Editor’s summary
Modern dogs display highly divergent morphology. The vast majority of this diversity was generated through intensive human selection over only the past 200 to 300 years. Dogs were domesticated at least 10,000 years ago, but we know little about their diversity during most of their time with humans. Evin et al. looked at more than 640 canid crania over the past 50,000 years (see the Perspective by Fillios) and found that by the beginning of the Holocene, dogs already displayed extensive variation. Although dog crania from the Pleistocene were not distinguishable from wolves, the degree of differentiation seen by the end of the era suggests even earlier human-canid associations. —Sacha Vignieri
Abstract
Dogs exhibit an exceptional range of morphological diversity as a result of their long-term association with humans. Attempts to identify when dog morphological variation began to expand have been constrained by the limited number of Pleistocene specimens, the fragmentary nature of remains, and difficulties in distinguishing early dogs from wolves on the basis of skeletal morphology. In this study, we used three-dimensional geometric morphometrics to analyze the size and shape of 643 canid crania spanning the past 50,000 years. Our analyses show that a distinctive dog morphology first appeared at about 11,000 calibrated years before present, and substantial phenotypic diversity already existed in early Holocene dogs. Thus, this variation emerged many millennia before the intense human-mediated selection shaping modern dog breeds beginning in the 19th century.
Access the full article
View all access options to continue reading this article.
Supplementary Materials
The PDF file includes:
Other Supplementary Material for this manuscript includes the following:
MDAR Reproducibility Checklist
- Download
- 180.50 KB
- Download
- 160.61 KB
- Download
- 541.04 KB
References and Notes
1
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).
2
A. R. Perri, T. R. Feuerborn, L. A. F. Frantz, G. Larson, R. S. Malhi, D. J. Meltzer, K. E. Witt, Dog domestication and the dual dispersal of people and dogs into the Americas. Proc. Natl. Acad. Sci. U.S.A. 118, e2010083118 (2021).
3
A. Bergström, L. Frantz, R. Schmidt, E. Ersmark, O. Lebrasseur, L. Girdland-Flink, A. T. Lin, J. Storå, K.-G. Sjögren, D. Anthony, E. Antipina, S. Amiri, G. Bar-Oz, V. I. Bazaliiskii, J. Bulatović, D. Brown, A. Carmagnini, T. Davy, S. Fedorov, I. Fiore, D. Fulton, M. Germonpré, J. Haile, E. K. Irving-Pease, A. Jamieson, L. Janssens, I. Kirillova, L. K. Horwitz, J. Kuzmanovic-Cvetković, Y. Kuzmin, R. J. Losey, D. L. Dizdar, M. Mashkour, M. Novak, V. Onar, D. Orton, M. Pasarić, M. Radivojević, D. Rajković, B. Roberts, H. Ryan, M. Sablin, F. Shidlovskiy, I. Stojanović, A. Tagliacozzo, K. Trantalidou, I. Ullén, A. Villaluenga, P. Wapnish, K. Dobney, A. Götherström, A. Linderholm, L. Dalén, R. Pinhasi, G. Larson, P. Skoglund, Origins and genetic legacy of prehistoric dogs. Science 370, 557–564 (2020).
4
L. Janssens, L. Giemsch, R. Schmitz, M. Street, S. Van Dongen, P. Crombé, A new look at an old dog: Bonn-Oberkassel reconsidered. J. Archaeol. Sci. 92, 126–138 (2018).
