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Arctic-adapted dogs emerged at the Pleistocene–Holocene transition | Science
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Arctic-adapted dogs emerged at the Pleistocene–Holocene transition

Mikkel-Holger S. Sinding https://orcid.org/0000-0003-1371-219X, Shyam Gopalakrishnan https://orcid.org/0000-0002-2004-6810, Jazmín Ramos-Madrigal https://orcid.org/0000-0002-1661-7991, Marc de Manuel https://orcid.org/0000-0002-1245-0127, Vladimir V. Pitulko https://orcid.org/0000-0001-5672-2756, Lukas Kuderna https://orcid.org/0000-0002-9992-9295, Tatiana R. Feuerborn https://orcid.org/0000-0003-1610-3402, Laurent A. F. Frantz https://orcid.org/0000-0001-8030-3885, Filipe G. Vieira https://orcid.org/0000-0002-8464-7770, Jonas Niemann https://orcid.org/0000-0002-5153-100X, Jose A. Samaniego Castruita, Christian Carøe https://orcid.org/0000-0001-9601-6768, Emilie U. Andersen-Ranberg https://orcid.org/0000-0002-3102-4844, Peter D. Jordan https://orcid.org/0000-0002-2837-3920, Elena Y. Pavlova, Pavel A. Nikolskiy https://orcid.org/0000-0001-6547-9890, Aleksei K. Kasparov https://orcid.org/0000-0001-7761-9301, Varvara V. Ivanova https://orcid.org/0000-0002-7614-660X, Eske Willerslev https://orcid.org/0000-0002-7081-6748, Pontus Skoglund https://orcid.org/0000-0002-3021-5913, Merete Fredholm https://orcid.org/0000-0002-3563-7648, Sanne Eline Wennerberg https://orcid.org/0000-0003-1726-171X, Mads Peter Heide-Jørgensen https://orcid.org/0000-0003-4846-7622, Rune Dietz https://orcid.org/0000-0001-9652-317X, Christian Sonne https://orcid.org/0000-0001-5723-5263, Morten Meldgaard, Love Dalén https://orcid.org/0000-0001-8270-7613, Greger Larson https://orcid.org/0000-0002-4092-0392, Bent Petersen https://orcid.org/0000-0002-2472-8317, Thomas Sicheritz-Pontén https://orcid.org/0000-0001-6615-1141, Lutz Bachmann https://orcid.org/0000-0001-7451-2074, Øystein Wiig https://orcid.org/0000-0003-0395-5251, Tomas Marques-Bonet https://orcid.org/0000-0002-5597-3075, Anders J. Hansen https://orcid.org/0000-0002-1890-2702, and M. Thomas P. Gilbert https://orcid.org/0000-0002-5805-7195Authors Info & Affiliations
Science
26 Jun 2020
Vol 368, Issue 6498
pp. 1495-1499

Sled dog arctic adaptations go far back

Dogs have been used for sledding in the Arctic as far back as ∼9500 years ago. However, the relationships among the earliest sled dogs, other dog populations, and wolves are unknown. Sinding et al. sequenced an ancient sled dog, 10 modern sled dogs, and an ancient wolf and analyzed their genetic relationships with other modern dogs. This analysis indicates that sled dogs represent an ancient lineage going back at least 9500 years and that wolves bred with the ancestors of sled dogs and precontact American dogs. However, gene flow between sled dogs and wolves likely stopped before ∼9500 years ago.
Science, this issue p. 1495

Abstract

Although sled dogs are one of the most specialized groups of dogs, their origin and evolution has received much less attention than many other dog groups. We applied a genomic approach to investigate their spatiotemporal emergence by sequencing the genomes of 10 modern Greenland sled dogs, an ~9500-year-old Siberian dog associated with archaeological evidence for sled technology, and an ~33,000-year-old Siberian wolf. We found noteworthy genetic similarity between the ancient dog and modern sled dogs. We detected gene flow from Pleistocene Siberian wolves, but not modern American wolves, to present-day sled dogs. The results indicate that the major ancestry of modern sled dogs traces back to Siberia, where sled dog–specific haplotypes of genes that potentially relate to Arctic adaptation were established by 9500 years ago.

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Supplementary Material

Summary

Materials and Methods
Figs. S1 to S21
Tables S1 to S6
References (2770)
MDAR Reproducibility Checklist

Resources

File (aaz8599-sinding-sm.pdf)
File (aaz8599-sinding_sm-reproducibility-checklist.pdf)

References and Notes

1
V. V. Pitulko, A. K. Kasparov, Ancient Arctic hunters: Material culture and survival strategy. Arctic Anthropol. 33, 1–36 (1996).
2
V. V. Pitulko, A. K. Kasparov, Archaeological dogs from the Early Holocene Zhokhov site in the Eastern Siberian Arctic. J. Archaeol. Sci. Rep. 13, 491–515 (2017).
