Abstract
We review the underlying principles and tools used in genomic studies of domestic dogs aimed at understanding the genetic changes that have occurred during domestication. We show that there are two principle modes of evolution within dogs. One primary mode that accounts for much of the remarkable diversity of dog breeds is the fixation of discrete mutations of large effect in individual lineages that are then crossed to various breed groupings. This transfer of mutations across the dog evolutionary tree leads to the appearance of high phenotypic diversity that in actuality reflects a small number of major genes. A second mechanism causing diversification involves the selective breeding of dogs within distinct phenotypic or functional groups, which enhances specific group attributes such as heading or tracking. Such progressive selection leads to a distinct genetic structure in evolutionary trees such that functional and phenotypic groups cluster genetically. We trace the origin of the nuclear genome in dogs based on haplotype-sharing analyses between dogs and gray wolves and show that contrary to previous mtDNA analyses, the nuclear genome of dogs derives primarily from Middle Eastern or European wolves, a result more consistent with the archeological record. Sequencing analysis of the IGF1 gene, which has been the target of size selection in small breeds, further supports this conclusion. Finally, we discuss how a black coat color mutation that evolved in dogs has transformed North American gray wolf populations, providing a first example of a mutation that appeared under domestication and selectively swept through a wild relative.
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(8):2175–2186
Akey JM, Ruhe AL, Akey DT et al (2010) Tracking footprints of artificial selection in the dog genome. Proc Natl Acad Sci USA 107(3):1160–1165
American Kennel Club (1992) The complete dog book, 18th edn. Macmillian, New York
Anderson T, vonHoldt BM, Candille SI et al (2009) Molecular and evolutionary history of melanism in North American gray wolves. Science 323(5919):1339–1343
Andersone Z, Lucchini V, Randi E et al (2002) Hybridisation between wolves and dogs in Latvia as documented using mitochondrial and microsatellite DNA markers. Mamm Biol 67:79–90
Ash EC (1927) Dogs: their history and development. Randall House, Santa Barbara
Bannasch D, Young A, Myers J et al (2010) Localization of canine brachycephaly using an across breed mapping approach. PLoS ONE 5(3):e9632
Bohling J, Waits LP (2011) Assessing the prevalence of hybridization between sympatric Canis species surrounding the red wolf (Canis rufus) recovery area in North Carolina. Mol Ecol 20(10):2142–2156
Boyko AR (2011) The domestic dog: man’s best friend in the genomic era. Genome Biol 12(2):216
Boyko AR, Quignon P, Lin L et al (2009) A simple genetic architecture underlies morphological variation in dogs. PLoS Biol 8(8):e1000451
Boyko AR, Quignon P, Li L et al (2010) A simple genetic architecture underlies morphological variation in dogs. PLoS Biol 8(8):e1000451
Bryc K, Velez C, Karafet T et al (2010a) Genome-wide patterns of population structure and admixture among Hispanic/Latino populations. Proc Natl Acad Sci USA 107(Suppl 2):8954–8961
Bryc K, Auton A, Nelson MR et al (2010b) Genome-wide patterns of population structure and admixture in West Africans and African Americans. Proc Natl Acad Sci USA 107(2):786–791
Buerkle CA, Lexer C (2008) Admixture as the basis for genetic mapping. Cell 23(12):686–694
Cadieu E, Neff M, Quignon P et al (2009) Coat variation in the domestic dog is governed by variants in three genes. Science 326(5949):150–153
Chase K, Carrier DR, Adler FR et al (2005) Interaction between the X chromosome and an autosome regulates size sexual dimorphism in Portuguese Water Dogs. Genome Res 15(12):1820–1824
Chase K, Jones P, Martin A et al (2009) Genetic mapping of fixed phenotypes: disease frequency as a breed characteristic. J Hered 100(Suppl 1):S37–S41
Cheng CY, Hao WH, Patterson N et al (2009) Admixture mapping of 15, 280 African Americans identifies obesity susceptibility loci on chromosomes 5 and X. PLoS Genet 5(5):e1000490
Cheng CY, Reich D, Coresh J et al (2010a) Admixture mapping of obesity-related traits in African Americans: the Atherosclerosis Risk in Communities (ARIC) study. Obesity 18:563–572
Cheng CY, Reich D, Wong TY et al (2010b) Admixture mapping scans identify a locus affecting retinal vascular caliber in hypertensive African Americans: the Atherosclerosis Risk in Communities (ARIC) study. PLoS Genet 6(4):e1000908