5
T. R. Feuerborn, A. Carmagnini, R. J. Losey, T. Nomokonova, A. Askeyev, I. Askeyev, O. Askeyev, E. E. Antipina, M. Appelt, O. P. Bachura, F. Beglane, D. G. Bradley, K. G. Daly, S. Gopalakrishnan, K. Murphy Gregersen, C. Guo, A. V. Gusev, C. Jones, P. A. Kosintsev, Y. V. Kuzmin, V. Mattiangeli, A. R. Perri, A. V. Plekhanov, J. Ramos-Madrigal, A. L. Schmidt, D. Shaymuratova, O. Smith, L. V. Yavorskaya, G. Zhang, E. Willerslev, M. Meldgaard, M. T. P. Gilbert, G. Larson, L. Dalén, A. J. Hansen, M. S. Sinding, L. Frantz, Modern Siberian dog ancestry was shaped by several thousand years of Eurasian-wide trade and human dispersal. Proc. Natl. Acad. Sci. U.S.A. 118, e2100338118 (2021).
6
P. Galeta, M. Lázničková-Galetová, M. Sablin, M. Germonpré, Morphological evidence for early dog domestication in the European Pleistocene: New evidence from a randomization approach to group differences. Anat. Rec. (Hoboken) 304, 42–62 (2021).
7
A. Bergström, D. W. G. Stanton, U. H. Taron, L. Frantz, M. S. Sinding, E. Ersmark, S. Pfrengle, M. Cassatt-Johnstone, O. Lebrasseur, L. Girdland-Flink, D. M. Fernandes, M. Ollivier, L. Speidel, S. Gopalakrishnan, M. V. Westbury, J. Ramos-Madrigal, T. R. Feuerborn, E. Reiter, J. Gretzinger, S. C. Münzel, P. Swali, N. J. Conard, C. Carøe, J. Haile, A. Linderholm, S. Androsov, I. Barnes, C. Baumann, N. Benecke, H. Bocherens, S. Brace, R. F. Carden, D. G. Drucker, S. Fedorov, M. Gasparik, M. Germonpré, S. Grigoriev, P. Groves, S. T. Hertwig, V. V. Ivanova, L. Janssens, R. P. Jennings, A. K. Kasparov, I. V. Kirillova, I. Kurmaniyazov, Y. V. Kuzmin, P. A. Kosintsev, M. Lázničková-Galetová, C. Leduc, P. Nikolskiy, M. Nussbaumer, C. O’Drisceoil, L. Orlando, A. Outram, E. Y. Pavlova, A. R. Perri, M. Pilot, V. V. Pitulko, V. V. Plotnikov, A. V. Protopopov, A. Rehazek, M. Sablin, A. Seguin-Orlando, J. Storå, C. Verjux, V. F. Zaibert, G. Zazula, P. Crombé, A. J. Hansen, E. Willerslev, J. A. Leonard, A. Götherström, R. Pinhasi, V. J. Schuenemann, M. Hofreiter, M. T. P. Gilbert, B. Shapiro, G. Larson, J. Krause, L. Dalén, P. Skoglund, Grey wolf genomic history reveals a dual ancestry of dogs. Nature 607, 313–320 (2022).
8
J. Ramos-Madrigal, M.-H. S. Sinding, C. Carøe, S. S. T. Mak, J. Niemann, J. A. Samaniego Castruita, S. Fedorov, A. Kandyba, M. Germonpré, H. Bocherens, T. R. Feuerborn, V. V. Pitulko, E. Y. Pavlova, P. A. Nikolskiy, A. K. Kasparov, V. V. Ivanova, G. Larson, L. A. F. Frantz, E. Willerslev, M. Meldgaard, B. Petersen, T. Sicheritz-Ponten, L. Bachmann, Ø. Wiig, A. J. Hansen, M. T. P. Gilbert, S. Gopalakrishnan, Genomes of Pleistocene Siberian wolves uncover multiple extinct wolf lineages. Curr. Biol. 31, 198–206.e8 (2021).
9
A. G. Drake, M. Coquerelle, G. Colombeau, 3D morphometric analysis of fossil canid skulls contradicts the suggested domestication of dogs during the late Paleolithic. Sci. Rep. 5, 8299 (2015).
