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3 - Origins of the dog: Genetic insights into dog domestication

from PART I - ORIGINS AND EVOLUTION

Published online by Cambridge University Press:  30 December 2016

Bridgett M. Vonholdt
Affiliation:
Department of Ecology and Evolutionary Biology, Princeton University, NJ, USA
Carlos A. Driscoll
Affiliation:
National Institute on Alcohol Abuse and Alcoholism; National Institutes of Health, MD, USA
James Serpell
Affiliation:
University of Pennsylvania
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Summary

Introduction

Dogs are the oldest domesticated animal and today are second only to cats as the most popular pet in western societies (Boyko, 2011; Leonard et al., 2006; Wayne and vonHoldt, 2012). The dog has taken on many significant roles in human society, ranging from companion, sentry, and hunting partner to its more recent function as a model for understanding human disease. By exploring the genetic and evolutionary history of our canine companions, we can better understand not only the natural history of dogs but also our own evolutionary history.

Inquiries into the dog's natural history are now enlightened by molecular and genetic data to an overwhelmingly greater degree then they were 20 years ago when the first edition of this book was published. This trend towards increasing molecular inference will certainly continue, though morphology and archaeology will remain vitally important in completing our understanding of the cultural context of the changes wrought by domestication.

The wolf, ancestor of the dog

The dog and its ancestor, the wolf (Canis lupus), belong to the family Canidae. The 34 living species of canids are grouped into four clades: a red fox-like clade, a South American clade, a wolf-like clade, and a clade comprising only the gray and island fox (Urocyon cinereoargenteus and U. littoralis, respectively) (Lindblad-Toh et al., 2005; Perini et al., 2009) (Figure 3.1). Canids are found in all terrestrial habitats and, with the human-assisted introduction of dogs and foxes to Australia and New Zealand, Antarctica is now the only continent without a resident population. Currently, seven species belong to the dog-like genus Canis (Figure 3.2), which arose nearly six million years ago (mya) in North America and, along with a number of other carnivore species, expanded into Eurasia (4 mya) via the Beringian land bridge, and subsequently into Africa (3 mya) (Wang & Tedford, 2008). The archaeological record indicates that the modern-day gray wolf (Canis lupus lupus) evolved in Eurasia around 3–4 mya, re-invading North America about 500 000 years ago (Wang & Tedford, 2008). Supremely adaptable, the wolf inhabits nearly every habitat and environmental condition (Mech & Boitani, 2003). Wolves vary greatly in size depending on their environmental distribution, from the gracile 13 kg wolves of the Middle Eastern deserts to the large robust individuals (over 78 kg) of the Arctic tundra.

Type
Chapter
Information
The Domestic Dog
Its Evolution, Behavior and Interactions with People
, pp. 22 - 41
Publisher: Cambridge University Press
Print publication year: 2016