Clark LA, Wahl JM, Rees CA et al (2006) Retrotransposon insertion in SILV is responsible for merle patterning of the domestic dog. Proc Natl Acad Sci USA 103(5):1376–1381
Coulson T, MacNulty DR, Stahler DR et al (2011) Modeling effects of environmental change on wolf population dynamics, trait evolution, and life history. Science 334(6060):1275–1278
Darwin C (1859) The origin of species. Penguin Press, London
Davis SJ, Valla FR (1978) Evidence for domestication of the dog 12, 000 years ago in the Natufian of Israel. Nature 276:608–610
Dayan T (1994) Early domesticated dogs of the Near East. J Archaeol Sci 21:640–663
Dennis-Bryan K, Clutton-Brock J (1988) Dogs of the last hundred years at the British Museum (Natural History). British Museum (Natural History), London
Dodman NH, Karlsson EK, Moon-Fanelli A et al (2010) A canine chromosome 7 locus confers compulsive disorder susceptibility. Mol Psychiatr 15(1):8–10
Drake AG, Klingenberg CP (2010) Large-scale diversification of skull shape in domestic dogs: disparity and modularity. Am Nat 175(3):289–301
Epstein H (1971) The origins of the domestic animals of Africa, vol. 1. Africana Publishing, New York
Fain S, Straughan D, Taylor B (2010) Genetic outcomes of wolf recovery in the western Great Lakes states. Conserv Genet 11(5):1747–1765
Fredrickson R, Hedrick P (2006) Dynamics of hybridization and introgression in red wolves and coyotes. Conserv Biol 20(4):1272–1283
Galibert F, Quignon P, Hitte C et al (2011) Toward understanding dog evolutionary and domestication history. C R Biol 334(3):190–196
Genomes Project Consortium (2010) A map of human genome variation from population-scale sequencing. Nature 467:1061–1073
Germonpré M, Sablin M, Stevens R et al (2009) Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes. J Archaeol Sci 36:473–490
Gray MM, Granka JM, Bustamante CD et al (2009) Linkage disequilibrium and demographic history of wild and domestic canids. Genetics 181:1493–1505
Gray MM, Sutter NB, Ostrander EA et al (2010) The IGF1 small dog haplotype is derived from Middle Eastern grey wolves. BMC Biol 8:16
Housley DJ, Venta PJ (2006) The long and short of it: evidence that FGF5 is a major determinant of canine ‘hair’-itability. Anim Genet 37(4):309–315
Huson HJ, Parker HG, Runstadler J et al (2010) A genetic dissection of breed composition and performance enhancement in the Alaskan sled dog. BMC Genet 11:71
Hutt FB (1979) Genetics for dog breeders. WH Freeman, San Francisco
Jones P, Chase K, Martin A et al (2008) Single-nucleotide polymorphism-based association mapping of dog stereotypes. Genetics 179:1033–1044
Kaplan NL, Hudson RR, Langley CH (1989) The “hitchhiking effect” revisited. Genetics 123:887–899
Karlsson EK, Baranowska I, Wade CM et al (2007) Efficient mapping of Mendelian traits in dogs through genome-wide association. Nat Genet 39(11):1321–1328
Kays R, Curtis A, Kirchman JJ (2010) Rapid adaptive evolution of northeastern coyotes via hybridization with wolves. Biol Lett 6:89–93
Kirkness EF, Bafna V, Halpern AL et al (2003) The dog genome: survey sequencing and comparative analysis. Science 301(5641):1898–1903
Kukekova A, Trut LN, Chase K et al (2010) Mapping loci for fox domestication: deconstruction/reconstruction of a behavioral phenotype. Behav Genet 41(4):593–606
Lindblad-Toh K, Wade CM, Mikkelsen TS et al (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438(7069):803–819
Macdonald DW, Barrett P (1993) Mammals of Britain and Europe. Harper Collins, New York
McCarthy MI, Abecasis GR, Cardon LR et al (2008) Genome-wide association studies for complex traits: consensus, uncertainty and challenges. Nat Rev Genet 9(5):356–369
Morey D (1994) The early evolution of the domestic dog. Am Sci 82:336–347
Morey DF (2010) Dogs: domestication and the development of a social bond. Cambridge University Press, New York
Olsen SJ, Olsen JW (1977) The Chinese wolf ancestor of new World dogs. Science 197:533–535
Ostrander EA, Kruglyak L (2000) Unleashing the canine genome. Genome Res 10(9):1271–1274
Ostrander EA, Wayne RK (2005) The canine genome. Genome Res 15:1706–1716
Ovodov MD, Crockford SJ, Kuzmin YV et al (2011) A 33, 000-year-old incipient dog from the Altai Mountains of Siberia: Evidence of the earliest domestication disruption by the last glacial maximum. PLoS ONE 6(7):e22821
Pang JF, Kluetsch C, Zou XJ et al (2009) mtDNA data indicate a single origin for dogs south of the Yangtze River, less than 16, 300 years ago, from numerous wolves. Mol Biol Evol 26(12):2849–2864
Parker HG, Ostrander EA (2005) Canine genomics and genetics: running with the pack. PLoS Genet 1(5):507–513
Parker HG, Kim LV, Sutter NB et al (2004) Genetic structure of the purebred domestic dog. Science 304(5674):1160–1164
