMOSOMAL INHERITANCE; GENE TRANSFER; HAPLOTYPE; INHERITANCE; NONHUMAN; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; SEQUENCE ANALYSIS; WOLF;

ANIMALS; BASE SEQUENCE; BREEDING; CARNIVORA; CROSSES, GENETIC; DNA, MITOCHONDRIAL; DOGS; EVOLUTION; FEMALE; HAPLOTYPES; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE HOMOLOGY, NUCLEIC ACID;

DOMESTIC DOG; EVOLUTION; WOLF;

CANIS FAMILIARIS; CANIS LUPUS;

EID: 0030616576     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.276.5319.1687     Document Type: Article

References (34)

1. J. Clutton-Brock, in The Domestic Dog, Its Evolution, Behaviour and Interactions with People, J. Serpell, Ed. (Cambridge Univ. Press, Cambridge, 1995), pp. 7-20.
2. S. J. Olsen and J. W. Olsen, Science 197, 533 (1977).
3. J. Clutton-Brock, A Natural History of Domesticated Mammals (Cambridge Univ. Press, British Museum of Natural History, Cambridge, 1987).
4. F. E. Zeuner, A History of Domesticated Animals (Harper & Row, New York, 1963); H. Epstein, The Origin of the Domestic Animals of Africa (Africana Publishing, New York, 1971); I. L. Brisbin Jr., Am. Kennel Gaz. January 1976, p. 23.
5. F. E. Zeuner, A History of Domesticated Animals (Harper & Row, New York, 1963); H. Epstein, The Origin of the Domestic Animals of Africa (Africana Publishing, New York, 1971); I. L. Brisbin Jr., Am. Kennel Gaz. January 1976, p. 23.
6. F. E. Zeuner, A History of Domesticated Animals (Harper & Row, New York, 1963); H. Epstein, The Origin of the Domestic Animals of Africa (Africana Publishing, New York, 1971); I. L. Brisbin Jr., Am. Kennel Gaz. January 1976, p. 23.
7. C. Saccone, M. Attimonelli, E. Sbisà, J. Mol. Evol. 26, 205 (1987).
8. DNA from blood, tissue, or hair was isolated by cell lysis followed by organic solvent purification. A 261-bp control region fragment was sequenced from a slightly larger (394 bp) fragment amplified with primers L15910 and H16498 [R. DeSalle, A. K. Williams, M. George, Methods Enzymol. 224, 176 (1993)]. See polymerase chain reaction and sequencing conditions and protocols in J. E. Maldonado, F. O. Davila, B. S. Stewart, E. Geffen, R. K. Wayne, Mar. Mamm. Sci. 11, 46 (1995).
9. DNA from blood, tissue, or hair was isolated by cell lysis followed by organic solvent purification. A 261-bp control region fragment was sequenced from a slightly larger (394 bp) fragment amplified with primers L15910 and H16498 [R. DeSalle, A. K. Williams, M. George, Methods Enzymol. 224, 176 (1993)]. See polymerase chain reaction and sequencing conditions and protocols in J. E. Maldonado, F. O. Davila, B. S. Stewart, E. Geffen, R. K. Wayne, Mar. Mamm. Sci. 11, 46 (1995).
10. A. P. Gray, Mammalian Hybrids, a Check-list with Bibliography (Farnham Royal, Bucks, Commonwealth Agricultural Bureaux, UK, 1954).
11. D. Gottelli et al., Mol. Ecol. 3, 301 (1994); J. García-Moreno, M. D. Matocq, M. S. Roy, E. Geffen, R. K. Wayne, Conserv. Biol. 10, 376 (1996); P.W. Hedrick, P. S. Miller, E. Geffen, R. K. Wayne, Zoo Biol. 16, 47 (1997).
12. D. Gottelli et al., Mol. Ecol. 3, 301 (1994); J. García-Moreno, M. D. Matocq, M. S. Roy, E. Geffen, R. K. Wayne, Conserv. Biol. 10, 376 (1996); P.W. Hedrick, P. S. Miller, E. Geffen, R. K. Wayne, Zoo Biol. 16, 47 (1997).
13. D. Gottelli et al., Mol. Ecol. 3, 301 (1994); J. García-Moreno, M. D. Matocq, M. S. Roy, E. Geffen, R. K. Wayne, Conserv. Biol. 10, 376 (1996); P.W. Hedrick, P. S. Miller, E. Geffen, R. K. Wayne, Zoo Biol. 16, 47 (1997).
14. K. Strimmer and A. von Haessler, Mol. Biol. Evol. 13, 964 (1996).
15. D. L. Swofford, PAUP: Phylogenetic Analysis Using Parsimony, Version 3.0 (Illinois Natural History Survey, Champaign, IL, 1990).
16. L. Excoffier, P. E. Smouse, J. M. Quattro, Genetics 131, 479 (1992).
17. A. R. Templeton, K. A. Crandall, C. F. Sing, ibid. 132, 619 (1992).
18. The coyote was used as an outgroup on the basis of morphologic and mitochondrial DNA sequence analyses [R. M. Nowak, North American Quaternary Canis (Monograph of the Museum of Natural History, University of Kansas, N 6, Lawrence, KS, 1979); R. K. Wayne, Trends Genet. 6, 218 (1993); C. Vilà et al., unpublished data]. Trees retaining the four indicated clades resulted from neighbor-joining searches with Tamura-Nei, Kimura 2-parameter, Kimura 3-parameter, and HKY85 models of evolution; parsimony searches with equal, 2:1, and 10:1 weights of transversions to transitions; and maximum likelihood analyses with the HKY85 model of evolution, taking into account differences in nucleotide frequencies and transition and transversion biases.