3
M. Ní Leathlobhair, A. R. Perri, E. K. Irving-Pease, K. E. Witt, A. Linderholm, J. Haile, O. Lebrasseur, C. Ameen, J. Blick, A. R. Boyko, S. Brace, Y. N. Cortes, S. J. Crockford, A. Devault, E. A. Dimopoulos, M. Eldridge, J. Enk, S. Gopalakrishnan, K. Gori, V. Grimes, E. Guiry, A. J. Hansen, A. Hulme-Beaman, J. Johnson, A. Kitchen, A. K. Kasparov, Y.-M. Kwon, P. A. Nikolskiy, C. P. Lope, A. Manin, T. Martin, M. Meyer, K. N. Myers, M. Omura, J.-M. Rouillard, E. Y. Pavlova, P. Sciulli, M. S. Sinding, A. Strakova, V. V. Ivanova, C. Widga, E. Willerslev, V. V. Pitulko, I. Barnes, M. T. P. Gilbert, K. M. Dobney, R. S. Malhi, E. P. Murchison, G. Larson, L. A. F. Frantz, The evolutionary history of dogs in the Americas. Science 361, 81–85 (2018).
4
See the supplementary materials.
5
P. Skoglund, E. Ersmark, E. Palkopoulou, L. Dalén, Ancient wolf genome reveals an early divergence of domestic dog ancestors and admixture into high-latitude breeds. Curr. Biol. 25, 1515–1519 (2015).
6
A. Baez-Ortega, K. Gori, A. Strakova, J. L. Allen, K. M. Allum, L. Bansse-Issa, T. N. Bhutia, J. L. Bisson, C. Briceño, A. Castillo Domracheva, A. M. Corrigan, H. R. Cran, J. T. Crawford, E. Davis, K. F. de Castro, A. B. de Nardi, A. P. de Vos, L. Delgadillo Keenan, E. M. Donelan, A. R. Espinoza Huerta, I. A. Faramade, M. Fazil, E. Fotopoulou, S. N. Fruean, F. Gallardo-Arrieta, O. Glebova, P. G. Gouletsou, R. F. Häfelin Manrique, J. J. G. P. Henriques, R. S. Horta, N. Ignatenko, Y. Kane, C. King, D. Koenig, A. Krupa, S. J. Kruzeniski, Y.-M. Kwon, M. Lanza-Perea, M. Lazyan, A. M. Lopez Quintana, T. Losfelt, G. Marino, S. Martínez Castañeda, M. F. Martínez-López, M. Meyer, E. J. Migneco, B. Nakanwagi, K. B. Neal, W. Neunzig, M. Ní Leathlobhair, S. J. Nixon, A. Ortega-Pacheco, F. Pedraza-Ordoñez, M. C. Peleteiro, K. Polak, R. J. Pye, J. F. Reece, J. Rojas Gutierrez, H. Sadia, S. K. Schmeling, O. Shamanova, A. G. Sherlock, M. Stammnitz, A. E. Steenland-Smit, A. Svitich, L. J. Tapia Martínez, I. Thoya Ngoka, C. G. Torres, E. M. Tudor, M. G. van der Wel, B. A. Viţălaru, S. A. Vural, O. Walkinton, J. Wang, A. S. Wehrle-Martinez, S. A. E. Widdowson, M. R. Stratton, L. B. Alexandrov, I. Martincorena, E. P. Murchison, Somatic evolution and global expansion of an ancient transmissible cancer lineage. Science 365, eaau9923 (2019).
7
Z. Fan, P. Silva, I. Gronau, S. Wang, A. S. Armero, R. M. Schweizer, O. Ramirez, J. Pollinger, M. Galaverni, D. Ortega Del-Vecchyo, L. Du, W. Zhang, Z. Zhang, J. Xing, C. Vilà, T. Marques-Bonet, R. Godinho, B. Yue, R. K. Wayne, Worldwide patterns of genomic variation and admixture in gray wolves. Genome Res. 26, 163–173 (2016).
8
B. Muus, F. Salomonsen, C. Vibe, Grønlands Fauna [in Danish] (Gyldendal, 1981).
9
M. Raghavan, M. DeGiorgio, A. Albrechtsen, I. Moltke, P. Skoglund, T. S. Korneliussen, B. Grønnow, M. Appelt, H. C. Gulløv, T. M. Friesen, W. Fitzhugh, H. Malmström, S. Rasmussen, J. Olsen, L. Melchior, B. T. Fuller, S. M. Fahrni, T. Stafford Jr., V. Grimes, M. A. P. Renouf, J. Cybulski, N. Lynnerup, M. M. Lahr, K. Britton, R. Knecht, J. Arneborg, M. Metspalu, O. E. Cornejo, A.-S. Malaspinas, Y. Wang, M. Rasmussen, V. Raghavan, T. V. O. Hansen, E. Khusnutdinova, T. Pierre, K. Dneprovsky, C. Andreasen, H. Lange, M. G. Hayes, J. Coltrain, V. A. Spitsyn, A. Götherström, L. Orlando, T. Kivisild, R. Villems, M. H. Crawford, F. C. Nielsen, J. Dissing, J. Heinemeier, M. Meldgaard, C. Bustamante, D. H. O’Rourke, M. Jakobsson, M. T. P. Gilbert, R. Nielsen, E. Willerslev, The genetic prehistory of the New World Arctic. Science 345, 1255832 (2014).