Parker HG, vonHoldt BM, Quignon P et al (2009) An expressed fgf4 retrogene is associated with breed-defining chondrodysplasia in domestic dogs. Science 325(5943):995–998
Patterson N, Hattangadi N, Lane B et al (2004) Methods for high-density admixture mapping of disease genes. Am J Hum Genet 74(5):979–1000
Pilgrim KL, Boyd DK, Forbes SH (1998) Testing for wolf-coyote hybridization in the Rocky Mountains using mitochondrial DNA. J Wildlife Manage 62(2):683–689
Pollinger JP, Bustamante CD, Fledel-Alon A et al (2005) Selective sweep mapping of genes with large phenotypic effects. Genome Res 15(12):1809–1819
Price AL, Patterson N, Yu F et al (2007) A genomewide admixture map for Latino populations. Am J Hum Genet 80(6):1024–1036
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
Reich DE, Cargill M, Bolk A et al (2001) Linkage disequilibrium in the human genome. Nature 411:199–204
Sablin MV, Khlopachev GA (2002) The earliest ice age dogs: evidence from Eliseevichi. Curr Anthropol 43:795–799
Salmon Hillbertz NH, Isaksson M, Karlsson EK et al (2007) Duplication of FGF3, FGF4, FGF19 and ORAOV1 causes hair ridge and predisposition to dermoid sinus in Ridgeback dogs. Nat Genet 39(11):1318–1320
Savolainen P, Zhang YP, Luo J et al (2002) Genetic evidence for an East Asian origin of domestic dogs. Science 298:1610–1613
Seldin MF, Posaniuc B, Price AL (2011) New approaches to disease mapping in admixed populations. Nat Rev Genet 12:523–528
Shearin AL, Ostrander EA (2010a) Canine morphology: hunting for genes and tracking mutations. PLoS Biol 8(3):e1000310
Shearin AL, Ostrander EA (2010b) Leading the way: canine models of genomics and disease. Dis Model Mech 3(1–2):24–34
Smith JM, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genet Res 23(1):23–35
Stephan W, Wiehe THE, Lenz MW (1992) The effect of strongly selected substitutions on neutral polymorphism: Analytical results based on diffusion theory. Theor Pop Biol 41:237–254
Stockard C (1941) Genetic and endocrinic basis for differences in form and behavior. Wistar Institute, Philadelphia
Sundqvist AK, Bjornerfeldt S, Leonard JA et al (2006) Unequal contribution of sexes in the origin of dog breeds. Genetics 172:1121–1128
Sutter NB, Ostrander EA (2004) Dog star rising: the canine genetic system. Nat Rev Genet 5(12):900–910
Sutter NB, Bustamante CD, Chase K et al (2007) A single IGF1 allele is a major determinant of small size in dogs. Science 316:112–115
Tang H, Coram M, Wang P et al (2006) Reconstructing genetic ancestry blocks in admixed individuals. Am J Hum Genet 79(1):1–12
Vilà C, Wayne RK (1999) Hybridization between wolves and dogs. Conserv Biol 13(1):195–198
Vilà C, Savolainen P, Maldonado JE et al (1997) Multiple and ancient origins of the domestic dog. Science 276:1687–1689
Vilà C, Walker C, Sundqvist A et al (2003) Combined use of maternal, paternal and bi-parental genetic markers for the identification of wolf-dog hybrids. Heredity 90(1):17–24
Vilà C, Seddon J, Ellegren H (2005) Genes of domestic mammals augmented by backcrossing with wild ancestors. Trends Genet 21(4):214–218
vonHoldt BM, Stahler DR, Smith DW et al (2008) The genealogy and genetic viability of reintroduced yellowstone gray wolves. Mol Ecol 17(1):252–274
vonHoldt BM, Pollinger JP, Lohmueller KE et al (2010) Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464:898–903
vonHoldt BM, Pollinger JP, Earl DA et al (2011) A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids. Genome Res 21(8):1294–1305
Wayne RK (1986a) Cranial morphology of domestic and wild canids: the influence of development on morphological change. Evolution 4:243–261
Wayne RK (1986b) Limb morphology of domestic and wild canids: the influence of development on morphologic change. J Morphol 187:301–319
Wayne RK, Ostrander EA (2007) Lessons learned from the dog genome. Trends Genet 23(11):557–567
Wilcox B, Walkowicz C (1995) The atlas of dog breeds of the World, 5th edn. TFH Publications, Neptune
Winkler CA, Nelson GW, Smith MW (2010) Admixture mapping comes of age. Annu Rev Genome Human Genet 11:65–89
Yang J, Benyamin B, McEvoy BP et al (2010) Common SNPs explain a large proportion of the heritability for human height. Nat Genet 42(7):565–569
Zeder MA, Emshwiller E, Smith BD et al (2006) Documenting domestication: the intersection of genetics and archaeology. Trends Genet 223:139–155
Zeuner FE (1963) A history of domesticated animals. Hutchinson of London, London
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wayne, R.K., vonHoldt, B.M. Evolutionary genomics of dog domestication. Mamm Genome 23, 3–18 (2012). https://doi.org/10.1007/s00335-011-9386-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00335-011-9386-7