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References

AKC (American Kennel Club) (2006). The Complete Dog Book, edition. New York, NY: Ballantine Books.
Anderson, T. M., vonHoldt, B. M., Candille, S. I. et al. (2009). Molecular and evolutionary history of melanism in North American gray wolves. Science, 323: 1339–43.CrossRefGoogle ScholarPubMed
Akey, J. M., Ruhe, A. L., Akey, D. T. et al. (2010). Tracking footprints of artificial selection in the dog genome. Proceedings of the National Academy of Sciences USA, 107: 1160–5.CrossRefGoogle ScholarPubMed
Baker, J., Liu, J. P., Robertson, E. J. & Efstratiadis, A. (1993). Role of insulin-like growth factors in embryonic and postnatal growth. Cell, 75: 73–82.CrossRefGoogle ScholarPubMed
Barrett, R. D. H. & Schluter, D. (2008). Adaptation from standing genetic variation. Trends in Ecology & Evolution, 23: 38–44.CrossRefGoogle ScholarPubMed
Barsh, G. S. (2007). How the dog got its spots. Nature Genetics, 39: 1304–6.CrossRefGoogle ScholarPubMed
Belyaev, D. K. (1969). Domestication of animals. Science, 5: 47–52.Google Scholar
Biswas, S. & Akey, J. M. (2006). Genomic insights into positive selection. Trends in Genetics, 22: 437–46.CrossRefGoogle ScholarPubMed
Boyko, A. R. (2011). The domestic dog: man's best friend in the genomic era. Genome Biology, 12: 216.CrossRefGoogle ScholarPubMed
Boyko, A. R., Boyko, R. H., Boyko, C. M. et al. (2009). Complex population structure in African village dogs and its implications for inferring dog domestication history. Proceedings of the National Academy of Sciences USA, 106: 13903–8.CrossRefGoogle ScholarPubMed
Boyko, A. R., Quignon, P., Li, L. et al. (2010). A simple genetic architecture underlies morphological variation in dogs. PLoS Biology, 8: e1000451.CrossRefGoogle ScholarPubMed
Cadieu, E., Neff, M., Quignon, P. et al. (2009). Coat variation in the domestic dog is governed by variants in three genes. Science, 326: 150–3.CrossRefGoogle ScholarPubMed
Chase, K., Carrier, D. R., Adler, F. R. et al. (2002). Genetic basis for systems of skeletal quantitative traits: principal component analysis of the canid skeleton. Proceedings of the National Academy of Sciences USA, 99: 9930–5.CrossRefGoogle ScholarPubMed
Chase, K., Carrier, D. R., Adler, F. R., Ostrander, E. A. & Lark, K. G. (2005). Interaction between the X chromosome and an autosome regulates size sexual dimorphism in Portuguese Water Dogs. Genome Research, 15: 1820–4.CrossRefGoogle ScholarPubMed
Chase, K., Jones, P., Martin, A., Ostrander, E. A. & Lark, K. G. (2009). Genetic mapping of fixed phenotypes: disease frequency as a breed characteristic. Journal of Heredity, 100: S37–41.CrossRefGoogle ScholarPubMed
Clutton-Brock, J. (1981). Domesticated Animals from Early Times. Cambridge: Cambridge University Press.Google Scholar
Coppinger, R., Spector, L. & Miller, L. (2009). What, if anything, is a wolf? In The World of Wolves: New Perspectives on Ecology, Behaviour and Management, eds. Musiani, M., Boitani, L. and Paquet, P.. Calgary, Alberta: The University of Calgary Press, pp. 51–65.Google Scholar
Cordaux, R. & Batzer, M. A. (2009). The impact of retrotransposons on human genome evolution. Nature Reviews Genetics, 10: 691–703.CrossRefGoogle ScholarPubMed
Crockford, S. J. & Kuzmin, Y. V. (2012) Comments on Germonpré, et al., Journal of Archaeological Science 26,
2009Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes”, and Germonpré, , Lázkicková-Galetová, , and Sablin, , Journal of Archaeological Science 26,Google Scholar
2012Paleolithic dog skulls at the Gravettian Predmostí site, the Czech Republic”. Journal of Archaeological Science, 39: 2797–801.
Darwin, C. (1868). The Variation of Animals and Plants under Domestication. London: John Murray.Google Scholar
Dayan, T. (1999). Early domesticated dogs of the Near East. Journal of Archaeological Science, 21: 633–40.Google Scholar
Diamond, J. (2005). Guns, Germs, and Steel. New York: Norton and Company, Inc. Google Scholar
Ding, Z., Oskarsson, M., Ardalan, A. et al. (2012). Origins of domestic dog in Southern East Asia is supported by analysis of Y-chromosome DNA. Heredity, 108: 507–14.CrossRefGoogle ScholarPubMed
Dobney, K. & Larson, G. (2006). Genetics and animal domestication: new windows on an elusive process. Journal of Zoology, 269: 261–71.Google Scholar