10
X. Yi, Y. Liang, E. Huerta-Sanchez, X. Jin, Z. X. P. Cuo, J. E. Pool, X. Xu, H. Jiang, N. Vinckenbosch, T. S. Korneliussen, H. Zheng, T. Liu, W. He, K. Li, R. Luo, X. Nie, H. Wu, M. Zhao, H. Cao, J. Zou, Y. Shan, S. Li, Q. Yang, P. Asan, P. Ni, G. Tian, J. Xu, X. Liu, T. Jiang, R. Wu, G. Zhou, M. Tang, J. Qin, T. Wang, S. Feng, G. Li, J. Huasang, J. Luosang, W. Wang, F. Chen, Y. Wang, X. Zheng, Z. Li, Z. Bianba, G. Yang, X. Wang, S. Tang, G. Gao, Y. Chen, Z. Luo, L. Gusang, Z. Cao, Q. Zhang, W. Ouyang, X. Ren, H. Liang, H. Zheng, Y. Huang, J. Li, L. Bolund, K. Kristiansen, Y. Li, Y. Zhang, X. Zhang, R. Li, S. Li, H. Yang, R. Nielsen, J. Wang, J. Wang, Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329, 75–78 (2010).
11
C. Tiruppathi, M. Freichel, S. M. Vogel, B. C. Paria, D. Mehta, V. Flockerzi, A. B. Malik, Impairment of store-operated Ca2+ entry in TRPC4(-/-) mice interferes with increase in lung microvascular permeability. Circ. Res. 91, 70–76 (2002).
12
T. Hofmann, M. Schaefer, G. Schultz, T. Gudermann, Subunit composition of mammalian transient receptor potential channels in living cells. Proc. Natl. Acad. Sci. U.S.A. 99, 7461–7466 (2002).
13
K. Zimmermann, J. K. Lennerz, A. Hein, A. S. Link, J. S. Kaczmarek, M. Delling, S. Uysal, J. D. Pfeifer, A. Riccio, D. E. Clapham, Transient receptor potential cation channel, subfamily C, member 5 (TRPC5) is a cold-transducer in the peripheral nervous system. Proc. Natl. Acad. Sci. U.S.A. 108, 18114–18119 (2011).
14
N. Qin, M. P. Neeper, Y. Liu, T. L. Hutchinson, M. L. Lubin, C. M. Flores, TRPV2 is activated by cannabidiol and mediates CGRP release in cultured rat dorsal root ganglion neurons. J. Neurosci. 28, 6231–6238 (2008).
15
V. J. Lynch, O. C. Bedoya-Reina, A. Ratan, M. Sulak, D. I. Drautz-Moses, G. H. Perry, W. Miller, S. C. Schuster, Elephantid Genomes Reveal the Molecular Bases of Woolly Mammoth Adaptations to the Arctic. Cell Rep. 12, 217–228 (2015).
16
S. Kaja, R. C. G. van de Ven, J. G. van Dijk, J. J. G. M. Verschuuren, K. Arahata, R. R. Frants, M. D. Ferrari, A. M. J. M. van den Maagdenberg, J. J. Plomp, Severely impaired neuromuscular synaptic transmission causes muscle weakness in the Cacna1a-mutant mouse rolling Nagoya. Eur. J. Neurosci. 25, 2009–2020 (2007).
17
M. A. Ilardo, I. Moltke, T. S. Korneliussen, J. Cheng, A. J. Stern, F. Racimo, P. de Barros Damgaard, M. Sikora, A. Seguin-Orlando, S. Rasmussen, I. C. L. van den Munckhof, R. Ter Horst, L. A. B. Joosten, M. G. Netea, S. Salingkat, R. Nielsen, E. Willerslev, Physiological and genetic adaptations to diving in sea nomads. Cell 173, 569–580.e15 (2018).
18
V. Wang, D. A. Davis, M. Haque, L. E. Huang, R. Yarchoan, Differential gene up-regulation by hypoxia-inducible factor-1alpha and hypoxia-inducible factor-2alpha in HEK293T cells. Cancer Res. 65, 3299–3306 (2005).