10
L. A. A. Janssens, M. Boudadi-Maligne, D. F. Lawler, F. R. O’Keefe, S. van Dongen, Morphology-based diagnostics of “protodogs.” A commentary to Galeta et al., 2021, Anatomical Record, 304, 42-62, doi: 10.1002/ar.24500. Anat. Rec. (Hoboken) 304, 2673–2684 (2021).
11
M. Boudadi-Maligne, G. Escarguel, A biometric re-evaluation of recent claims for Early Upper Palaeolithic wolf domestication in Eurasia. J. Archaeol. Sci. 45, 80–89 (2014).
12
C. Brassard, A. Bălăşescu, R.-M. Arbogast, V. Forest, C. Bemilli, A. Boroneanţ, F. Convertini, M. Gandelin, V. Radu, P. A. Fleming, C. Guintard, T. L. Kreplins, C. Callou, A. Filippo, A. Tresset, R. Cornette, A. Herrel, S. Bréhard, Unexpected morphological diversity in ancient dogs compared to modern relatives. Proc. Biol. Sci. 289, 20220147 (2022).
13
A. Evin, L. Bouby, V. Bonhomme, A. Jeanty, M. Jeanjean, J.-F. Terral, Archaeophenomics of ancient domestic plants and animals using geometric morphometrics: A review. Peer Community J. 2, e27 (2022).
14
A. G. Drake, C. P. Klingenberg, Large-scale diversification of skull shape in domestic dogs: Disparity and modularity. Am. Nat. 175, 289–301 (2010).
15
A. V. Schweizer, R. Lebrun, L. A. B. Wilson, L. Costeur, T. Schmelzle, M. R. Sánchez-Villagra, Size Variation under Domestication: Conservatism in the inner ear shape of wolves, dogs and dingoes. Sci. Rep. 7, 13330 (2017).
16
A. Evin, T. Cucchi, A. Cardini, U. Strand Vidarsdottir, G. Larson, K. Dobney, The long and winding road: Identifying pig domestication through molar size and shape. J. Archaeol. Sci. 40, 735–743 (2013).
17
A. Evin, L. G. Flink, A. Bălăşescu, D. Popovici, R. Andreescu, D. Bailey, P. Mirea, C. Lazăr, A. Boroneanţ, C. Bonsall, U. S. Vidarsdottir, S. Brehard, A. Tresset, T. Cucchi, G. Larson, K. Dobney, Unravelling the complexity of domestication: A case study using morphometrics and ancient DNA analyses of archaeological pigs from Romania. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20130616 (2015).
18
J. Peters, B. S. Arbuckle, N. Pöllath, Subsistence and beyond: Animals in Neolithic Anatolia. The Neolithic in Turkey 6, 135–203 (2014).
19
M. Germonpré, M. V. Sablin, R. E. Stevens, R. E. M. Hedges, M. Hofreiter, M. Stiller, V. R. Després, 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 (2009).
20
N. D. Ovodov, S. J. Crockford, Y. V. Kuzmin, T. F. G. Higham, G. W. L. Hodgins, J. van der Plicht, A 33,000-year-old incipient dog from the Altai Mountains of Siberia: Evidence of the earliest domestication disrupted by the Last Glacial Maximum. PLOS ONE 6, e22821 (2011).
21
S. V. Oshibkina, Mezolit Vostochnogo Prionezh’ya. Kul’tura Veret’e (Mesolithic of the Eastern Onega Region. The Veretye Culture) (Nauka, 2006).
22
V. G. Childe, The Mesolithic and neolithic in northern Europe. Man 43, 34 (1943).
23
R. J. Losey, T. Nomokonova, E. Guiry, L. S. Fleming, S. J. Garvie-Lok, A. L. Waters-Rist, M. Bieraugle, P. Szpak, O. P. Bachura, V. I. Bazaliiskii, N. E. Berdnikova, N. G. Diatchina, I. V. Frolov, V. V. Gorbunov, O. I. Goriunova, S. P. Grushin, A. V. Gusev, L. G. Iaroslavtseva, G. L. Ivanov, A. V. Kharinskii, M. V. Konstantinov, P. A. Kosintsev, E. V. Kovychev, B. Lazin, I. G. Nikitin, D. V. Papin, A. N. Popov, M. V. Sablin, N. A. Savel’ev, A. B. Savinetsky, A. A. Tishkin, The evolution of dog diet and foraging: Insights from archaeological canids in Siberia. Sci. Adv. 8, eabo6493 (2022).