Driscoll, C. A., Macdonald, D. W. & O'Brien, S. J. (2009). From wild animals to domestic pets, an evolutionary view of domestication. Proceedings of the National Academy of Sciences, 106: S9971–8.CrossRefGoogle ScholarPubMed
Driscoll, C. A., Menotti-Reymond, M., Roca, A. L. et al. (2007). The Near Eastern origin of cat domestication. Science, 317: 519–23.CrossRefGoogle ScholarPubMed
Druzhkova, A. S., Thalmann, O., Trifonov, V. A., Leonard, J. A., Vorobieva, N.V., Ovodov, N. D., Graphodatsky, A. S. & Wayne, R. K. (2013). Ancient DNA analysis affirms the canid from Altai as a primitive dog. PLoS One, 8: e57754.CrossRefGoogle ScholarPubMed
Fan, Z., Silva, P., Gronau, I., Wang, S., Serres Armero, A., Schweizer, R. M., Ramirez, O. et al. (2016). Worldwide patterns of genomic variation and admixture in gray wolves. Genome Research, 26: 163–73.CrossRefGoogle ScholarPubMed
Flint, J. & Mackay, T. F. C. (2009). Genetic architecture of quantitative traits in mice, flies and humans. Genome Research, 19: 723–33.CrossRefGoogle ScholarPubMed
Frantz, L. A., Mullin, V. E., Pionnier-Capitan, M., Lebrasseur, O., Olliver, M., Perri, A. et al. (2016). Genomic and archaeological evidence suggest a dual origin of domestic dogs. Science, 352: 1228–31.CrossRefGoogle ScholarPubMed
Freedman, A. H., Gronau, I, Schweizer, R. M. et al. (2014). Genome sequencing highlights the dynamic early history of dogs. PLoS Genetics, 10: e1004016 CrossRefGoogle ScholarPubMed
Freedman, A. H., Schweizer, R. M., Ortega-Del Vecchyo, D., Han, E., Davis, B. W., Gronau, I. et al. (2016). Demographically-based evaluation of genomic regions under selection in domestic dogs. PLoS Genetics, 12: e1005851 CrossRefGoogle ScholarPubMed
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. Journal of Archaeological Science, 36: 473–60.CrossRefGoogle Scholar
Giustina, A., Mazziotti, G. & Canalis, E. (2008). Growth hormone, insulin-like growth factors, and the skeleton. Endocrine Reviews, 29: 535–59.CrossRefGoogle ScholarPubMed
Goebel, T., Waters, M. R. & O'Rourke, D. H. (2008). The late Pleistocene dispersal of modern humans in the Americas. Science, 319: 1497–502.CrossRefGoogle ScholarPubMed
Gray, M. M., Sutter, N. B., Ostrander, E. A. & Wayne, R. K. (2010). The IGF1 small dog haplotype is derived from Middle Eastern gray wolves. BMC Biology, 8: 16.CrossRefGoogle Scholar
Hare, B., Plyusnina, I., Ignacio, N. et al. (2005). Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication. Current Biology, 15: 226–30.CrossRefGoogle ScholarPubMed
Innan, H. & Kim, Y. (2004). Pattern of polymorphism after strong artificial selection in a domestication event. Proceedings of the National Academy of Sciences USA, 101: 10667–72.CrossRefGoogle Scholar
IUCN (2012). The IUCN Red List of threatened species. Version 2012.1 [Online]. Available: www.iucnredlist.org
Jones, P., Chase, K., Martin, A., Ostrander, E. A. & Lark, K. G. (2008). Single-nucleotide polymorphism-based association mapping of dog stereotypes. Genetics, 179: 1033–44.CrossRefGoogle ScholarPubMed
Kazazian, H. (2004). Mobile elements: drivers of genome evolution. Science, 303: 1626–32.CrossRefGoogle ScholarPubMed
Kirkness, E. F., Bafna, V., Halpern, A. L. et al. (2003). The dog genome: survey sequencing and comparative analysis. Science, 301: 1898–903.CrossRefGoogle ScholarPubMed
Kukekova, A. V., Trut, L. N., Chase, K. et al. (2010). Mapping loci for fox domestication: Deconstruction/reconstruction of a behavioral phenotype. Behavorial Genetics, 41: 593–606.Google ScholarPubMed
Laron, Z. (2001). Insulin-like growth factor 1 (IGF-1): a growth hormone. Molecular Pathology, 54: 311–16.CrossRefGoogle ScholarPubMed
Larson, G., Karlsson, E. K., Perri, A. et al. (2012). Rethinking dog domestication by integrating genetics, archeology, and biogeography. Proceedings of the National Academy of Sciences USA, 109: 8878–83.CrossRefGoogle ScholarPubMed
Lefebvre, V. & Bhattaram, P. (2010). Vertebrate skeletogenesis. Current Topics in Developmental Biology, 90: 291–317.Google ScholarPubMed
Leonard, J. A., Vilà, C. & Wayne, R. K. (2006). From wild wolf to domestic dog. In The Dog and Its Genome, eds. Ostrander, E. A., Giger, U. & Lindblad-Toh, K.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 95–118.Google Scholar