19
E. Axelsson, A. Ratnakumar, M.-L. Arendt, K. Maqbool, M. T. Webster, M. Perloski, O. Liberg, J. M. Arnemo, A. Hedhammar, K. Lindblad-Toh, The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495, 360–364 (2013).
20
M. Arendt, K. M. Cairns, J. W. O. Ballard, P. Savolainen, E. Axelsson, Diet adaptation in dog reflects spread of prehistoric agriculture. Heredity 117, 301–306 (2016).
21
E. A. Rosenthal, J. Ranchalis, D. R. Crosslin, A. Burt, J. D. Brunzell, A. G. Motulsky, D. A. Nickerson, E. M. Wijsman, G. P. Jarvik; NHLBI GO Exome Sequencing Project, Joint linkage and association analysis with exome sequence data implicates SLC25A40 in hypertriglyceridemia. Am. J. Hum. Genet. 93, 1035–1045 (2013).
22
A. Turkieh, C. Caubère, M. Barutaut, F. Desmoulin, R. Harmancey, M. Galinier, M. Berry, C. Dambrin, C. Polidori, L. Casteilla, F. Koukoui, P. Rouet, F. Smih, Apolipoprotein O is mitochondrial and promotes lipotoxicity in heart. J. Clin. Invest. 124, 2277–2286 (2014).
23
S. Liu, E. D. Lorenzen, M. Fumagalli, B. Li, K. Harris, Z. Xiong, L. Zhou, T. S. Korneliussen, M. Somel, C. Babbitt, G. Wray, J. Li, W. He, Z. Wang, W. Fu, X. Xiang, C. C. Morgan, A. Doherty, M. J. O’Connell, J. O. McInerney, E. W. Born, L. Dalén, R. Dietz, L. Orlando, C. Sonne, G. Zhang, R. Nielsen, E. Willerslev, J. Wang, Population genomics reveal recent speciation and rapid evolutionary adaptation in polar bears. Cell 157, 785–794 (2014).
24
A. Cardona, L. Pagani, T. Antao, D. J. Lawson, C. A. Eichstaedt, B. Yngvadottir, M. T. T. Shwe, J. Wee, I. G. Romero, S. Raj, M. Metspalu, R. Villems, E. Willerslev, C. Tyler-Smith, B. A. Malyarchuk, M. V. Derenko, T. Kivisild, Genome-wide analysis of cold adaptation in indigenous Siberian populations. PLOS ONE 9, e98076 (2014).
25
M. Fumagalli, I. Moltke, N. Grarup, F. Racimo, P. Bjerregaard, M. E. Jørgensen, T. S. Korneliussen, P. Gerbault, L. Skotte, A. Linneberg, C. Christensen, I. Brandslund, T. Jørgensen, E. Huerta-Sánchez, E. B. Schmidt, O. Pedersen, T. Hansen, A. Albrechtsen, R. Nielsen, Greenlandic Inuit show genetic signatures of diet and climate adaptation. Science 349, 1343–1347 (2015).
26
V. V. Pitulko, V. V. Ivanova, A. K. Kasparov, E. Y. Pavlova, Reconstructing prey selection, hunting strategy and seasonality of the early Holocene frozen site in the Siberian High Arctic: A case study on the Zhokhov site faunal remains, De Long Islands. Environ. Archaeol. 20, 120–157 (2015).
27
C. B. Ramsey, M. Scott, H. van der Plicht, Calibration for archaeological and environmental terrestrial samples in the time range 26-50 ka cal BP. Radiocarbon 55, 2021–2027 (2013).
28
L. Orlando, A. Ginolhac, G. Zhang, D. Froese, A. Albrechtsen, M. Stiller, M. Schubert, E. Cappellini, B. Petersen, I. Moltke, P. L. F. Johnson, M. Fumagalli, J. T. Vilstrup, M. Raghavan, T. Korneliussen, A.-S. Malaspinas, J. Vogt, D. Szklarczyk, C. D. Kelstrup, J. Vinther, A. Dolocan, J. Stenderup, A. M. V. Velazquez, J. Cahill, M. Rasmussen, X. Wang, J. Min, G. D. Zazula, A. Seguin-Orlando, C. Mortensen, K. Magnussen, J. F. Thompson, J. Weinstock, K. Gregersen, K. H. Røed, V. Eisenmann, C. J. Rubin, D. C. Miller, D. F. Antczak, M. F. Bertelsen, S. Brunak, K. A. S. Al-Rasheid, O. Ryder, L. Andersson, J. Mundy, A. Krogh, M. T. P. Gilbert, K. Kjær, T. Sicheritz-Ponten, L. J. Jensen, J. V. Olsen, M. Hofreiter, R. Nielsen, B. Shapiro, J. Wang, E. Willerslev, Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499, 74–78 (2013).
29
E. Ersmark, L. Orlando, E. Sandoval-Castellanos, I. Barnes, R. Barnett, A. Stuart, A. Lister, L. Dalén, Population demography and genetic diversity in the Pleistocene cave lion. Open Quaternary 1, p.Art.4 (2015); .