24
J. A. Leonard, C. Vilà, K. Fox-Dobbs, P. L. Koch, R. K. Wayne, B. Van Valkenburgh, Megafaunal extinctions and the disappearance of a specialized wolf ecomorph. Curr. Biol. 17, 1146–1150 (2007).
25
A. Perri, C. Widga, D. Lawler, T. Martin, T. Loebel, K. Farnsworth, L. Kohn, B. Buenger, New evidence of the earliest domestic dogs in the Americas. Am. Antiq. 84, 68–87 (2019).
26
F. A. da Silva Coelho, S. Gill, C. M. Tomlin, T. H. Heaton, C. Lindqvist, An early dog from southeast Alaska supports a coastal route for the first dog migration into the Americas. Proc. Biol. Sci. 288, 20203103 (2021).
27
A. Perri, A wolf in dog’s clothing: Initial dog domestication and Pleistocene wolf variation. J. Archaeol. Sci. 68, 1–4 (2016).
28
M. Zelditch, D. L. Swiderski, H. David Sheets, Geometric Morphometrics for Biologists: A Primer (Academic, ed. 2, 2012).
29
A. Turner, Large carnivores and earliest European hominids: Changing determinants of resource availability during the Lower and Middle Pleistocene. J. Hum. Evol. 22, 109–126 (1992).
30
C. Dufresnes, C. Miquel, N. Remollino, F. Biollaz, N. Salamin, P. Taberlet, L. Fumagalli, Howling from the past: Historical phylogeography and diversity losses in European grey wolves. Proc. Biol. Sci. 285, 20181148 (2018).
31
H. Harbers, D. Neaux, K. Ortiz, B. Blanc, F. Laurens, I. Baly, C. Callou, R. Schafberg, A. Haruda, F. Lecompte, F. Casabianca, J. Studer, S. Renaud, R. Cornette, Y. Locatelli, J.-D. Vigne, A. Herrel, T. Cucchi, The mark of captivity: Plastic responses in the ankle bone of a wild ungulate (Sus scrofa). R. Soc. Open Sci. 7, 192039 (2020).
32
K. A. Lord, G. Larson, R. G. Allaby, E. K. Karlsson, A universally applicable definition for domestication. Proc. Natl. Acad. Sci. U.S.A. 122, e2413207122 (2025).
33
G.-A. Lee, S. Bestel, Contextual analysis of plant remains at the Erlitou-Period Huizui site, Henan, China. Bull. Indo-Pac. Prehistory Assoc. 27 (2007).
34
J. Claude, Morphometrics with R. Use R! (Springer, 2008).
35
S. Schlager, “Morpho and Rvcg - Shape Analysis in R” in Statistical Shape and Deformation Analysis, G. Zheng, S. Li, G. Szekely, Eds. (Academic Press, 2017), pp. 217–256.
38
M. L. Collyer, D. C. Adams, RRPP: An r package for fitting linear models to high-dimensional data using residual randomization. Methods Ecol. Evol. 9, 1772–1779 (2018).
39
M. Baylac, M. Friess, “Fourier descriptors, procrustes superimposition, and data dimensionality: An example of cranial human populations” in Modern Morphometrics in Physical Anthropology, D. F. Slice, Ed. (Springer Nature, 2005), pp. 145–165; 10.1007/0-387-27614-9_6.
40
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).
41
Y. Benjamini, Y. Hochberg, Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289–300 (1995).