Leonard, J. A., Wayne, R. K., Wheeler, J. et al. (2002). Ancient DNA evidence for Old World origin of New World dogs. Science, 298: 1613–16.CrossRefGoogle ScholarPubMed
Lindblad-Toh, K., Wade, C. M., Mikkelsen, T. S. et al. (2005). Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature, 438: 803–19.CrossRefGoogle ScholarPubMed
Mech, L. D. & Boitani, L. (2003). Wolf social ecology. In Wolves: Behavior, Ecology, and Conservation, eds. Mech, L. D. & Boitani, L.. Chicago, IL: The University of Chicago Press, pp. 1–34.CrossRefGoogle Scholar
McClintock, B. (1956). Controlling element and the gene. Cold Spring Harbor Symposia on Quantitative Biology, 31: 197–216.Google Scholar
Morey, D. F. (1994). The early evolution of the domestic dog. American Scientist, 82: 336–47.Google Scholar
Ovodov, M. D., Crockford, S. J., Kuzmin, Y. V. 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: e22821.CrossRefGoogle Scholar
Packard, J. M. (2003). Wolf behavior: Reproductive, social, and intelligent. In Wolves: Behavior, Ecology, and Conservation, eds. Mech, L. D. & Boitani, L.. Chicago, IL: The University of Chicago Press, pp. 35–65.Google Scholar
Pang, J. F., Kluetsch, C., Zou, X. J. et al. (2009). MtDNA data indicate a single origin for dogs south of Yangtze River, less than 16,300 years ago, from numerous wolves. Molecular Biology & Evolution, 26: 2849–64.CrossRefGoogle ScholarPubMed
Parker, H. G. (2012). Genomic analyses of modern dog breeds. Mammalian Genome, 23: 19–27.CrossRefGoogle ScholarPubMed
Parker, H. G., Kim, L. V., Sutter, N. B. et al. (2004). Genetic structure of the purebred domestic dog. Science, 304: 1160–4.CrossRefGoogle ScholarPubMed
Parker, H. G. & Ostrander, E. A. (2005). Canine genomics and genetics: running with the pack. PLoS Genetics, 1: e58.CrossRefGoogle ScholarPubMed
Parker, H. G., vonHoldt, B. M., Quignon, P. et al. (2009). An expressed fgf4 retrogene is associated with breed-defining chondrodysplasia in domestic dogs. Science, 325: 995–8.CrossRefGoogle ScholarPubMed
Parker, H. P., Shearin, A. L. & Ostrander, E. A. (2010). Man's best friend becomes biology's best in show: genome analyses in the domestic dog. Annual Review of Genetics, 44: 309–36.CrossRefGoogle ScholarPubMed
Perini, F. A., Russo, C. A. & Schrago, C. G. (2009). The evolution of South American endemic canids: a history of rapid diversification and morphological parallelism. Journal of Evolutionary Biology, 23: 311–22.Google ScholarPubMed
Randi, E. (2008). Detecting hybridization between wild species and their domesticated relatives. Molecular Ecology, 17: 285–93.CrossRefGoogle ScholarPubMed
Ritvo, H. (1989). The Animal Estate: The English and Other Creatures in the Victorian Age. Cambridge, MA: Harvard University Press.Google Scholar
Sablin, M. & Khlopachev, G. (2002). The earliest Ice Age dogs: evidence from Eliseevichi I. Current Anthropology, 45: 795–819.Google Scholar
Savolainen, P., Zhang, Y. P., Luo, J., Lundeberg, J. & Leitner, T. (2002). Genetic evidence for an East Asian origin of domestic dogs. Science, 298: 1610–13.CrossRefGoogle ScholarPubMed
Savolainen, P., Leitner, T., Wilton, A. N., Matisoo-Smith, E. & Lundeberg, J. (2004). A detailed picture of the origin of the Australian dingo, obtained from the study of mitochondrial DNA. Proceedings of the National Academy of Sciences USA, 101: 12387–90.CrossRefGoogle Scholar
Shannon, L. M., Boyko, R. H., Castelhano, M., Corey, E., Hayward, J. J., McLean, C. et al. (2015). Genetic structure in village dogs reveals a Central Asian domestication origin. PNAS, 112: 13639–44.CrossRefGoogle ScholarPubMed
Spady, T. C. & Ostrander, E. A. (2008). Canine behavioral genetics: pointing out the phenotypes and herding up the genes. American Journal of Human Genetics, 82: 10–18.CrossRefGoogle ScholarPubMed
Statham, M. J., Trut, L. N., Sacks, B. N. et al. (2011). On the origin of a domesticated species: indentifying the parent population of Russian silver foxes (Vulpes vulpes). Biological Journal of the Linnean Society, 103: 168–75.CrossRefGoogle Scholar
Stockard, C. R. (1941). The Genetic and Endocrinic Basis for Differences in Form and Behavior: As Elucidated by Studies of Contrasted Pure-line Dog Breeds and their Hybrids. Philadelphia, PA: The Wistar Institute of Anatomy and Biology.Google Scholar