30
J. Dabney, M. Knapp, I. Glocke, M.-T. Gansauge, A. Weihmann, B. Nickel, C. Valdiosera, N. García, S. Pääbo, J.-L. Arsuaga, M. Meyer, Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl. Acad. Sci. U.S.A. 110, 15758–15763 (2013).
31
M. E. Allentoft, M. Sikora, K.-G. Sjögren, S. Rasmussen, M. Rasmussen, J. Stenderup, P. B. Damgaard, H. Schroeder, T. Ahlström, L. Vinner, A.-S. Malaspinas, A. Margaryan, T. Higham, D. Chivall, N. Lynnerup, L. Harvig, J. Baron, P. Della Casa, P. Dąbrowski, P. R. Duffy, A. V. Ebel, A. Epimakhov, K. Frei, M. Furmanek, T. Gralak, A. Gromov, S. Gronkiewicz, G. Grupe, T. Hajdu, R. Jarysz, V. Khartanovich, A. Khokhlov, V. Kiss, J. Kolář, A. Kriiska, I. Lasak, C. Longhi, G. McGlynn, A. Merkevicius, I. Merkyte, M. Metspalu, R. Mkrtchyan, V. Moiseyev, L. Paja, G. Pálfi, D. Pokutta, Ł. Pospieszny, T. D. Price, L. Saag, M. Sablin, N. Shishlina, V. Smrčka, V. I. Soenov, V. Szeverényi, G. Tóth, S. V. Trifanova, L. Varul, M. Vicze, L. Yepiskoposyan, V. Zhitenev, L. Orlando, T. Sicheritz-Pontén, S. Brunak, R. Nielsen, K. Kristiansen, E. Willerslev, Population genomics of Bronze Age Eurasia. Nature 522, 167–172 (2015).
32
C. Carøe, S. Gopalakrishnan, L. Vinner, S. S. T. Mak, M.-H. S. Sinding, J. A. Samaniego, N. Wales, T. Sicheritz-Pontén, M. T. P. Gilbert, Single-tube library preparation for degraded DNA. Methods Ecol. Evol. (2017).
33
M. Schubert, L. Ermini, C. Der Sarkissian, H. Jónsson, A. Ginolhac, R. Schaefer, M. D. Martin, R. Fernández, M. Kircher, M. McCue, E. Willerslev, L. Orlando, Characterization of ancient and modern genomes by SNP detection and phylogenomic and metagenomic analysis using PALEOMIX. Nat. Protoc. 9, 1056–1082 (2014).
34
M. Schubert, S. Lindgreen, L. Orlando, AdapterRemoval v2: Rapid adapter trimming, identification, and read merging. BMC Res. Notes 9, 88 (2016).
35
S. Gopalakrishnan, J. A. Samaniego Castruita, M. S. Sinding, L. F. K. Kuderna, J. Räikkönen, B. Petersen, T. Sicheritz-Ponten, G. Larson, L. Orlando, T. Marques-Bonet, A. J. Hansen, L. Dalén, M. T. P. Gilbert, The wolf reference genome sequence (Canis lupus lupus) and its implications for Canis spp. population genomics. BMC Genomics 18, 495 (2017).
36
H. Li, B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, R. Durbin; 1000 Genome Project Data Processing Subgroup, The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
37
M. A. DePristo, E. Banks, R. Poplin, K. V. Garimella, J. R. Maguire, C. Hartl, A. A. Philippakis, G. del Angel, M. A. Rivas, M. Hanna, A. McKenna, T. J. Fennell, A. M. Kernytsky, A. Y. Sivachenko, K. Cibulskis, S. B. Gabriel, D. Altshuler, M. J. Daly, A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491–498 (2011).
38
A. McKenna, M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis, A. Kernytsky, K. Garimella, D. Altshuler, S. Gabriel, M. Daly, M. A. DePristo, The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).
39
H. Jónsson, A. Ginolhac, M. Schubert, P. L. F. Johnson, L. Orlando, mapDamage2.0: Fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 29, 1682–1684 (2013).
40
L. A. F. Frantz, V. E. Mullin, M. Pionnier-Capitan, O. Lebrasseur, M. Ollivier, A. Perri, A. Linderholm, V. Mattiangeli, M. D. Teasdale, E. A. Dimopoulos, A. Tresset, M. Duffraisse, F. McCormick, L. Bartosiewicz, E. Gál, É. A. Nyerges, M. V. Sablin, S. Bréhard, M. Mashkour, A. Bălăşescu, B. Gillet, S. Hughes, O. Chassaing, C. Hitte, J.-D. Vigne, K. Dobney, C. Hänni, D. G. Bradley, G. Larson, Genomic and archaeological evidence suggest a dual origin of domestic dogs. Science 352, 1228–1231 (2016).