19. The coyote was used as an outgroup on the basis of morphologic and mitochondrial DNA sequence analyses [R. M. Nowak, North American Quaternary Canis (Monograph of the Museum of Natural History, University of Kansas, N 6, Lawrence, KS, 1979); R. K. Wayne, Trends Genet. 6, 218 (1993); C. Vilà et al., unpublished data]. Trees retaining the four indicated clades resulted from neighbor-joining searches with Tamura-Nei, Kimura 2-parameter, Kimura 3-parameter, and HKY85 models of evolution; parsimony searches with equal, 2:1, and 10:1 weights of transversions to transitions; and maximum likelihood analyses with the HKY85 model of evolution, taking into account differences in nucleotide frequencies and transition and transversion biases.
20. The coyote was used as an outgroup on the basis of morphologic and mitochondrial DNA sequence analyses [R. M. Nowak, North American Quaternary Canis (Monograph of the Museum of Natural History, University of Kansas, N 6, Lawrence, KS, 1979); R. K. Wayne, Trends Genet. 6, 218 (1993); C. Vilà et al., unpublished data]. Trees retaining the four indicated clades resulted from neighbor-joining searches with Tamura-Nei, Kimura 2-parameter, Kimura 3-parameter, and HKY85 models of evolution; parsimony searches with equal, 2:1, and 10:1 weights of transversions to transitions; and maximum likelihood analyses with the HKY85 model of evolution, taking into account differences in nucleotide frequencies and transition and transversion biases.
21. R. Coppinger and R. Schneider, in The Domestic Dog, Its Evolution, Behaviour and Interactions with People, J. Serpell, Ed. (Cambridge Univ. Press, Cambridge, 1995), pp. 21-47.
22. We amplified the entire canid control region with primers in (6) and the following primers: L16462 (5′-CATACTAACGTGGGGGTTAC-3′), H222 (5′-AAACTATATGTCCTGAAACC-3′), L296 (5′-ATACAAACCCCCCTTACC-3′), and H652 (5′-AAGGCTAGGACCAAACCT-3′). The primer numbering refers to their approximate location in the human mitochondrial genome [S. Anderson et al., Nature 290, 457 (1981)]. The 1030-bp sequence that we report includes the entire control region except for a hypervariable region close to the 3′ end that encompasses an imperfect 20-bp repeat having a variable number of units [A. R. Hoelzel, J. V. Lopez, G. A. Dover, S. J. O'Brien, J. Mol. Evol. 39, 191 (1994)].
23. We amplified the entire canid control region with primers in (6) and the following primers: L16462 (5′-CATACTAACGTGGGGGTTAC-3′), H222 (5′-AAACTATATGTCCTGAAACC-3′), L296 (5′-ATACAAACCCCCCTTACC-3′), and H652 (5′-AAGGCTAGGACCAAACCT-3′). The primer numbering refers to their approximate location in the human mitochondrial genome [S. Anderson et al., Nature 290, 457 (1981)]. The 1030-bp sequence that we report includes the entire control region except for a hypervariable region close to the 3′ end that encompasses an imperfect 20-bp repeat having a variable number of units [A. R. Hoelzel, J. V. Lopez, G. A. Dover, S. J. O'Brien, J. Mol. Evol. 39, 191 (1994)].
24. A. R. Templeton, Evolution 37, 221 (1983).
25. Sequence divergence values and trees were based on a gamma correction [K. Tamura and M. Nei, Mol. Biol. Evol. 10, 513 (1993)] with the empirically determined parameter a = 0.18 for the 261-bp sequences and a = 0.22 for the 1030-bp sequences [S. Kumar, K. Tamura, M. Nei, MEGA: Molecular Evolutionary Genetic Analysis, Version 1.01 (Pennsylvania State University, University Park, PA, 1993)].
26. Sequence divergence values and trees were based on a gamma correction [K. Tamura and M. Nei, Mol. Biol. Evol. 10, 513 (1993)] with the empirically determined parameter a = 0.18 for the 261-bp sequences and a = 0.22 for the 1030-bp sequences [S. Kumar, K. Tamura, M. Nei, MEGA: Molecular Evolutionary Genetic Analysis, Version 1.01 (Pennsylvania State University, University Park, PA, 1993)].
27. R. K. Wayne, B. Van Valkenburgh, S. J. O'Brien, Mol. Biol. Evol. 8, 297 (1991).
28. A relative rate test indicated that substitution rates were similar for all wolf and dog sequences [F. Tajima, Genetics 135, 599 (1993)].
29. T. J. Parsons et al., Nature Genet. 15, 363 (1997).
30. G. Nobis, Umshau 19, 610 (1979); S. J. Olsen, Origins of the Domestic Dog (University of Arizona Press, Tucson, AZ, 1985).
31. G. Nobis, Umshau 19, 610 (1979); S. J. Olsen, Origins of the Domestic Dog (University of Arizona Press, Tucson, AZ, 1985).
32. M. E. Thurston, The Lost History of the Canine Race. Our 15,000-Year Love Affair with Dogs (Andrews & McMeel, Kansas City, KS, 1996).
33. D. F. Morey, Am. Sci. 82, 336 (1994).
34. We thank P. Taberlet for providing wolf sequences from France and Poland and J. Castroviejo, Grupo Lobo-Portugal, E. Geffen, and many others for their help in obtaining samples. C.V. was supported by a postdoctoral fellowship from the Spanish Ministerio de Educación y Ciencia, and I.R.A. was supported by a fellowship from Junta Nacional de Investigasão Científica e Tecnológica, Portugal. This research was supported in part by NSF grants to R.L.H. (DEB-9208022) and R.K.W. (BSR-9020282) and by a Sloan Young Investigator Award to K.A.C.