Su, N., Du, X. & Chen, L. (2008). FGF signaling: its role in bone development and human skeleton diseases. Frontiers in Bioscience, 13: 2842–65.CrossRefGoogle ScholarPubMed
Sundqvist, A. K., Bjornfeldt, S., Leonard, J. A. et al. (2006). Unequal contribution of sexes in the origin of dog breeds. Genetics, 172: 1121–8.CrossRefGoogle ScholarPubMed
Sutter, N. B., Bustamante, C. D., Chase, K. et al. (2007). A single IGF1 allele is a major determinant of small size in dogs. Science, 316: 112–15.CrossRefGoogle ScholarPubMed
Sutter, N. B. & Ostrander, E. A. (2004). Dog star rising: the canine genetic system. Nature Reviews Genetics, 5: 900–10.CrossRefGoogle ScholarPubMed
Thalmann, O., Shapiro, B., Cui, P. et al. (2013) Complete mitochondrial genomes of ancient canids suggest a European origin of domestic dogs. Nature, 342: 871–4.Google ScholarPubMed
Trut, L. (1999). Early canid domestication: the farm-fox experiment. American Scientist, 87: 160–9.CrossRefGoogle Scholar
Trut, L., Oskina, I. & Kharlamova, A. (2009). Animal evolution during domestication: the domesticated fox as a model. Bioessays, 31: 349–60.CrossRefGoogle Scholar
Vigne, J. D. (2011). The origins of animal domestication and husbandry: a major change in the history of humanity and the biosphere. Comptes Rendus Biologie, 334: 171–81.CrossRefGoogle Scholar
Vilà, C., Savolainen, P., Maldonado, J. E. et al. (1997). Multiple and ancient origins of the domestic dog. Science, 276: 1687–9.CrossRefGoogle ScholarPubMed
Vilà, C., Seddon, J. & Ellegren, H. (2005). Genes of domestic mammals augmented by backcrossing with wild ancestors. Trends in Genetics, 21: 214–18.CrossRefGoogle ScholarPubMed
Vilà, C. & Wayne, R. K. (1999). Hybridization between wolves and dogs. Conservation Biology, 13: 195–8.CrossRefGoogle Scholar
Visscher, P. M. (2008). Sizing up human height variation. Nature Genetics, 40: 489–90.CrossRefGoogle ScholarPubMed
Voight, B. F., Kudaravalli, S., Wen, X. & Pritchard, J. K. (2006). A map of recent positive selection in the human genome. PLoS Biology, 4: e72.CrossRefGoogle ScholarPubMed
vonHoldt, B. M., Pollinger, J. P., Lohmueller, K. E. et al. (2010). Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature, 464: 898–902.CrossRefGoogle ScholarPubMed
vonHoldt, B. M., Stahler, D. R., Smith, D. W. et al. (2008). The genealogy and genetic viability of reintroduced Yellowstone gray wolves. Molecular Ecology, 17: 252–74.CrossRefGoogle Scholar
Wang, G.-D., Zhai, W., Yang, H.-C., Wang, L., Zhong, L., Liu, Y.-H., et al. (2016) Out of southern East Asia: the natural history of domestic dogs across the world. Cell Research, 26: 21–33.CrossRefGoogle Scholar
Wang, X. & Tedford, R. H. (2008). Dogs: Their Fossil Relatives and Evolutionary History. New York, NY: Columbia University Press.CrossRefGoogle Scholar
Waters, M. R. & Stafford, T. W. Jr. (2007). Redefining the age of Clovis: implications for the peopling of the Americas. Science, 315: 1122–6.CrossRefGoogle ScholarPubMed
Wayne, R. K. & vonHoldt, B. M. (2012). Evolutionary genomics of dog domestication. Mammalian Genome, 23: 3–18.CrossRefGoogle ScholarPubMed
Wellcome Trust Case Consortium (2007). Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature, 447: 661–78.
Yakar, S., Rosen, C. J., Beamer, W. G. et al. (2002). Circulating levels of IGF-1 directly regulate bone growth and density. Journal of Clinical Investigation, 110: 771–81.CrossRefGoogle ScholarPubMed
Young, A. & Bannasch, D. (2006). Morphological variation in the dog. In The Dog and Its Genome, eds. Ostrander, E. A., Giger, U. & Lindblad-Toh, K.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 47–65.Google Scholar
Zeder, M. A. (2008). Domestication and early agriculture in the Mediterranean Basin: origins, diffusion, and impact. Proceedings of the National Academy of Sciences USA, 105: 11597–604.CrossRefGoogle ScholarPubMed
Zeder, M. A. (2012). The domestication of animals. Journal of Anthropological Research, 68(2): 161.CrossRefGoogle Scholar
Zeder, M. A., Emshwiller, E., Smith, B. D. & Bradley, D. G. (2006). Documenting domestication: the intersection of genetics and archaeology. Trends in Genetics, 22: 139–55.CrossRefGoogle ScholarPubMed

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