41
L. R. Botigué, S. Song, A. Scheu, S. Gopalan, A. L. Pendleton, M. Oetjens, A. M. Taravella, T. Seregély, A. Zeeb-Lanz, R.-M. Arbogast, D. Bobo, K. Daly, M. Unterländer, J. Burger, J. M. Kidd, K. R. Veeramah, Ancient European dog genomes reveal continuity since the Early Neolithic. Nat. Commun. 8, 16082 (2017).
42
K. J. Galinsky, G. Bhatia, P.-R. Loh, S. Georgiev, S. Mukherjee, N. J. Patterson, A. L. Price, Fast principal-component analysis reveals convergent evolution of ADH1B in Europe and East Asia. Am. J. Hum. Genet. 98, 456–472 (2016).
43
A. L. Price, N. J. Patterson, R. M. Plenge, M. E. Weinblatt, N. A. Shadick, D. Reich, Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904–909 (2006).
44
C. C. Chang, C. C. Chow, L. C. Tellier, S. Vattikuti, S. M. Purcell, J. J. Lee, Second-generation PLINK: Rising to the challenge of larger and richer datasets. Gigascience 4, 7 (2015).
45
R. Nielsen, J. S. Paul, A. Albrechtsen, Y. S. Song, Genotype and SNP calling from next-generation sequencing data. Nat. Rev. Genet. 12, 443–451 (2011).
46
T. S. Korneliussen, A. Albrechtsen, R. Nielsen, ANGSD: Analysis of next generation sequencing data. BMC Bioinformatics 15, 356 (2014).
47
L. Skotte, T. S. Korneliussen, A. Albrechtsen, Estimating individual admixture proportions from next generation sequencing data. Genetics 195, 693–702 (2013).
48
J. K. Pickrell, J. K. Pritchard, Inference of population splits and mixtures from genome-wide allele frequency data. PLOS Genet. 8, e1002967 (2012).
49
E. P. Murchison, D. C. Wedge, L. B. Alexandrov, B. Fu, I. Martincorena, Z. Ning, J. M. C. Tubio, E. I. Werner, J. Allen, A. B. De Nardi, E. M. Donelan, G. Marino, A. Fassati, P. J. Campbell, F. Yang, A. Burt, R. A. Weiss, M. R. Stratton, Transmissible [corrected] dog cancer genome reveals the origin and history of an ancient cell lineage. Science 343, 437–440 (2014).
50
S. Purcell, B. Neale, K. Todd-Brown, L. Thomas, M. A. R. Ferreira, D. Bender, J. Maller, P. Sklar, P. I. W. de Bakker, M. J. Daly, P. C. Sham, PLINK: A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).
51
E. Paradis, J. Claude, K. Strimmer, APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).
52
N. Patterson, P. Moorjani, Y. Luo, S. Mallick, N. Rohland, Y. Zhan, T. Genschoreck, T. Webster, D. Reich, Ancient admixture in human history. Genetics 192, 1065–1093 (2012).
53
S. Gopalakrishnan, M. S. Sinding, J. Ramos-Madrigal, J. Niemann, J. A. Samaniego Castruita, F. G. Vieira, C. Carøe, M. M. Montero, L. Kuderna, A. Serres, V. M. González-Basallote, Y.-H. Liu, G.-D. Wang, T. Marques-Bonet, S. Mirarab, C. Fernandes, P. Gaubert, K.-P. Koepfli, J. Budd, E. K. Rueness, C. Sillero, M. P. Heide-Jørgensen, B. Petersen, T. Sicheritz-Ponten, L. Bachmann, Ø. Wiig, A. J. Hansen, M. T. P. Gilbert, Interspecific gene flow shaped the evolution of the genus Canis. Curr. Biol. 28, 3441–3449.e5 (2018).
54
P. Freuchen, “Den rene eskimohund,” in Hundevennernes jul (Dansk Kennel Klub, 1943), pp. 39–42.
55
S. P. Young, E. A. Goldman, The Wolves of North America: Part I. Their History, Life Habits, Economic Status, and Control (Dover, 1944).
56
M. S. Sinding, S. Gopalakrishan, F. G. Vieira, J. A. Samaniego Castruita, K. Raundrup, M. P. Heide Jørgensen, M. Meldgaard, B. Petersen, T. Sicheritz-Ponten, J. B. Mikkelsen, U. Marquard-Petersen, R. Dietz, C. Sonne, L. Dalén, L. Bachmann, Ø. Wiig, A. J. Hansen, M. T. P. Gilbert, Population genomics of grey wolves and wolf-like canids in North America. PLOS Genet. 14, e1007745 (2018).
57
G. Bhatia, N. Patterson, S. Sankararaman, A. L. Price, Estimating and interpreting FST: The impact of rare variants. Genome Res. 23, 1514–1521 (2013).
58
H. Chen, N. Patterson, D. Reich, Population differentiation as a test for selective sweeps. Genome Res. 20, 393–402 (2010).
59
P. H. Lee, C. O’Dushlaine, B. Thomas, S. M. Purcell, INRICH: Interval-based enrichment analysis for genome-wide association studies. Bioinformatics 28, 1797–1799 (2012).
60
G.-D. Wang, W. Zhai, H.-C. Yang, L. Wang, L. Zhong, Y.-H. Liu, R.-X. Fan, T.-T. Yin, C.-L. Zhu, A. D. Poyarkov, D. M. Irwin, M. K. Hytönen, H. Lohi, C.-I. Wu, P. Savolainen, Y.-P. Zhang, Out of southern East Asia: The natural history of domestic dogs across the world. Cell Res. 26, 21–33 (2016).
61
M. Wiedmer, A. Oevermann, A RAB3GAP1 SINE insertion in Alaskan huskies with polyneuropathy, ocular abnormalities, and neuronal vacuolation (POANV) resembling human Warburg micro microsyndrome 1 (WARBM1). G3 6, 225–262 (2016).
62
B. Decker, B. W. Davis, M. Rimbault, A. H. Long, E. Karlins, V. Jagannathan, R. Reiman, H. G. Parker, C. Drögemüller, J. J. Corneveaux, E. S. Chapman, J. M. Trent, T. Leeb, M. J. Huentelman, R. K. Wayne, D. M. Karyadi, E. A. Ostrander, Comparison against 186 canid whole-genome sequences reveals survival strategies of an ancient clonally transmissible canine tumor. Genome Res. 25, 1646–1655 (2015).
63
B. M. vonHoldt, J. A. Cahill, Z. Fan, I. Gronau, J. Robinson, J. P. Pollinger, B. Shapiro, J. Wall, R. K. Wayne, Whole-genome sequence analysis shows that two endemic species of North American wolf are admixtures of the coyote and gray wolf. Sci. Adv. 2, e1501714 (2016).
64
A. H. Freedman, I. Gronau, R. M. Schweizer, D. Ortega-Del Vecchyo, E. Han, P. M. Silva, M. Galaverni, Z. Fan, P. Marx, B. Lorente-Galdos, H. Beale, O. Ramirez, F. Hormozdiari, C. Alkan, C. Vilà, K. Squire, E. Geffen, J. Kusak, A. R. Boyko, H. G. Parker, C. Lee, V. Tadigotla, A. Siepel, C. D. Bustamante, T. T. Harkins, S. F. Nelson, E. A. Ostrander, T. Marques-Bonet, R. K. Wayne, J. Novembre, Genome sequencing highlights the dynamic early history of dogs. PLOS Genet. 10, e1004016 (2014).
65
G.-D. Wang, W. Zhai, H.-C. Yang, R.-X. Fan, X. Cao, L. Zhong, L. Wang, F. Liu, H. Wu, L.-G. Cheng, A. D. Poyarkov, N. A. Poyarkov Jr., S.-S. Tang, W.-M. Zhao, Y. Gao, X.-M. Lv, D. M. Irwin, P. Savolainen, C.-I. Wu, Y.-P. Zhang, The genomics of selection in dogs and the parallel evolution between dogs and humans. Nat. Commun. 4, 1860 (2013).
66
W. Zhang, Z. Fan, E. Han, R. Hou, L. Zhang, M. Galaverni, J. Huang, H. Liu, P. Silva, P. Li, J. P. Pollinger, L. Du, X. Zhang, B. Yue, R. K. Wayne, Z. Zhang, Hypoxia adaptations in the grey wolf (Canis lupus chanco) from Qinghai-Tibet Plateau. PLOS Genet. 10, e1004466 (2014).
67
K. Lindblad-Toh, C. M. Wade, T. S. Mikkelsen, E. K. Karlsson, D. B. Jaffe, M. Kamal, M. Clamp, J. L. Chang, E. J. Kulbokas 3rd, M. C. Zody, E. Mauceli, X. Xie, M. Breen, R. K. Wayne, E. A. Ostrander, C. P. Ponting, F. Galibert, D. R. Smith, P. J. DeJong, E. Kirkness, P. Alvarez, T. Biagi, W. Brockman, J. Butler, C.-W. Chin, A. Cook, J. Cuff, M. J. Daly, D. DeCaprio, S. Gnerre, M. Grabherr, M. Kellis, M. Kleber, C. Bardeleben, L. Goodstadt, A. Heger, C. Hitte, L. Kim, K.-P. Koepfli, H. G. Parker, J. P. Pollinger, S. M. J. Searle, N. B. Sutter, R. Thomas, C. Webber, J. Baldwin, A. Abebe, A. Abouelleil, L. Aftuck, M. Ait-Zahra, T. Aldredge, N. Allen, P. An, S. Anderson, C. Antoine, H. Arachchi, A. Aslam, L. Ayotte, P. Bachantsang, A. Barry, T. Bayul, M. Benamara, A. Berlin, D. Bessette, B. Blitshteyn, T. Bloom, J. Blye, L. Boguslavskiy, C. Bonnet, B. Boukhgalter, A. Brown, P. Cahill, N. Calixte, J. Camarata, Y. Cheshatsang, J. Chu, M. Citroen, A. Collymore, P. Cooke, T. Dawoe, R. Daza, K. Decktor, S. DeGray, N. Dhargay, K. Dooley, K. Dooley, P. Dorje, K. Dorjee, L. Dorris, N. Duffey, A. Dupes, O. Egbiremolen, R. Elong, J. Falk, A. Farina, S. Faro, D. Ferguson, P. Ferreira, S. Fisher, M. FitzGerald, K. Foley, C. Foley, A. Franke, D. Friedrich, D. Gage, M. Garber, G. Gearin, G. Giannoukos, T. Goode, A. Goyette, J. Graham, E. Grandbois, K. Gyaltsen, N. Hafez, D. Hagopian, B. Hagos, J. Hall, C. Healy, R. Hegarty, T. Honan, A. Horn, N. Houde, L. Hughes, L. Hunnicutt, M. Husby, B. Jester, C. Jones, A. Kamat, B. Kanga, C. Kells, D. Khazanovich, A. C. Kieu, P. Kisner, M. Kumar, K. Lance, T. Landers, M. Lara, W. Lee, J.-P. Leger, N. Lennon, L. Leuper, S. LeVine, J. Liu, X. Liu, Y. Lokyitsang, T. Lokyitsang, A. Lui, J. Macdonald, J. Major, R. Marabella, K. Maru, C. Matthews, S. McDonough, T. Mehta, J. Meldrim, A. Melnikov, L. Meneus, A. Mihalev, T. Mihova, K. Miller, R. Mittelman, V. Mlenga, L. Mulrain, G. Munson, A. Navidi, J. Naylor, T. Nguyen, N. Nguyen, C. Nguyen, T. Nguyen, R. Nicol, N. Norbu, C. Norbu, N. Novod, T. Nyima, P. Olandt, B. O’Neill, K. O’Neill, S. Osman, L. Oyono, C. Patti, D. Perrin, P. Phunkhang, F. Pierre, M. Priest, A. Rachupka, S. Raghuraman, R. Rameau, V. Ray, C. Raymond, F. Rege, C. Rise, J. Rogers, P. Rogov, J. Sahalie, S. Settipalli, T. Sharpe, T. Shea, M. Sheehan, N. Sherpa, J. Shi, D. Shih, J. Sloan, C. Smith, T. Sparrow, J. Stalker, N. Stange-Thomann, S. Stavropoulos, C. Stone, S. Stone, S. Sykes, P. Tchuinga, P. Tenzing, S. Tesfaye, D. Thoulutsang, Y. Thoulutsang, K. Topham, I. Topping, T. Tsamla, H. Vassiliev, V. Venkataraman, A. Vo, T. Wangchuk, T. Wangdi, M. Weiand, J. Wilkinson, A. Wilson, S. Yadav, S. Yang, X. Yang, G. Young, Q. Yu, J. Zainoun, L. Zembek, A. Zimmer, E. S. Lander, Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438, 803–819 (2005).
68
C. D. Marsden, D. Ortega-Del Vecchyo, D. P. O’Brien, J. F. Taylor, O. Ramirez, C. Vilà, T. Marques-Bonet, R. D. Schnabel, R. K. Wayne, K. E. Lohmueller, Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs. Proc. Natl. Acad. Sci. U.S.A. 113, 152–157 (2016).
69
A. Auton, Y. Rui Li, J. Kidd, K. Oliveira, J. Nadel, J. K. Holloway, J. J. Hayward, P. E. Cohen, J. M. Greally, J. Wang, C. D. Bustamante, A. R. Boyko, Genetic recombination is targeted towards gene promoter regions in dogs. PLOS Genet. 9, e1003984 (2013).
70
L. M. Shannon, R. H. Boyko, M. Castelhano, E. Corey, J. J. Hayward, C. McLean, M. E. White, M. Abi Said, B. A. Anita, N. I. Bondjengo, J. Calero, A. Galov, M. Hedimbi, B. Imam, R. Khalap, D. Lally, A. Masta, K. C. Oliveira, L. Pérez, J. Randall, N. M. Tam, F. J. Trujillo-Cornejo, C. Valeriano, N. B. Sutter, R. J. Todhunter, C. D. Bustamante, A. R. Boyko, Genetic structure in village dogs reveals a Central Asian domestication origin. Proc. Natl. Acad. Sci. U.S.A. 112, 13639–13644 (2015).

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